Course Handout - From Frontal Lobe Syndrome to Dysexecutive Syndrome

Copyright Notice: This material was written and published in Wales by Derek J. Smith (Chartered Engineer). It forms part of a multifile e-learning resource, and subject only to acknowledging Derek J. Smith's rights under international copyright law to be identified as author may be freely downloaded and printed off in single complete copies solely for the purposes of private study and/or review. Commercial exploitation rights are reserved. The remote hyperlinks have been selected for the academic appropriacy of their contents; they were free of offensive and litigious content when selected, and will be periodically checked to have remained so. Copyright © 2010, High Tower Consultants Limited.

 

First published online 08:59 GMT 13th March 2003, Copyright Derek J. Smith (Chartered Engineer). This version [HT.11 - reinstate lost links] dated 18:00 8th December 2010

 

The skeleton of this material previously appeared in Smith (1996; Chapter 5). It is repeated here with major extensions and supported with hyperlinks.

 

1 - Frontal Lobe Neuroanatomy

From the highest primate to the lowliest invertebrate, the nervous system has sustained the animal kingdom against predation and environmental hazard for around half a billion years, and this, in vertebrates, has meant reliance on progressive specialisation of the brain as ganglion-in-chief of an axially elongated and segmented system. Admittedly, a lot of sensory information is processed at the various segments of the spinal cord, but this is only for reflex or biomechanical purposes (balance, say, or multiple limb coordination), and as soon as any "higher function" is needed the information is routed instead "rostrally" - forwards - to the brain. This basic set-up was already well known by the early 19th century, being seen, for example, in Bell and Magendie's analysis of the sensory and motor roots of the peripheral nerves [check it out]. However, the brain also has evolutionary layers within itself, being traditionally divided into brainstem, midbrain, and forebrain, and one popular way to think about this is to adopt the concept of the "triune" (that is to say, three-in-one) brain .....

Key Concept - The Triune Brain: A number of useful neuroanatomical names derive from the order of evolutionary emergence of the structures in question, that is to say, from phylogenetic considerations. These are the terms palaeocortex ("ancient cortex"), archicortex ("old cortex") [the term archipallium ("old cloak") is also often seen], and neocortex ("new cortex") [the term neopallium ("new cloak") is also often seen, and is in fact more accurate because the term cortex, strictly speaking, refers solely to the surface grey matter of the cerebrum, not to its overall bulk]. The palaeocortex is the hippocampal gyrus, a gyrus which in humans is situated on the medial surface of the temporal lobe. Historically, it was the first cortex to emerge, and was probably olfactory in function. The archicortex is the hippocampus, an important nucleus which in humans is situated deep within the temporal lobe. It was the next area of cortex to emerge, and was "largely concerned with the integration of information from different sensory modalities" (Rose, 1976, p169). The neopallium is the rest of the cerebrum, and, in humans, includes by far the largest area of cortex. Considerations of this sort prompted the neurologist Paul MacLean to distinguish between (1) what he called "the reptilian brain", the most primitive structures of the brainstem, midbrain, and cerebellum, (2) the "limbic system", the phylogenetically more recent structures of the diencephalon and archicortex, and (3) the neopallium, the most recent addition of all.

Here are the main components of the forebrain, set in the broader context of the main divisions of the central nervous system .....

Figure 1 - Structures of the Forebrain: Here is a tree-structured analysis showing the component structures of the vertebrate brain, and with conventional neuroanatomical naming shown in black. MacLean's reptilian brain is then indicated by the tan highlighting, and his limbic brain by the mauve highlighting. Structures not specifically highlighted make up the neopallium, that is to say, the neocortex, its underlying white matter, and the basal ganglia.

FLOBES-fig1.gif

Simplified from a black-and-white original in Smith (1997c; Figure 1.4). This graphic Copyright © 2003-2004, Derek J. Smith.

The gradual development of rostral processing power during evolution is often referred to as "encephalisation", and there is a logical pattern to what happens as you move up through the animal kingdom, because brain anatomy simply follows lifestyle demand. Thus species which need sharp eyes (eg. eagles) grow large eyes and "visual brains", those which need acute hearing (eg. bats) grow large ears and "auditory brains", and those which need an acute sense of smell (eg. fish, reptiles, and lower mammals such as rodents) develop extensive olfactory cortex and exhibit behaviour driven in large part by the sense of smell. Those, on the other hand, which need to be flexible and solve problems develop the "uncommitted cortex" needed to support the necessary higher functions. It is therefore commonly accepted that the best indicator of brain power is forebrain development in general, and frontal lobe development in particular. Primates, for example, have been large-brained throughout their known history (Jerison, 1987), and the highest grade of encephalisation is shared by humans and cetaceans (dolphins). Figure 2 shows some of the steps on the evolutionary ladder leading ultimately to H. sapiens, and Figure 3 shows the basics of human frontal lobe neuroanatomy .....

Figure 2 - Evolution of the Vertebrate Cerebrum: This diagram shows the schematised brain anatomy of (a) fish, (b) reptile, (c) bird, (d) small mammal, (e) large mammal (non-primate), and (f) primate. Note the progressive growth of the cerebrum (grey) with respect to both midbrain and hindbrain. Note the close association of olfactory bulb with palaeocortex and optic tract with optic tectum (only really visible in specimens (a) to (c)), and that this, given the known motor functions of the cerebellum, leaves little room for any behaviour other than sniffing, seeing, and locomotion in animals (a) to (d). Only with the development of "uncommitted cortex" (see text) is there brainpower to spare for more complicated types of cognition. To cut a long story short, the key product of encephalisation is the "forebrain", comprising the lobes and lobules of the cerebral hemispheres, together with the underlying basal ganglia and the mass of axon tracts which allow these components to function as an integrated information processing whole. And the jewels in the forebrain's crown are the frontal lobes, which in humankind comprise the most rostral 40% of the cerebral hemispheres, anterior to the Rolandic Fissure. Brodmann (1912) estimated that the prefrontal cortex constitutes 29% of the total cortex in man, 17% in chimpanzees, 11.5% in gibbons, and 8.5% in lemurs.

FLOBES-fig2.gif

Redrawn from a black-and-white original in Smith (1997c; Figure 1.7). This graphic Copyright © 2003-2004, Derek J. Smith.

 

Figure 3 - Frontal Lobe Neuroanatomy: Here is a left lateral view of the undissected left frontal lobe. The precentral [or "Pre-Rolandic"] gyrus [red stipple] is primary motor area, and the band of superior, middle, and third frontal gyri in front of that [blue stipple] is supplementary motor area. The remainder of the superior and middle frontal gyri [white stipple] is known as the "prefrontal region". It is generally involved in managing the activity of the more caudal areas, and is specifically responsible for such higher cognitive processes as forward planning and directed attention. The orbital cortex [bottom centre] is so named because it is situated just above the orbit of the eye. [For the corresponding Brodmann's Numbers, and an indication of the layout of the medial aspect of the cerebral hemispheres, see Kleist (1934).]

FLOBES-fig3.gif

Redrawn from a black-and-white original in Smith (1997c; Figure 2.1). This graphic Copyright © 2003-2004, Derek J. Smith.

2 - Frontal Lobe Syndrome

So what happens when frontal lobe structures are damaged by injury or disease? Well one of the earliest accounts of a frontal lobe lesion is Bigelow's (1850) description of the brain-injured American railway labourer Phineas P. Gage [timeline; other sources], who suffered pronounced personality changes after an accidental prefrontal leucotomy. This was followed by investigations of deliberately inflicted frontal lesions in animals by the likes of Fritsch and Hitzig (1870) and Ferrier (1876/1886), and shortly after that by the pioneer attempts at "psychosurgery", that is to say, human brain surgery performed expressly for the purpose of alleviating psychological (rather than medical) symptoms.

The first planned (as opposed to accidental) attempts at psychosurgery were carried out by Gottlieb Burckhardt on 29th December 1888, and first reported in 1891. Burckhardt carried out various unilateral cortical lesions on a series of six institutionalised psychiatric patients with "not spectacular" results. The idea was then resurrected following the International Neurological Congress in London in July 1935 at which the comparative psychologists John F. Fulton and Carlyle Jacobsen reported on the removal of the frontal cortex in chimpanzees, one of whom - an animal called Becky - had been cured of a particularly temperamental disposition by the procedure [much as the fictitious Randall P. McMurphy was "cured" of loving life just a bit too much in the movie One Flew Over the Cuckoo's Nest]. In short, "the animal without its frontal areas no longer appears to 'worry' over mistakes" (Jacobsen, 1936). Jacobsen also cited the earlier work by Ferrier (1876/1986) to the effect that removal of the frontal lobes (again in monkeys) caused no impairment of the "special sensory or motor faculties", but "very decided" alterations in the animals' character and behaviour. Thus .....

"Instead of, as before, being actively interested in their surroundings, and curiously prying into all things that came within the field of their observation, they remained apathetic and dull, or dozed off to sleep []. While not actually deprived of intelligence, they had lost, to all appearance, the faculty of attentive and intelligent observation." (Ferrier, 1876, pp231-232.)

Italy's Leonardo Bianchi (1848-1927) was another early student of the effects of frontal lobe ablation in monkeys and dogs, and concluded from his observations that the frontal lobes were more than centres of attention .....

"The frontal lobes are the seat of coordination and fusion of the incoming and outgoing products of the several sensory and motor areas of the cortex" (Bianchi, 1895, p34).

This, of course, was classic encephalisation restated, but Bianchi was then more precise in 1922, when he summarised the animal studies as showing five areas of frontal deficit, as follows .....

  1. Loss of "perceptive power", leading to defective attention and object recognition.
  2. Reduction in memory.
  3. Reduction in "associative power", leading to lack of coordination of the individual steps leading towards a given goal, and thus to severe difficulty solving anything but the most simple problem.
  4. Altered emotional attachments, leading to serious changes in "sociality" [one of the main aspects of Phineas Gage's post-traumatic behaviour].
  5. Disruption of focal consciousness and purposive behaviour, leading to apathy and/or distractibility [one of the main aspects of Becky's post-operative behaviour].

The point was that Bianchi's (1922) five areas of deficit usually tended to co-occur, more or less, in patient after patient and therefore qualified for the medical descriptor "syndrome", and so "frontal lobe syndrome" was born.

3 - Frontal Lobe Psychosurgery

Meanwhile, one of the other delegates to the 1935 London conference, the Portuguese neurosurgeon Antonio Egas Moniz (1874-1955), had returned to Lisbon and in September 1935, in conjunction with his colleague Almeida Lima, had pioneered the deliberate "prefrontal lobotomy" on humans in an attempt to alleviate the symptoms of psychoticism. Moniz's belief (based upon the earlier studies) was that psychotic behaviour patterns (especially fixedness, repetitiveness, and over-emotionality) were the result of abnormal brain activity, and so he developed a technique to destroy "the more or less fixed arrangements of cellular connections that exist in the brain, and particularly those which are related to the frontal lobes". This involved surgically removing or destroying ("ablating") the prefrontal region (the lobotomy proper), or at least severing the association tracts linking this region to the rest of the brain (a leucotomy or tractotomy). According to Youngson and Schott (1996), Moniz's initial female patient was less agitated and overtly paranoid after the operation than she had been before it, but more disoriented and apathetic than expected.

Despite the fact that the results of Moniz's first attempt at this procedure were not wholly conclusive, the method was quickly introduced into the United States by Walter J. Freeman (1895-1972) and James Watts. They carried out their first operation on 14th September 1936 on a 63-year old woman, and found a striking decrease in her levels of agitation and fearfulness. Freeman and Watts proudly publicised their procedure, and thanks to an initially positive press it rapidly became hugely popular. During the 1940s, around 50,000 patients were lobotomised in the United States alone (Restak, 1973). "Freeman, a lobotomy zealot, calculated he had personally performed over 4000 operations, using a gold-plated ice pick" (Restak, 1973). There was also the Freeman-Watts standard lobotomy and the slightly later Freeman transorbital lobotomy. The effective instrument in this latter routine was a standard kitchen icepick. This is driven 5 cm up through the roof of the eye socket with a light tap from a mallet, and then rocked to and fro [picture] to sever the frontal white matter from beneath ["it goes through just like soft butter," said Watts].

ASIDE: Freeman seems to have been a bit of a psychosurgery zealot - Youngson and Schott (1996) mischievously suggest that he would cheerfully have used a food mixer to do the job had one been handy!

Following surgery, patients did indeed become less anxious and withdrawn, although their intellectual level remained ostensibly unchanged. Particularly good results were obtained in cases of paranoia, catatonia, and simple schizophrenia. Side-effects of the surgery included loss of community consciousness and feeling for others, cessation of dreaming, complacency, placidity, loss of initiative, apathy, loss of concentration, loss of enthusiasm for life, and reduced creativity and artistic expression. Also - since surgery reduced disruptive emotional responses - the ability to interact socially tended to return. Sadly, there was also a removal of social inhibitions, leading to insensitivity to criticism, unrestrained exposure, or depressed table manners. In other words, social interaction was not actually any the more meaningful, but there was far less worry on the part of the patient whether it was or not. As to why this effect should be seen, Denny-Brown (1951) describes frontal polar cortex as having small cells, a thick internal granular layer, and "an almost exclusive connection with the dorsomedial nucleus of the thalamus" (p400). It is therefore in close communication with what is known as the "limbic system", and thus with the full range of the brain's emotional and motivational systems. The prefrontal region in general is commonly linked with such functions as problem solving, behaviour planning, working memory [glossary], and eye movements. It is the more ventrally placed orbital cortex which is involved in personality and social behaviour.

And as to the procedures themselves, a number of variants soon emerged, two of which were compared by Petrie (1952). In what he termed the bilateral standard operation, an incision was made 3 cm behind the lateral margin of the orbit and 5-6 cm above the zygoma. A 1 cm burr-hole was then drilled through the skull, and the dura mater cut through and folded back. Finally, a needle was pushed down through the exposed cortex and rocked to and fro through the underlying white matter. In the bilateral rostral operation, the needle is angled more obliquely forwards. The standard procedure thus isolates Areas 9, 10, 11, 46, 47, and possibly part of Area 45, whilst the rostral procedure isolates only Areas 9 and 10 - the prefrontal cortex proper - and leaves the orbital cortex relatively intact [compare the two top arrows on Figure 4]. However, with deteriorating press and the discovery of chlorpromazine antidepressant drugs in 1952, the numbers started to fall. By the 1950s, psychosurgery had whipped up a storm of objections on a variety of grounds, not least the difficulty in obtaining genuinely informed medical consent in such circumstances [see Restak (op cit) for details]. The economics were another cause of overeagerness to operate - the lobotomies cost $250 and needed to be carried out only once, whereas the costs of institutionalisation were over $35,000 per patient per annum. There were also further improvements in technique, so that the surgery involved gradually became less extensive. Knight (1966) reviewed many tractotomies and concluded that the most effective lesion site was in a relatively small bundle of the thalamocortical tract as it passes beneath the head of the caudate nucleus level with Area 13. He developed a procedure known as the restricted undercut specifically to attack this tract and this tract alone (for details of which, see Blakemore, 1977, p181). The most modern methods are assisted by three-dimensional computer imaging of the patient's brain. Electrodes are positioned using an externally mounted stereotaxic frame, and the lesions produced either by electro-coagulation or minute radioactive implant. Lesions can therefore be placed very precisely and extend only a few millimetres. This allows what Girgis (1971) describes as "unnecessary encroachment" upon uninvolved cortex to be more or less totally avoided. The target area is still the orbital cortex, although Brian Simpson of University Hospital Wales now attacks the thalamocortical tract very early on, while it is still within the anterior parts of the internal capsule (Simpson, 1996). Bridges (1996) reports that between 20 and 30 procedures are currently carried out annually in Britain, mainly for depression or obsessive anxiety.

Figure 4 - Frontal Lobe Psychosurgery: Here is Figure 3 again, overprinted now with the appropriate Brodmann's Numbers and locating the various psychosurgical procedures described in the text. Each arrow shows the point of entry of the instrument and the plane of the resulting lesion. The Knight restricted undercut is shown as a double-headed arrow to reflect the fact that the instrument enters laterally and is rocked up and down. Note how the Freeman transorbital technique involves penetrating the orbital cortex from below. Note also how the later procedures concentrate on orbital cortex rather than prefrontal, and in this respect note carefully the position of Area 13, as implicated by the Knight (1966) report.  [For a more complete display of the Brodmann's Numbers, and an indication of the layout of the medial aspect of the frontal lobes, see Kleist (1934).]

FLOBES-fig4.gif

Redrawn from a black-and-white original in Smith (1997c; Figure 3.8). This graphic Copyright © 2003-2004, Derek J. Smith.

4 - Causes of Frontal Lobe Lesions

Apart from taking its fair share of the brain's normal exposure to cerebrovascular and space occupying lesions, the frontal lobes are at risk in multiple sclerosis, Huntington's disease, Alzheimer's disease, and the normal ageing process (Stuss and Benson, 1986). They are also regularly involved in traumatic brain injury, partly for the simple reason that they are frontal and therefore take the brunt of any forward collision impact, and partly because the orbital region is close to the relatively sharp contours of the bones of the orbit. [For further details, including a brief animation of the coup/contre-coup effect in closed head injury (CHI), click here.]

Another not uncommon cluster of frontal lobe lesions arises following haemorrhage of the anterior communicating artery (ACoA), that part of the circle of Willis which connects the two anterior cerebral arteries just anterior to the optic chiasm. According to Parkin and Leng (1993), the ACoA is curiously prone to the development of aneurisms, and when such aneurisms rupture they reduce the supply to the basal forebrain, the septal area, and the anterior portions of the cingulate gyrus, fornix, hypothalamus, and corpus callosum. As to the resulting clinical picture, Parkin and Leng (1993) summarise a number of separate case reports and report a severe confusional state, attention problems, severe retrograde amnesia, and misorientation to an earlier time period. Language and general knowledge are unaffected, and recognition memory seems to be relatively well preserved compared to recall. Confabulation (discussed in detail in Section 9) is common, as in Kapur and Coughlan's (1980) ACoA patient SB .....

"He would claim, first thing in the morning, to have fictitious business appointments, when in fact he was attending a day centre, and would frequently dress for dinner in the evening in the mistaken belief that guests were coming. He would also attempt to take cups of tea outside, saying that these were for his foreman, who had discontinued employment with him several years earlier." (Kapur and Coughlan, 1980, p461)

5 - Early Attempts at Assessing Frontal Lobe Function

All in all, therefore, frontal amnesias turned out to be neither as immediately obvious nor as clinically clear-cut as those arising from temporal lobe damage, and neither memory nor intelligence tests, generally speaking, were particularly good at detecting frontal lobe damage. Because of this, clinical neuropsychologists devised their own special "frontal lobe tasks", or "frontal batteries", that is to say, tests designed to be selectively sensitive to frontal lobe damage. One of the first to do this was Rieger (1888, cited in Benton, 1994), who assembled a battery of 40 tests of cognitive abilities. The early clinicians were further assisted by a steady stream of focal brain injury cases from the battlefields of the First World War, and this tragic caseload eventually became the subject of several influential post-war reviews. The British neurologist Sir Henry Head (1861-1940) used such data in his monograph, "Aphasia and Kindred Disorders of Speech" (Head, 1926), as did the German military surgeons Poppelreuter, Feuchtwanger, and Kleist. Feuchtwanger (1923) reviewed 200 cases of frontal injury, reporting the usual curious combination of preserved intelligence and memory with impaired application and social inappropriacy. Kleist (various to 1934) did likewise, and drew up a detailed functional mapping of the cerebrum on the strength of his observations [check it out].

One of the earliest surviving assessments from this period is the Porteus Maze, developed as a psychometric test of intelligence in 1914 by Stanley Porteus of the University of Hawaii, and in constant use ever since [Porteus himself summarised his lifetime's work in Porteus (1950)]. The technique addresses the logically opposed hypothetical constructs of "planfulness" and "impulsiveness", and is scored by counting the number of false trails on the response sheet. Another early test was devised by John Ridley Stroop (1897-1973), and requires subjects to name the ink colours used when reading printed stimulus words (Stroop, 1935). Thus the correct answer for the stimulus <walk> is "red", not "walk". The problem is that reading printed words is a very automatic act in appropriately trained adult subjects, and so there is an "attentional conflict" situation (Pardo et al, 1990), in which the response of first impulse needs to be consciously suppressed in favour of the colour-response. Even more interference comes when the printed words are themselves colour names, but not matching the ink colour. The Stroop test is valuable as a clinical screening tool because brain injury - and specifically frontal brain injury - renders patients less able to control this interference, whereupon they respond automatically. The test has been in constant use ever since it was first introduced, and the latest research regularly implicates the anterior cingulate gyrus in the selection of the appropriate response under conditions of doubt (see, for example, Pardo et al, 1990). Try this for yourself: read the following ink colours out loud as fast as you can .....

BLUE

YELLOW

GREEN

RED

PURPLE

BROWN

Another type of test involves "category sorting". The first to make his name here was Egon Weigl (Weigl, 1927/1941), who had been investigating his patients' ability to sort coloured wool samples when he noted some strange idiosyncrasies, thus .....

"The patients have no principle of classification such as is formed in categorial [sic] behaviour. The primitive concrete behaviour of patients was demonstrated in a particularly instructive way in the following experiment. They were given three colours and told to place the two together which were 'most alike'. Whether or not the desired result was apparently obtained depended on the way the colours were combined. Thus, for example, the patient Th. [sic], when presented with a dark red, a pink, and a medium brown skein, reacted in the way intended by the experimenter; that is, he put the two reddish skeins together. If, however, he was given a sky blue skein instead of the medium brown one, the patient usually could not decide at all, because, for him, the paleness of the sky blue and of the pink 'cohered' as much as the two variants of [red]. [.....] We are dealing with a pathological change in these patients which is connected with the problem of so-called 'isolating abstraction'." (Weigl, 1927/1941, p5; italics original.)

But it was not just failures of abstraction which impaired the sorting performance of frontal patients. They also typically showed "perseveration" [glossary], an inability to cancel one sorting strategy in favour of an alternative one when circumstances or instructions required it. Weigl therefore developed a more compact version of the test, using simple cardboard shapes rather than skeins of wool, thus .....

"The patient was presented with 12 unarranged cardboard figures of different colour and form: four equilateral triangles (red, green, yellow, blue), four squares (red, green, yellow, blue), four circles (red, green, yellow, blue). He was told to sort them. The patient carried out the task as follows: First he put together a red triangle, a red circle, and a red square in a vertical row. Similarly he put together the yellow, green, and blue figures, so that as a result a series of rows, one red, one yellow, one green, one blue, lay next to each other a few centimetres apart." (Weigl, 1941, p9; italics original.) [Subsequent revisions of the test use 20 counters and vary thickness, size, and overprinted shape as well.]

ASIDE - WEIGL AND TRANSCODING: In a later paper (Weigl, 1974), Weigl was one of first to use the term "transcoding" to describe the process of recoding information in transit through the cognitive system, specifically from spoken to written language form and back again. For more on the transcoding model genre within psycholinguistics, see our e-paper on "The Transcoding Model Series".

Another testing pioneer was Ward C. Halstead (1908-1968), of the University of Chicago Medical School. In Halstead (1940), for example, he exposed patients to a display of common objects and invited them to sort them into piles on the basis of their similarity. He then scored omissions and idiosyncrasies as evidence of underlying pathology. Other tests were added in Halstead (1947), and further improvements were then made by Ralph M. Reitan, so that the modern form of the battery is the Halstead-Reitan Battery (Reitan, 1955). This test package is still on the market, published by the Reitan Neuropsychology Laboratories at the University of Arizona [check it out].

Despite these early developments, not every clinician found the available tests useful. For example, Hebb and Penfield (1940) reported their examination of patient KM, a 27-year-old right-handed male who had suffered a depressed fracture of the frontal bone in a workplace accident in 1928. This had left him subject to post-traumatic epilepsy, and in 1938 it was decided to operate to remove the irritant intracranial scar tissue which was causing his fits. The resulting partial bilateral frontal lobotomy removed "one third of the mass of the frontal lobes" (p427) [approximately the white stippled area in Figure 3]. Here are some observations from the subsequent case notes .....

"The patient was conscious and cooperative throughout. After the surgical removal had been completed it was desired to put the patient to sleep [and] during the introduction of the tube the patient made inappropriately facetious remarks" (p425).

"On the tenth day after operation the patient was again responsive, but was disoriented, irrational, and slightly facetious and used obscene language" (p426).

"Immediately before operation the patient was examined with the revised Standford-Binet and the McGill revision of the army beta test. Two months after operation he was [re-examined]. The preoperative intelligence quotient was 83 [and] postoperative scores were consistently higher" (p431). [In fact, there was a 13-month improvement of 11 IQ points.]

"The important fact is the absence of grossly pathologic defects and of 'frontal lobe signs'. [.....] There seems also to be little question of 'loss of abstract behaviour' [citation]. No difficulty in categorising was found on a sorting test" (pp433-434).

 "For the effect of lesions of the frontal lobe on human intelligence, it seems that one will have to look elsewhere than to clinical observation or ratings by intelligence tests such as are now available" (p437).

Nevertheless, most reviewers in that era were continuing to side with Bianchi .....

"..... patients with frontal lobe lesions or destruction of a frontal lobe by an operation are changed in a characteristic way in their behaviour in everyday life. Their mental capacity may be sufficient for executing routine work but they lack initiative, foresight, activity, and ability to handle new tasks." (Goldstein, 1944, p192; italics original)

Another sorting task, the Wisconsin Card Sorting Test (WCST) [glossary] was developed in 1948 (Berg, 1948; Grant and Berg, 1948), and subsequently modified in 1976 as the MCST [glossary] (Nelson, 1976). The effect of brain lesions on WCST performance was then summarised by Brenda Milner of the Montreal Neurological Institute .....

"The results of the present study provide strong support for the view that the ability to shift from one mode of solution to another on a sorting task is more impaired by frontal than by posterior cerebral injury [.....] all removals which encroached upon the superior frontal region were associated with poor performance on the sorting test. The critical lesion cannot be more precisely defined, although area 9 of Brodmann was implicated in most cases. [.....] The impairment shown by patients after frontal lobectomy reveals itself as a strong perseverative tendency. In extreme cases, a patient may sort all 128 cards to one preferred category (for example form), despite the experimenter repeatedly telling him that his responses are wrong. When the sorting is done rapidly, the patient may not even wait for the experimenter to say 'right' or 'wrong', before proceeding to place the next card. In such cases, it is tempting to argue that the main defect is motivation [but] one can see the same perseverative behaviour in patients who work slowly, pausing between cards, and who become manifestly distressed by the frequency of their errors." (Milner, 1963, pp96-97.)

Milner and Petrides (1984) report further experience with this test, as follows .....

"Although patients with frontal lobe lesions respond normally to environmental stimuli, they appear to have difficulty in using these stimuli to regulate their actions. A clear example of this is provided by the performance of such patients on [the WCST, where] the impairments observed after a frontal-lobe lesion appear to stem from the patient's inability to overcome previously established response tendencies, resulting in the generation of fewer hypotheses and, frequently, in a high incidence of errors including perseveration." (Milner and Petrides, 1984, p405.)

..... and it was this inability to regulate their actions which led Katz, Ford, Moscowitz et al (1963) to develop the Activities of Daily Living (ADL) test [glossary], and Lawton and Brody (1969) to add the Instrumental Activities of Daily Living (IADL) test.

Other authors, meanwhile, were still trying to get to the bottom of the frontal lobes' role in cognition.  Luria and Homskaya (1964), for example, took an analytical eye to the classic symptomatology of frontal lobe syndrome and managed to reduce Bianchi's five areas of deficit [see Section 2] to just two, thus ..... 

"Disturbances occurring after lesions of the frontal lobes often manifest themselves as two basic symptoms: loss of spontaneity or initiative, and lack of critical attitude toward the results of one's own behaviour. [.....] The latter symptom [can] be regarded as the result of a general loss of some feedback mechanism, a disturbance in signals of error, or an inadequate evaluation of the patient's own action. It can be reduced to a deficit in matching of action carried out with the original intention [.....] the patient with severe frontal lobe lesions becomes unable to evaluate the adequacy of his own action, does not try to modify his behaviour when it fails, and remains satisfied with his own actions no matter how ineffective they may be." (Luria and Homskaya, 1964, pp373-374; bold emphasis added.)

Milner was also instrumental in introducing the Corsi blocks tasks [glossary] (Milner, 1971). The Corsi task is regularly used in cognitive research (Berch, Krikorian, and Huha, 1998, go so far as to describe it as "arguably the single most important nonverbal task in neuropsychological research"), and has recently been analysed for its consumption of working memory [glossary] resources (see, for example Vandieronck et al, 2004).

The year 1971 also saw a major theoretical review by Walle J.H. Nauta at MIT, who homed in on the frontal lobes' involvement in the process we now know as "motor programming" .....

"The frontal lobe, despite decades of intensive research by physiologists, anatomists, and clinicians, has remained the most mystifying of the major subdivisions of the cerebral cortex. Unlike any other of the great cerebral promontories, the frontal lobe appears not to contain a single sub-field that can be identified with any particular sensory modality, and its entire expanse must accordingly be considered association cortex [loss of which] leads to a complex functional deficit, the fundamental nature of which continues to elude laboratory investigators and clinicians alike. [.....] It is clear [that] the frontal lobe disorder is characterised foremost by a derangement of behavioural programming. One of the essential functional deficits of the frontal lobe patient appears to be in an inability to maintain in his behaviour a normal stability-in-time: his action programs, once started, are likely to fade out, to stagnate in reiteration, or to become deflected away from the intended goal." (Nauta, 1971, pp167-171.)

Just such a derangement of behavioural programming can also be seen in the following clinical anecdote .....

"If the patient's hands are lying on top of his blanket, he can respond to the command 'Lift the hand' without difficulty. However, during the performance of the second or third trial, symptoms of inactivity may appear; the movements slow down, the hands are not lifted as high, and after several repetitions of the orders the movements may be fully discontinued.  Now let us repeat the same experiment under different conditions. This time, the hands of the patient (with a massive bilateral lesion of the frontal lobes) are under the blanket; in order to execute the instruction, 'lift the hand', he must perform a complex series of movements. First, he must free his hand from under the blanket, and only then can he lift it. It should be pointed out that the first part of this program was not mentioned in the instructions, and this intermediate intention must be formulated by the patient himself. As a rule, patients with massive bilateral lesions (tumours) of the frontal lobes do not perform such an action and soon replace the required movements with an echolalic repetition of the instruction: 'Yes, lift the hand'. This observation supports the conclusion that patients with massive frontal lobe lesions are able to execute a direct order [but] unable to execute a complex program of actions if some links of it have not been formulated in the instruction." (Luria, 1973, p10.)

Luria's own approach to frontal assessment was set out in the Luria-Nebraska Neuropsychological Battery, a 14-subscale battery of "unstructured qualitative" neuropsychological tests [see sales material]. Luria's "tapping tests" are particularly easy to carry out and readily disclose a multitude of sins. The tests have many sub-variants, but the best known is the "Go/No-Go" test, which is based on the deliberately awkward instruction: "Tap once when I tap once, but do not tap at all when I tap twice".

The Word Fluency Test (WFT) was introduced by Goodglass and Kaplan (1972) and promoted by Benton and Hamsher (1976), and measures how many words a patient can generate beginning with a given letter of the alphabet in a measured minute. The usual stimulus letters are F, A, and S, and the underlying theory implicates our old friend the semantic network [glossary; further discussion], thus ..... 

"The cognitive processes that are activated during a fluency task can be conceptualised as a memory search that involves the use or active restriction of associations. Memory has been theorised as being organised on a conceptually related basis and in lexicons or categories (Collins and Loftus, 1975). Within these two systems, a memory search is thought to involve a spreading activation throughout nodes in the memory structure. The model assumes that everything in memory is linked or associated. [.....] These codes are further broken down into nodes that have inter-emanating associations. A concept, such as an animal or a letter category, would consist of all the associated nodes dominated by a particular node. [.....] Effective productivity within fluency tasks suggests either a concisely structured network of associations within a category or a very efficient search strategy [and] one aspect of the frontal lobe component in a fluency deficit may involve an impaired ability to effectively search memory stores or, perhaps, to restrict an active memory search." (Butler et al, 1993, p520.)

Noting that frontal patients regularly made bizarre estimates of such things as value, Shallice and Evans (1978) reported on experience with "Cognitive Estimation" Tasks (CET). They begin with a case study illustration of the nature of the problem. Patient JS had suffered "a massive right frontal lesion" in an explosion, but his pre- and post-event intelligence scores were nevertheless the same. In one particular respect, however, he was seriously impaired .....

"The one deficit observed was a gross inability to produce adequate cognitive estimates. For instance, when questioned, he replied that the height of the highest building in London was between 18,000 and 20,000 feet, that the largest fish in the world was a 3 foot long trout, that the best paid occupation was that of a long distance lorry driver, that the number of cars in Britain was over 50,000, and that the length of the average spine was between 4 and 5 feet. He did not appear to realise that the answers he gave were bizarre and he justified them when pressed. When it was pointed out to him that the height he had given for the highest building was greater than the estimate he had given earlier of 17,000 feet for the highest mountain in Britain he merely reduced his estimate for the building to 15,000 feet. (Shallice and Evans, 1978, pp294-295.)

The last of the early tests was the Tower of Hanoi (TOH) task. In its typical form, this problem consists of three equal length pegs set vertically into a base, onto which are stacked three quoits of varying size. The patient is presented with a starting configuration of the discs and required to move one at a time until a specified end configuration is achieved in the lowest possible number of moves. However, you are not allowed ever to have a larger disc on top of a smaller one. As can be felt from the MazeWorks TOH animation [click to play], this task calls for considerable forward planning. In fact, the TOH test has an interesting history, having been first used in the field of machine problem solving. The oldest PsycINFO reference is to a paper by Klix, Neumann, Seeber, and Sydow (1963), who describe it as "Cook's 'disc transfer' problem", and chronicle its use at tracking "the unfolding of thought" during a reasoning task. The problem was then further developed by Sydow (1970), adopted by the artificial intelligence guru Herbert A. Simon (1916-2001) (eg. Simon, 1975), who identified four major classes of solution strategy, and then further investigated by Anzai and Simon (1979).

6 - Recent Improvements in Assessing Frontal Lobe Function

"We talk of amnesia, aphasia, dyslexia, dyscalculia, and so forth, describing the dysfunction, and leaving open the question of its possible localisation. I would like to suggest that a similar approach be taken in the case of possible dysfunctions of the central executive. Unfortunately no term exists for this, and I for one cannot think of an obvious neat descriptive label [.....] As a stop-gap I suggest the term dysexecutive syndrome." (Baddeley, 1986, p238; italics original.)

For our present purposes, we are dating the modern age of frontal assessment to 1982, when Shallice (1982) devised a variant of the Tower of Hanoi, called the Tower of London (TOL) task [buy one]. In its usual form, this problem consists of three different length pegs, capable of holding one, two, and three beads respectively. However, where the TOH discs are the same colour but different sizes, the TOL beads are the same size, but different colours. As a result, the TOL is easier to grade for problem difficulty (how many moves it takes), and this makes for a more sensitive psychometric test (Shallice 1988). Shallice (1982) found a significant left anterior frontal deficit for TOL performance. 

Muriel D. Lezak is another who has pointed to the problems of assessing executive functions (eg. Lezak, 1982). "With few exceptions," she writes, "we do not have standardised methods for making objective or reliably replicable estimates of gradations of impairment of the functions [or] for making intra- and inter-individual comparisons" (p281). Like Luria, she, too, is especially concerned about the cognitive processing involved during "goal formulation", thus ..... 

"The capacity to formulate a goal, or to have an intention, is bound up with motivation and with awareness of self and how one's surroundings impinge on oneself. Goal-directed motivation differs from the simple arousal states that spur infants, impulsive adults, and subhuman animals. Simple arousal states lead automatically to reactive or instinctive activity. In contrast, persons capable of goal formulation not only can conceptualise their needs and desires before acting upon them but can entertain motives that may be far removed from organismic drive states and much more complex than are impulsive acts or automatic responses to physiological needs or environmental stimuli. The ability to create motives out of past experiences, out of an appreciation of physically or temporally distant needs, or out of one's imagination, requires self-awareness at a number of levels including awareness of internal states, an experiential sense of self, and self-consciousness vis-ŗ-vis the social and objective environment. It also requires the ability to identify those aspects of one's surroundings that may have personal relevance. [.....] It simply does not occur to [persons lacking this capacity] to do anything." (Lezak, 1982, p286; bold emphasis added.)

There then came a flurry of innovative assessment techniques. In 1984, for example, Milner and Petrides (1984) added the Self-Ordered Pointing Test (SOPT) to the frontal assessment repertoire [glossary]. This was followed by Reitan and Wolfson's (1985)resurrection of the Trail Making Test (TMT), a simple pen-and-paper task in which the patient has to join up specified sequences of letters and/or numbers printed randomly across the page. The test was previously part of the Army Individual Test Battery (1944), and comes in two parts. Part A requires only that patients connect a sequence of numbers, say in ascending order. Part B, however, requires that numbers and letters be connected alternately in ascending order, and provides the better test of frontal performance (Stern and Prohaska, 1996, p252). And then, in the same year that Baddeley devoted an entire chapter to the central executive and its problems, coining as he did so the name "dysexecutive syndrome" (DES), came two papers which challenged our conception of nothing less than "the will" itself. We refer here to Lhermitte's work on "imitation behaviour" (IB) and "utilisation behaviour" (UB). These are types of behaviour which reflect directly on a frontal patient's fundamental ability to direct his/her own life; to maintain what Lhermitte (1986) calls "the shifting balance between dependence and independence" (p335). Here are some typical descriptions .....

"A 52-year-old right-handed housewife had suffered from [.....] a right hemiparesis. CT scan revealed an astrocytoma in the basal left frontal lobe. Treatment consisted of a left frontal lobectomy and radiotherapy. She recovered well, returned home, and resumed her domestic work but showed a lack of initiative. [During testing] I put some medical instruments on my desk. She immediately picked up the blood pressure gauge and very meticulously took my blood pressure [photograph]. After this she took the tongue depressor and placed it in front of my mouth, which I opened, and she examined my throat [photograph]. [Later, she] and I were speaking in my office. Suddenly, I got up and I left the room. She accompanied me and followed me outside without comment. I walked toward my car and got in. She went to the other door and got in beside me. [.....] Not a word was spoken during this outing (which lasted about 40 minutes). When asked about it a few days later, she recalled the outing clearly and considered it quite normal." (Lhermitte, 1986, pp336-338.)

Anxious to get some prevalence data, Lhermitte, Pillon, and Serdaru (1986) screened for IB and UB in a sample of 125 "patients with a definite diagnosis of cerebral lesions". IB was tested by having the examiner suddenly interrupt the clinical examination to perform without explanation or comment various sequences of bodily gesture, all more or less inappropriate to the setting (eg. saluting, kicking, combing the hair, etc.), and UB by presenting the patient (again without explanation or comment) with specific objects. This is what they found ..... 

"75 patients demonstrated IB (35 with and 40 without UB). Almost all patients imitated the examiner starting with the first gesture. [.....] All gesture sequences were imitated without surprise: the patients tried to follow as best they could the order they thought they had to obey. No patient ever forgot a detail of gestural sequence (eg. when lighting a candle, he would always blow the match out). If the gestures were not easy to perform, the patient adapted himself perfectly to overcome the difficulties. Male patients even imitated such socially unacceptable gestures as using a urinal, or urinating against a wall, in front of 20 or 30 people. Some of them smiled when imitating unusual gestures (kneeling as if to receive a blessing or putting on eyeglasses when already wearing some). Several patients refused to imitate. They indicated that they considered the gesture ridiculous, or did not want to perform it (eg. a patient who wore a wig refused to comb his hair)." (Lhermitte, Pillon, and Serdaru, 1986, p328.) 

Lhermitte et al explained their observations by proposing that regions of the parietal cortex are responsible for integrating the jumble of multi-channel sensory data arriving in the various areas of sensory cortex. This sets up "links of dependence" between the individual and the outside world. However, the parietal cortex is itself subject to an inhibitory influence from the frontal lobe. In normal subjects, the authors see this as setting up a dynamic equilibrium between these two forces. When the frontal lobes are damaged, however, the inhibition stops, leaving the parietal lobe accordingly oversensitive to external stimuli. Because the patient's behaviour is more controlled by external rather than internal factors, Lhermitte calls this "Environmental Dependency Syndrome". [Small wonder, therefore, that McKenna and Warrington (1986) were able to complain that "the organisation of cognitive functions is more complex than has hitherto been supposed" (p32).]

The late 1980s then saw the sorting tasks being challenged. Anderson, Damasio, Jones, and Tranel (1991) compared frontal (n=49) and non-frontal (n=24) performance on the WCST, and found that "the WCST alone should not be used to group brain-damaged subjects into 'frontal' and 'nonfrontal' groups" (p920). This is not to say that the frontal lobes are not involved in the sorting process, merely that "performance on a multifaceted cognitive task such as the WCST will necessarily involve the coordinated interaction of multiple and separate brain regions" (p920). Shallice and Burgess (1991) agree, arguing that more lifelike "multiple subgoal tasks" are the best means of establishing ability in life-like situations. All too often, they point out, the "relevant tests" are not applied. When preparing a meal, for example, one has in real life to consider not just the isolated merits of a particular menu, but also the practical issues of availability of ingredients, available time, etc. Far better, therefore, if testing tapped into the "many minor decisions" which everyday living typically consists of, and especially those which need to be "undertaken in parallel with other activities" (p728). Shallice and Burgess then report three case studies where the standard battery of tests was supplemented by two new tests, the "Six Element" (SE) Test [glossary] and the "Multiple Errands" (ME) Test [glossary], before concluding as follows .....

"If one considers what is involved in carrying out these multiple subgoal tasks, then at a very general level, four basic types of process are relevant. Motivational and memory processes are clearly required and so are a variety of special-purpose cognitive processes of the sort that standard neuropsychological tests assess. In addition there are certain bridge processes which enable the special-purpose cognitive processes to be used to satisfy motivational requirements. A deficit in basic special-purpose cognitive processes seems an implausible explanation of their difficulties on the experimental tasks, given the performance of the patients on the baseline tests. Indeed the most difficult Multiple Errands subtest gave problems for some of the controls as well as the patients; it was the least sensitive part of the procedure. However, frontal patients often manifest inappropriate affect and have frequently been described as apathetic or impulsive [citation], and also they can have memory problems [citation]. The possibility of motivational or memory difficulties therefore needs to be considered, especially as the patients, when asked to account for some action, often said that they had completely forgotten their prior intention. A possible motivational explanation of the impaired performance of the 3 patients is that they require continuous social reinforcement to carry out psychological tasks, and without it their spontaneous motivation would tend to dwindle rapidly; without it they do not persevere." (Shallice and Burgess, 1991, p735.)

7 - Some Comparative Studies

Ever since the days of Fritsch and Hitzig and Ferrier [see Section 2], animal brain vivisection studies have helped inform clinical interpretation of human frontal performance. Such research has continued to this day, and in this section we look at some of the studies which have cast light on forebrain involvement in memory functions. The first major finding came from the same Carlyle Jacobsen who in 1935 had helped to persuade Moniz to carry out the first psychosurgery [again see Section 2]. Jacobsen (1936) found that frontally damaged monkeys had particular difficulties with "delayed response learning", that is to say, with learning tasks where there is an enforced delay between stimulus and response. In its simplest form, this experiment offers the animal two lidded bowls, shows a piece of food being put beneath one of the lids, and then enforces a delay before allowing the animal to lift one of the lids. Normal monkeys can respond correctly over delays of one or two minutes, but a frontal monkey's performance tails off (so to speak) after one or two seconds! Jacobsen interpreted these observations as suggesting an abnormally rapid decay of immediate memory, however contradictory evidence started to emerge when Malmo (1942) replicated Jacobsen's study, and found that the test animals would perform normally if kept in the dark during the delay period. This therefore suggested that it had been interference or distraction which had been doing the damage in Jacobsen's animals, and not memory decay per se. Thus .....

"The results of the present experiment may be summarised briefly as follows: successful performance in delayed response is possible for monkeys after their frontal association areas have been removed bilaterally. The difference between normal and operated monkeys with respect to such performance is not one of presence or absence of the capacity for delayed response, but rather the difference is one of degree of susceptibility to the interfering effects of extraneous stimuli occurring during the delay interval. Jacobsen's hypothesis that immediate memory is functionally located in the frontal lobes is not sufficient to account for the results." (Malmo, 1942, p354.)

More recently, animal studies have been helping to locate working memory, "the capacity to retain information no longer present in the environment, to manipulate and/or transform this information, and to use it to guide behaviour" (Postle, Druzgal, and D'Esposito, 2003/2004 online, p1). Here researchers have been aided by technical improvements which allow the discharge records of individual prefrontal neurons to be examined. Among the lead authors in this area were/are Joachin M. Fuster at the UCLA Neuropsychiatric Institute and Patricia S. Goldman-Rakic at the Yale University School of Medicine. Here is Fuster on the technicalities .....

"In the microelectrode exploration of the prefrontal cortex during behavioural tasks, one is struck by the variety of stimuli to which its units are responsive. To be sure, the magnitude and selectivity (tuning) of prefrontal unit responses to sensory stimuli are generally much lower than those of units in primary sensory or postcentral associative cortex to appropriate stimuli. Yet nowhere else in the neocortex are cells attuned to so many different sensory inputs as in the prefrontal cortex. On closer analysis it becomes apparent, however, that most prefrontal cells simply respond primarily, if not exclusively, to the broad category of stimuli that, in one way or another, are related to the task at hand, without much regard for their most particular sensory or physical characteristics. [.....] In a delay trial, for example, it is obvious that some units are especially responsive to the cue and the visual or auditory stimuli that constitute it or accompany its presence; other units are mostly responsive to the stimuli that appear for choice at the end of the delay, others to the presumably proprioceptive input that results from other instrumental manual response of the animal, and still others to the delivery of reinforcement for a correct response." (Fuster, 1992, pp352-355.)

..... and here is his general theoretical orientation .....

"A large body of empirical evidence supports the notion of a critical role of the prefrontal cortex in the temporal organisation of goal-directed behavioural sequences. The key element of that role is the bridging of cross-temporal contingencies of behaviour, in other words, the adjustment of the actions of the organism to temporally distant events and objectives. By the analysis of lesion effects, neuroelectrical phenomena, and metabolic activity we are led to conclude that the prefrontal cortex subserves at least three cognitive functions that allow the mediation of cross-temporal contingencies and, thereby, the formation of temporally extended structures of behaviour: short-term memory, preparatory set, and control of interference." (Fuster, 1985, p169.)

For her part, Goldman-Rakic has resurrected Jacobsen's delayed response paradigm, but with the added sophistication of modern electrode technology to monitor the electrical behaviour of single neurons in the prefrontal cortex. As a result of gaining direct access to brain activity during the learning task she was able to test Jacobsen's original suspicion that the secret of working memory lay in the prefrontal cortex, and that this might well explain the "gross deficiencies" in the ways frontal patients "use knowledge to guide their behaviour in everyday situations" (p73). Here is the method .....

"At Yale, Shintaro Funahashi, Charles J. Bruce, and I have used the single-neuron technique in conjunction with a delayed-response experiment that tests spatial memory. For our experiment, a monkey is trained to fix its gaze on a small spot in the centre of a television screen. A visual stimulus, typically a small square, appears briefly in one of eight locations on the screen and then vanishes. At the end of a delay of three to six seconds, the central light, or fixation spot, switches off, instructing the animal to move its eyes to the location where the stimulus was seen before the delay. [.....] Because the animal's gaze is locked into the fixation spot, each stimulus activates a specific set of retinal cells. Those cells, in turn, trigger only a certain subset of the visual pathways in the brain. Using the eye movement experiment, we have demonstrated that certain neurons in the prefrontal cortex possess what we call 'memory fields': when a particular target disappears from view, an individual prefrontal neuron switches into an active state, producing electrical signals at more than twice the baseline rate. The neuron remains activated until the end of the delay period, when the animal delivers its response. A given neuron appears always to code the same visual location [and] other neurons code for other target locations in working memory." (Goldman-Rakic, 1992, p75.)

Work of this sort continues apace, with Curtis and D'Esposito (2003/2004 online) providing a recent review of the role played by dorsolateral prefrontal cortex in working memory, and Postle, Druzgal, and D'Esposito (2003/2004 online) suggesting the involvement of more posterior tissues as well.

8 - Advanced Memory Theory (1): "Online Representational Memory"

Daigneault, BraŁn, and Whitaker (1992) have attempted to test the hypothesis that the "basic prefrontal function" is "on-line representational memory", a form of memory which can operate independently of incoming stimulation. They adopt Goldman-Rakic's (1987) theory of working memory, as follows .....

"Goldman-Rakic (1987) postulated that prefrontal cortex receives sensory and mnemonic representations of reality as well as symbolic representations (eg. concepts, plans) which have been elaborated in other cerebral areas. These are kept activated ('on line') by prefrontal cortex in 'representational memory' long enough for this live memory to modulate behaviour appropriately despite the absence of external contingencies or despite the presence of external task-irrelevant 'discriminative' stimuli. Different prefrontal areas are postulated to house different representational memory units which are related to each other anatomically and functionally [and] any one prefrontal area is assumed to exert inhibitory as well as excitatory influence on the relevant motor systems. Discrete prefrontal lesions are understood to hinder specific representational memory units resulting in specific difficulties in the regulation of behaviour." (Daigneault, BraŁn, and Whitaker, 1992, p50.)

Daigneault et al then exposed 259 normal adults to seven selected frontal lobe tests, and a factor analysis of the results revealed five "prefrontal functional constructs", as follows .....

Factor 1 - Planning: This is the frontal lobe skill tapped by the SOPT and simple errors on the Porteus Maze. It may also be viewed as "the elaboration of strategy" (p49). 

Factor 2 - Self-Regulation: This is the frontal lobe skill tapped by perseverative errors on the WCST and repeated errors on the Porteus Maze. It indicates that patients are failing to modify a chosen course of action despite the availability of error feedback. 

Factor 3 - Maintenance of a "nonautomatic cognitive or behavioural set": This is the frontal lobe skill tapped by interference errors on the Stroop Test, category break errors on the WCST, and alternation errors on the Trail Making Test. It indicates that patients are failing to maintain a complex behavioural plan in the face of distraction.  

Factor 4 - Spontaneity and sustained mental productivity: This is the frontal lobe skill tapped by verbal fluency and design fluency tasks. 

Factor 5 - Spatiotemporal Segmentation and Organisation: This is the frontal lobe skill tapped by tests of recency judgement.

In yet another assault on the problem of actually defining executive cognition, Duffy and Campbell (1994) identify three areas of interest, namely .....

Working Memory: This is the problem of how the prefrontal cortex supports the "neural chalkboard" (p380) of short-term memory, that is to say, the memory resource which "enables the individual to simultaneously evaluate multiple intra- and inter-personal cognitive representations [by putting together] a reasoned strategy for dealing with the particular task at hand" (p380). This resource seems to be situated particularly in the dorsolateral area.

"Mediation of Cross-Temporal Contingencies": Here Duffy and Campbell buy into the work of Fuster (1985), who proposed that "the overarching function of the prefrontal cortex (and the core characteristic of executive cognition) is 'the integration of sensory information and motor acts into novel, complex, and purposive behavioural sequences'" (p380).

"Modulation of Large-Scale Neurocognitive Networks": This is the problem of finally assuming an executive role in behaviour, enabling the individual "to respond to a particular stimulus on the basis of a distillate of previous experience and current environmental stimuli; for example, 'although I'm tired I must continue studying if I want to pass the exam tomorrow'" (p381).

They also distinguish three separate "prefrontal syndromes", namely .....

(1) Dysexecutive Type: This syndrome arises from lesions of the "dorsal convexity" [that is to say, the gentle "hump" in the region of Brodmann's Area 9], and is characterised by dysfunction in flexibility, sequencing, and planning ahead. 

(2) Disinhibited Type: This syndrome arises from lesions of the orbitofrontal region [that is to say, the ventral surface of the frontal lobe, where it contacts (and can easily be damaged by) the bony roof of the orbits of the eyes], and is characterised by "poor impulse control, explosive aggressive outbursts, inappropriate verbal lewdness, jocularity, and a lack of interpersonal sensitivity" (p383). 

(3) Apathetic Type: This syndrome arises from lesions of the medial region of the frontal lobe, at the anterior end of the cingulate gyrus, and is characterised by apathy and inertness, perhaps because said area is normally involved in exploration and motivation.

Jacobs (2004 online) offers a concise alternative description of the dysexecutive and disinhibited types, if interested [take me there].

9 - Advanced Memory Theory (2): Autobiographical Memory

Another frontal sign to attract the attention of cognitive theorists is "confabulation", the inventing of factually spurious explanations to "fit" otherwise fragmentary and/or inconsistent recollections, and another hot line of enquiry is into the relationship between confabulation and "autobiographical memory" [glossary]. Papagno and Baddeley (1997/2004 online) give an example of how that relationship may present itself, describing the behaviour of patient MM, a 29-year-old man who had suffered a severe right hemisphere stroke .....

"His confabulations were spontaneous and consistent and not triggered by a lack of memory. For example, each time we left the testing room, which was close to a lift, he claimed that he had to take the lift and go upstairs (in fact we were on the top floor) to see his children. MM's wife had given birth ten days before the accident to a child whose name was Enea; he could remember it exactly (including date of birth, name of baby, etc.) but he claimed his wife had also had a second child, born one month later, whose name he could not remember. When asked how it was possible to have a child one month after the other, he answered 'Ask my wife, she did it'." (Papagno and Baddeley, 1997/2004 online, pp744-745.)

Other theorists have highlighted the processes of "reality monitoring", that is to say, the ability to maintain an accurate internal representation of the world and what is going on within it. The key theoretical construct here is Johnson, Hashtroudi, and Lindsay's (1993) "source monitoring framework" (SMF). This is a collection of mechanisms capable of tagging retrieved memory content as actual or imagined. Thus ..... 

"Typically, memories for experienced (external) events have information denoting time, location, spatial arrangement, emotion or sensory perceptual details such as colour or shape. In contrast, memories for thoughts and imagined events typically have much less or less vivid information of these types, but often have more information about cognitive operations (such as intention and planning, deliberate imaging, actively searching for a piece of information and drawing conclusions). [.....] Memory monitoring processes capitalise on such differences by evaluating memories (or mental experiences in general) for their match with the expected characteristics of a given source. Such attributions are correct sufficiently often to keep our memories and beliefs constrained by reality, but, importantly, are subject to error." (Johnson and Raye, 1998, pp137-138.)

Insofar as "source monitoring" was concerned ..... 

"..... we trust our source monitoring processes to indicate not only when memories probably correspond to reality but also when they might not do so. Various processes operate to constrain the amount of distortion that arises from our imperfect memory system and to signal us when we should be cautious about the truthfulness of a memory. The feeling of remembering is important to our well-being, but so is the feeling of not remembering that accompanies vague, inconsistent, ir implausible recollections. Accurate memory is knowing when we do not remember as well as knowing when we do. The subtle balance of the encoding, consolidation, reactivation, retrieval, and evaluation processes that underlie the 'meta-memory' function of source monitoring develops throughout childhood, tends to weaken in old age, and can be disrupted at any age by distraction, stress, drugs, hypnosis, and social or motivational pressures. A profound disorganisation of memories and beliefs can occur when memory monitoring processes are disrupted as a consequence of frontal brain damage." (Johnson and Raye, 1998, p144.)

Antonio R. Damasio, Head of Neurology at the University of Iowa School of Medicine has recently (Damasio, 2002) turned his high tech brain scanners onto the problem of episodic memory [glossary]. He invokes the concept of the "time stamp" to differentiate episodic from semantic memory content, thus .....

"In the course of evolution, humans have developed a biological clock set to [the] alternating rhythm of light and dark. This clock, located in the brain's hypothalamus, governs what I call body time [.....]. But there is another kind of time altogether. 'Mind time' has to do with how we experience the passage of time and how we organise chronology. [..... We] place events in time, deciding when they occurred, in which order and on what scale, whether that of a lifetime or of a few seconds. How mind time relates to the biological clock of body time is unknown. It is also not clear whether mind time depends on a single timekeeping device or if our experiences of duration and temporal order rely primarily, or even exclusively, on information processing. [In any event, the] ability to form memories is an indispensable part of the construction of a sense of our own chronology. We build our time line event by event, and we connect personal happenings to those that occur around us. When the hippocampus is impaired, patients become unable to hold factual memories for longer than about one minute. Patients so afflicted are said to have anterograde amnesia. Intriguingly, the memories that the hippocampus helps to create are not stored in the hippocampus. They are distributed in neural networks [ie. cell assemblies] located in parts of the cerebral cortex (including the temporal lobe) related to the material being recorded: areas dedicated to visual impressions, sounds, tactile information, and so forth. These networks must be activated to both lay down and recall a memory; when they are destroyed, patients cannot recover long-term memories, a condition known as retrograde amnesia. The memories most markedly lost in retrograde amnesia are precisely those that bear a time stamp: recollections of unique events that happened in a particular context on a particular occasion. For instance, the memory of one's wedding bears a time stamp. [.....] The temporal lobe that surrounds the hippocampus is critical in the making and recalling of such memories." (Damasio, 2002, pp50-51.)

10 - Advanced Memory Theory (3): Structured Event Complexes

One of the most innovative theorist-clinicians in the last 15 years is Jordan Grafman, Head of the Cognitive Neuroscience Section in the US National Institute for Neurological Disorders and Stroke (NINDS) in Bethesda, MD. Grafman (1989) has developed his own ideas as to the nature of the cognitive structures in the frontal lobes which coordinate lesser blocks of memory into meaningful sequences [1994 press release]. He terms these "managerial knowledge units". They are more or less synonymous with the terms action schema and script, and have recently been described as a category of script-like structures "with a beginning and an end and a hierarchical organisation going from more abstract [.....] to more concrete levels" (Chevignard et al, 2000/2003 online). Not surprisingly, this leaves them highly susceptible to frontal lobe lesions. Here are the main points of Grafman's analysis .....

"Cognitive science has long been concerned with trying to understand how people represent in memory events that occur in our lives [.....]. A variety of cognitive structures have been hypothesised to account for this kind of knowledge [including] schemas, scripts, frames, cases, and story grammars [.....]. What these knowledge structures have in common are that they are composed of a set of events, actions, or ideas that when linked together form a knowledge unit (eg. a schema). A unit could be a series of simple movements or the set of rules used to solve a physics problem. We have called this general class of linked unitised information the Structured Event Complex (SEC). We have called the SEC that is specifically involved with planning, social behaviour, and the management of knowledge, the managerial knowledge unit (MKU). It is the MKU and its more primitive SEC neighbours that we hypothesise are only stored in the prefrontal cortex [citation]. What might the informational content of an MKU be like? It is suggested that an MKU is composed of a series of events. There should be a typical order to the occurrence of these events. The ordering of events obeys multiple constraints. Some constraints are physical. You cannot have coffee in a cup unless it is first poured into the cup. Some constraints are cultural. In the United States, people generally shower on a daily basis in the morning before eating breakfast. Some constraints are purely individual. Some people brush their teeth twice in the morning, once before and once after eating breakfast. The rigidity of the event order is also dependent on the frequency of its activation. That is, a rigid event order carried out daily should have a 'stronger' representation that one carried out monthly." (Grafman, 1994, p194; bold emphasis added.)

Goel and Grafman (1995) have pointed to the dangers of presuming that the superficially similar Tower of Hanoi and Shallice's (1982) Tower of London tests actually measure the same thing, and can therefore be used interchangeably. They tested a sample of 20 frontal lobe patients on a set of nine TOH problems of increasing difficulty, and found that performance was impaired relative to normal controls. However, the precise how and why of the impairment were not clear, thus ..... 

"[Our] results confirm the widely held belief that patients with frontal lobe lesions are impaired on the [TOH] task with respect to normal controls. However, such a conclusion is only a first step. What we really want to know is whether they are especially impaired, more so than on other cognitive tasks. And if they are so impaired, we want to know why." (Goel and Grafman, 1995, pp629-630; italics original.)

They then call for greater discipline in conceptualising the term "planning", thus .....

"To plan is to chart a course from point A to point B, without 'bumping' into the world. All the 'bumping' must be done in some modelling space, and some satisfactory path extracted. Once the path has been constructed, the planning component is complete. The execution or following of a plan is quite a different process. It is the construction and evaluation of this path in some modelling space that we are referring to when we use the term 'planning'." (Goel and Grafman, 1995, p638.)

Their substantive criticism of the TOH puzzle is then that the ability to "look ahead" is neither necessary nor sufficient to solve the TOH. It is not necessary, they point out, because computers can be programmed to do the TOH job quite adequately [this being what Herbert Simon was up to at the end of Section 5], and computers do not understand. Nor is it sufficient, because "you can look ahead all you like, but unless you see the 'trick', the counterintuitive backward move, you won't solve the puzzle" (Goel and Grafman, 1995, p638). Frontal processing, in other words, often includes the sort of "insightful problem solving" once so popular with workers such as Maier, and Duncker.

As it happens, the WCST has also been technically criticised of late. For example, Dunbar and Sussman (1995/2004 online) have argued that the WCST is "a classic concept attainment task" (that is to say, subjects have to formulate, apply, and monitor hypotheses as to the "rules" of the game at hand), and, as such, offers "a number of different possible sources of perseveration".

The frontal lobes are also increasingly being implicated in phenomena such as consciousness and volition. For example, Badgaiyan (2000/2004 online) has studied executive control and the will, and reviews neuroimaging studies which suggest "several cortical areas that mediate different functions of the central executive" (p39). The cingulate cortex, for example, is activated in the Stroop task and is apparently involved in "executive functions such as error detection and response monitoring" (p39). Indeed the cingulate is involved in so many executive functions that it may be "considered crucial for execution of supervisory function" (p39).

11 - Advanced Memory Theory (4): Hemispheric Differences

Although Shallice (1982) found a left hemisphere deficit on TOL performance [see Section 6], and Mesulam (1995) found contralateral symptoms of "motivational neglect" with unilateral lesions of the anterior cingulate cortex, most hemispheric differences in frontal function are restricted to the more posterior motor areas. It would be wrong, however, to proceed without noting the writings of Elkhonon Goldberg at the New York University Medical Centre. Following a review of the literature on hemispheric differences, Goldberg, Podell, and Lovell (1994) have suggested the following principle of hemispheric specialisation .....

"..... the right hemisphere is critical for the exploratory processing of novel cognitive situations to which none of the codes or strategies preexisting in the subject's cognitive repertoire readily applies. The left hemisphere is critical for processing based on preexisting representations and routinised cognitive strategies. The traditional language/nonlanguage dichotomy then becomes a special case of this more fundamental principle. The novelty-routinisation principle of hemispheric specialisation is different from the more traditional ones in several major respects. First, the distinction between cognitive novelty and cognitive routinisation is not limited to humans. [.....] In addition, the novelty-routinisation approach emphasises individual differences and argues against the fixed assignment of particular materials and tasks to one or the other hemisphere. What is cognitively novel to one individual is familiar and routinised to another. Finally, the novelty-routinisation hypothesis offers a dynamic rather than a static view of hemispheric specialisation. It implies that the pattern of hemispheric specialisation is different in a given individual at different developmental stages. Specifically, it implies that the locus of cortical control shifts from the right to the left hemisphere in the course of cognitive skill development." (Goldberg, Podell, and Lovell, 1994, pp372-373; bold emphasis added.)

12 - Control Architecture Consideration

"Nothing is more chastening to human vanity than the realisation that the richness of our mental life - all the thoughts, feelings, emotions, even what we regard as our intimate self - arises exclusively from the activity of little wisps of protoplasm in the brain." (Ramachandran and Hirstein, 1997, p429.)

We must now make an explicit connection between two study areas - the Tim Shallice with the reputation as frontal lobe theorist is the same Tim Shallice who teamed up with America's Donald Norman in the early 1980s to formulate their theory of the Supervisory Attentional System (SAS). We have introduced this theory in our e-paper on "Mode Error in System Control", so here is an alternative telling of the story .....

"Norman & Shallice (1980) and Shallice (1982) have adopted a computational information-processing approach to modelling disorders of 'executive' functions. Norman & Shallice took as their starting point the distinction between habitual and novel action routines [and] suggested that the selection and integration of these two classes of action were based on different principles. Norman & Shallice proposed that control over the sequencing and integration of the components required for complex but well-established patterns of behaviour is mediated by hierarchically organised 'schemas' or motor representations [.....]. In driving to work the highest level of the schema might be a comparatively abstract representation of the route. Such high-level schemas can call up subordinate 'programs' or subroutines; thus 'driving to work' will have component schemas including at the lowest level instructions to muscles to press pedals and turn the steering wheel. Norman & Shallice suggested that under many conditions we can function on "auto pilot", selecting and integrating cognitive or behavioural skills on the basis of established schemata. Once a schema has been triggered it 'competes' for dominance and control of action by a process of inhibiting other schemas which would be likely to conflict with it [.....] (a process which they termed contention scheduling). When one needs to suppress an automatically attractive alternative source of stimulation, to plan novel solutions to problems, or to change flexibly from one pattern of behaviour to another, the selection of schemas on the basis of the strength of their initial activation might be disastrous. Norman & Shallice argued that, under these circumstances, the selection of schemas was modulated by the operation of a supervisory attentional system [which] can provide a boost to a schema's level of activation, thereby enabling it to 'get ahead' in the competition for dominance despite starting from a handicapped position." (McCarthy and Warrington, 1990, pp362-363; italics original.)

ASIDE: If interested in the topic of action schemas and motor programming - itself a major research area - see our e-paper on "Motor Programming". The term "contention scheduling" was borrowed originally from computer science, where it was an important aspect of the sort of "job execution scheduling" carried out by virtual machine mainframe operating systems - see Section 1.2 of our e-paper on "Short-Term Memory Subtypes in Computing and Artificial Intelligence" (Part 5), for a longer introduction

Now we mention the SAS theory because it may well be that defects in contention scheduling underlie the sort of utilisation behaviour discussed in Section 6. For example, Shallice, Burgess, Schon, and Baxter (1989) report on signs of UB in case LE, a 52-year-old right-handed man .....

"On September 17, 1987, his son reported that the patient was found early in the morning wearing someone else's shoes, not apparently talking or responding to simple commands but putting coins into his mouth and grabbing imaginary objects. [.....] A CT brain scan showed acute ischaemic [glossary] changes in the inferior and medial aspect of both cerebral hemispheres and the genu and rostrum of the corpus callosum [and] carotid angiography revealed complete occlusion of the left proximal anterior cerebral artery just beyond it origin. [.....] Some clinical improvement occurred during the 6 months after his stroke when the present investigation was undertaken. [.....] On all frontal lobe tests his performance was grossly impaired. He failed the Weigl (1941) Sorting Test and a simple alternation problem [citation]. The Tower of London test (Shallice, 1982) was abandoned at the halfway stage because of his continual rule violations. On Verbal Fluency (Goodglass and Kaplan, 1972) he produced 3 words beginning with F in 60 s, and 4 with S; for the letter A he produced only names despite repeated instructions that they were not appropriate. In summary, LE's performance on spatial, perceptual, language, and simple praxic tests was satisfactory. By contrast his performance on tasks that involved a frontal or long-term memory component was uniformly and severely impaired. [.....] Utilisation behaviour occurred not only when LE was in conversation with the examiner, but also when he was in the middle of performing [other tasks]. Thus he took the playing cards and dealt them while attempting to explain some common proverbs ....." (Shallice et al, 1989, pp1588-1591.)

These authors then fit these observations into the Supervisory System theoretical framework as follows .....

"First, in the absence of a working Supervisory System in the frontal lobes, perceptual input alone can lead to activation of an action schema and its selection in contention scheduling; for instance, the sight of a pair of scissors and paper activates the actions associated with the objects, and these behaviours are then carried out (selected) in the absence of supervisory inhibition. This is precisely what happens in utilisation behaviour. [.....] Secondly, even when the Supervisory System is impaired - as can be assumed for LE - the probability of utilisation behaviour occurring will depend on whether any action schema which is being randomly triggered in contention scheduling is or is not being inhibited by an already active schema. This is more likely when the patient has been instructed to carry out a task and task-irrelevant stimuli are being presented. The model would predict that utilisation behaviour should occur most frequently in a patient with an impaired Supervisory System when no task is being undertaken. Utilisation behaviour should also be more frequently observed when the required task is in the auditory-verbal domain, when there would be no overlap in the cognitive subsystems involved, than when a task-irrelevant visual input is competing with the triggering stimuli. Such a model provides a more articulated version of Lhermitte's general position and predicts differences in the frequency of utilisation behaviour according to the particular activity the patient is performing. It fits the pattern of results found in our patient LE." (Shallice et al, 1989, pp1596-1597.)

The concept of control layers was taken up in detail by Donald T. Stuss of the University of Toronto. Stuss (1991, 1992) has proposed a "hierarchical feedback-feedforward model", as now described .....

"This model represents a hierarchy of brain abilities, meaning that there are 'higher' and 'lower' order functions. [.....] An important component of the model is the feedback loop present at each level. Incoming information is forwarded to a comparator which analyses in a pattern-recognition format the incoming specific fact or group of facts. These comparator values have been developed through previous experience, modelling, and training. If there is no difference between the input and comparator values, no adjustment is necessary. If they are different, a change output is automatically triggered. Depending on the level or the demand, this could be action to change the environment, a call for increased information from the environment, or a requirement for direction from higher levels and alteration of the comparator. A feedforward system is postulated to preset the system in an anticipatory manner. Three levels of monitoring or feedback-feedforward systems are proposed [figure]. The lower level(s), at least, may be considered as modules as described in cognitive psychology [citation]. One could postulate more levels or smaller feedback loops within particular systems. The three levels proposed are satisfactory as a skeleton outline for the specific needs of this paper. Neuropsychological input at the lowest level presented is sensory/perceptual and is domain- or module-specific: consequently, multiple systems relating to specific functions may exist. At this level operations may range from simple to complex. Regardless of their complexity, they are overlearned and routinised. The processes are thus virtually automatic - speed of operations is rapid. [.....] The routinised activity is not conscious or easily changed by conscious effort. The process of routine selection of routine actions or thought processes has been labelled 'contention scheduling' by Norman and Shallice [citations]. [.....] The second level described is associated with the executive control or supervisory functions of the frontal lobes [citation]. The neural input for this second level derives primarily from the information elaborated by the sensory/perceptual level. The neural substrate for this second level is the well-documented reciprocal connections of the frontal regions with all posterior multimodal and basic limbic structures [citations]. The primary role of this level is the conscious direction of the lower level systems toward a selected goal. This control is higher order, an adjustment of the ongoing activities of lower modules [citations]. This control may well be divided into specific functions such as anticipation, goal selection, plan formulation, evaluation and monitoring of behaviour, and anterior attentional functions such as selectivity and possibly persistence [citations]. [.....] At this level, the feedback loop is slower, deliberate, effortful, and required in the processing of new or complex material where routine responses or knowledge are not available. With repetition, the new complex behaviours requiring active conscious deliberation may eventually become automatic in the sense that control of these behaviours in ordinary circumstances is transferred to a lower level. The highest level described is consciousness - the ability to be aware of oneself and the relation of self to the environment. This prefrontal self-awareness appears to be similar to the concept of metacognition, the ability to reflect on any process itself. This level implies a self-reflectiveness of all levels, including its own. Inputs are presumably the abstract mental representations of the executive's alternative choices. The primary anatomical representation of this highest level has been postulated as the prefrontal region [citations]. The abstract representation of this concept, however, necessitates involvement of all functionally lower levels (of the brain)." (Stuss, 1992, pp10-12; bold emphasis added.)

As far as the modularity of the control architecture is concerned, Godefroy et al (1999/2004 online) have (quite rightly) lamented cognitive science's general confusion as to what a biological control system qua control system needs to do ..... 

"The underspecification of control operations stems from the methodology used to assess executive functions. Most studies have used complex tests such as card sorting, planning, and problem solving tests, which involve numerous cognitive processes and greatly load short-term memory [citations]. Thus, the finding of low performance does not allow to characterise the impairment in terms of cognitive processes. The underspecification of control operations results in a severe limitation of any theoretical account. [.....] The cognitive architecture of the models of Shallice and Baddeley relies on two main assumptions: (1) a hierarchical organisation [and] (2) that control processes depend on an amodal central-supervisory system regulating specific-purpose 'slave' modules. The fractionation of the central control system has been suggested by Shallice (1994) and Baddeley (1996) mainly on the basis of the few clinical data showing the large variety of executive deficits. However, it remains largely unknown whether executive functions depend on a unique control system or on multiple subsystems." (Godefroy et al, 1999/2004 online, pp2-3.)

Godefroy's team therefore recommends a more focused attack on the problem, and identifies three discrete research objectives, namely (1) to decipher the role played by short-term storage, (2) to establish the "architecture of executive functions" (p16), and (3) to specify the various "control operations". It is a rare treat to see such a technical approach in an area usually reserved for clinicians and philosophers. However, we should not underestimate the complexity of the task, because .....

"..... studies of regional cerebral metabolism have identified seventeen functionally distinct areas within frontal cortex, excluding cingulate and orbital cortex, and have led Roland (1984) to conclude that in humans any structured processing of information requires the involvement of one or more regions within the frontal lobe." (Parker and Crawford, 1992, p267.)

Our own views on the brain as an instance of a modular real-time control system are set out in Sections 3.7 and 3.8 of our e-paper on "Short-Term Memory Subtypes in Computing and Artificial Intelligence" (Part 6).

Finally under this section, we may mention Upton and Thompson's (1999) work with the "Twenty Questions" Test .....

ASIDE: The Twenty Questions parlour game was made a tool of formal scientific enquiry by Mosher and Hornsby (1966), who used the method to investigate the developmental stages of purposeful questioning behaviour in normal children. Subjects were told that the experimenter had a type of animal in mind, and had to work out what it was by accumulating question-and-yes/no-answer knowledge about it. They found that children become increasingly able (a) to guide the enquiry process "by what [they] found out earlier" (p101), and (b) to rule out whole classes of irrelevant possibilities at a time. The test was then upgraded for clinical use with alcoholics by Laine and Butters (1982), and with frontal lobe patients by Klouda and Cooper (1990) .....

Concerned that Klouda and Cooper (1990) had only examined five patients, Upton and Thompson followed up with a much larger sample. They assessed 88 patients with frontal lobe dysfunction (42 left frontal, 32 right frontal, and 14 bifrontal), and compared them to 57 temporal lobe neurological controls and 28 normal controls. Here is the nature of the scoring scheme used .....

"All questions asked by the participant were recorded verbatim and classified into one of three types: (1) Constraint: Questions of this type are the most effective search question. These types of question narrow the field by as much as half, by eliminating a series of different types of animals (eg. 'Does it have four legs?' or 'Does it live in water?'). (2) Pseudoconstraint: Questions of this variety are a less effective search strategy. Although they appear to be constraining, they only apply to one particular type of animal (eg. 'Does it have a trunk?' or 'Does it bark?'). (3) Hypothesis Scanning: This is a less effective search strategy and basically involves guessing with no previous basis for such a guess (eg. 'Is it a dog?' or 'Is it a cat?'). The number of each type of question was recorded. Apart from the number of different types of question asked, two other indices of performance were recorded: (a) the number of questions needed to arrive at the correct response (maximum 20) and (b) the number of questions asked before the first guess (presumed to be a measure of impulsivity." (Upton and Thompson, 1999, pp206-207; italics original.)

Results indicated that the bifrontal group required the most questions (mean = 17.32), the left frontal group were next (mean = 14.63), and the right temporal next (mean = 12.36). Right frontals, left temporals and normals all fell in the range 10 to 12. Further analysis by question type revealed that the inefficient hypothesis scanning questions (that is to say, the specific guesses) were most common in the bifrontal group. In addition, orbitofrontal patients showed impaired understanding of the strategy to be employed, although - surprisingly - dorsolateral patients were not thus impaired.  

Well that's the frontal theory, folks, and at this point the question may reasonably be put as to what this enormous cauldron of opinion and data actually boils down to if you are a clinician who wishes merely to manage a caseload. In the closing sections of this handout, we look at some of the practical recommendations which can be made.

13 - Paediatric Frontal Management Issues

Turning firstly to the problems of paediatric management, Tranel, Anderson, and Benton (1994) remind us of the normal developmental sequence .....

"Development and maturation of executive functions in normal children have been addressed in several recent studies. Levin, Culhane, Hartmann, et al (1991) studied 52 children aged 7-15, with a battery of tests. [.....] A principal components analysis revealed a three-factor solution which included factors related to concept formation, freedom from perseveration, and planning. Similar results were reported in a study by Welsh, Pennington, and Groiser (1991). They studied 'executive function' in 100 children aged 3-12. Executive function was defined as 'goal-directed behaviour, including planning, organised search, and impulse control', and six measures were utilised: visual search, verbal fluency, motor sequencing, the [WCST], the [TOH], and the Matching Familiar Figures Test. The authors found that the age at which children achieved adult-level performance on the tasks varied considerably across different tasks. On visual search and a simple version of the TOH, for example, 6-year-old children performed at adult levels. More complex tasks, including the WCST and a complex version of the TOH, showed more protracted development curves, and even 12-year-olds had not achieved adult levels on some of the response variables (eg. complex planning on a four-disc TOH)." (Tranel, Anderson, and Benton, 1994, p131.)

Diamond and Taylor (1996) add that the Luria Go/No-Go tapping task needs to be administered with caution in this client group because the normally developing child finds it difficult at age 3Ĺ years [online abstract].

The frontal lobes play a part in Attention-Deficit (Hyperactivity) Disorders (ADD/ADHD). It does not take long to spot the potentially frontal aspects in this summary of the symptoms from Lombard (2001/2004 online) .....

 "Attention Deficit Hyperactivity Disorder or ADHD is regarded as the most common neurobehavioural disorder affecting children. Its prevalence is estimated to be between 3-10% of school age children with a two-three times greater preponderance in boys compared to girls. The diagnosis of ADHD is based upon clinical grounds as defined by DSM-IV criteria. Core symptoms include hyperactivity, impulsivity, distractibility, and inattentiveness." (e1.)

Anderson and Pentland (1998) warn of residual attentional deficits following childhood CHI. They found that head-injured adolescents "exhibited deficits on a wide range of summary variables extracted from attention tasks" (p283). Anderson (1998) then explains that the natural immaturity of executive processing in children may render this aspect of cognition particularly vulnerable to brain injury. However, it is worth noting that Barkley and Grodzinsky (1994) have had only limited success using selected frontal tests to screen for Attention Deficit Disorders (ADD) in otherwise normal children. They found .....

"Most tests did not perform much above base rate levels of positive predictive power for the subtype of ADD+H and rarely exceeded that which might be achieved by tossing a coin." (Barkley and Grodzinsky, 1994, p137.)

Bishop (1993) has speculated on a possible relationship between executive functions and "theory of mind", thus making frontal lobe psychology directly relevant to clinicians dealing with autistic children .....

"[Ozonoff, Pennington, and Rogers (1991)] proposed that both tests [ie. the frontal tests of executive function already described, and the "Sally-Anne" genre of theory of mind tests] involve the use of stored information to govern behaviour. Impairment in using different types of stored information could affect performance on a wide range of superficially different tasks. To perform well on a theory of mind task, subjects must access internal representations of the mental state of others; to perform executive function tasks, they must generate representations of hypothetical configurations to guide their planning and problem solving. The problem with this explanation is that it is so general that it would be easy to explain almost any deficit on any task in terms of the theory, because most behaviours are governed to some extent by stored information. [.....] An alternative possible point of similarity between frontal lobe patients and autistic children could be that in both cases behaviour is largely driven by external environmental stimulation. Shallice and Burgess [(1996)] argue that people have available a large but finite set of action and thought schemas that, like computer programs, can be activated if well-learned triggers (either from the environment or from the output of other schemas) are excited. The problem for the organism is how to select the appropriate schema when several are activated at once. According to Shallice and Burgess this process of contention scheduling [glossary] is controlled by a supervisory system, whose operation depends on the integrity of the frontal lobes. When the supervisory system malfunctions, external stimulation will elicit responses associated with the stimulus, but there will be little evidence of planned behaviour. Impairments of cognitive function will be particularly apparent in situations where the individual is presented with environmental stimuli but required to withhold the habitual response to these and to perform some other operation instead. For instance, Baddeley (1986) described a man with an acquired frontal lobe lesion who was given a piece of string, a ruler and scissors and instructed to measure out a piece of string in order to cut it later. He immediately started to cut, and when told not to replied: 'Yes, I know I'm not to cut it', while continuing to do so. Viewed in this light, it is of interest to note that in the theory of mind tasks described so far, the child is required to make a statement that is directly contradictory to the visible evidence. Thus, in the Sally-Anne experiment, children must say that Sally will look for her marble in the basket when in reality they have seen it in the box. [.....] This raises the question as to whether the child actually does have a theory of mind and appreciates false beliefs, but is unable to act on this knowledge because of an inability to inhibit a more prepotent response." (Bishop, 1993, pp287-288.)

Mateer and Williams (1991) have studied the effects of frontal lobe injury in children and recommend the following classroom management guidelines .....

1 - Do Not Offer Options: This is because frontal cases have difficulty recognising and prioritising alternative courses of action. Prepare instead a simple course of action.

2 - Do Not Bargain: This is because frontal cases have difficulty recognising contingent benefit.

3 - Structure and Predictability: These are important aids to memory and the scheduling of effort, so detailed timetables and explicit deadlines should be provided.

4 - Use Memory Books and Organisers: These are important to store modelled and directed good practice as it is established during management.

5 - Use Direct Instruction: Again because frontal cases are generally disorganised and have difficulty abstracting the relative importance of things for themselves, their teachers should state precise final and substage objectives.

6 - Provide Study Skills/Organisational Assistance: Under this heading, it is useful (a) to distribute practice over time, and to follow a shared written plan, and (b) to identify the "main idea" in any new material. 

7 - Provide Positive Feedback: Use "constructive timely feedback" to reinforce students' positive self-esteem.

At the same time, clinicians need to guard against doing too much of their patient's thinking for them. For example, Ylvisaker and Feeney (draft 2004 online) have reviewed the literature on paediatric frontal rehabilitation and identify the fundamental problem as one of measuring patients' "self-determination" in a clinician-patient encounter where the clinician is likely to be doing all the determining. They adopt Wehmeyer, Agran, and Hughes' (1998) analysis of self-determination into four components .....

(1) Autonomy: This is Wehmeyer, Agran, and Hughes' first self-determination factor, namely "acting in a way that is free from undue external influence or interference" (p2). 

(2) Self-Regulation: This is Wehmeyer, Agran, and Hughes' second self-determination factor, namely "formulating, enacting, and evaluating plans of action, with revisions as necessary" (p2). 

(3) Psychological Empowerment: This is Wehmeyer, Agran, and Hughes' third self-determination factor, namely "acting on the belief that one can influence important outcomes in the environment and in life" (p2). 

(4) Self-Realisation: This is Wehmeyer, Agran, and Hughes' fourth self-determination factor, namely "using a reasonably accurate knowledge of self (strengths and needs) and acting in a manner that capitalises on this knowledge in a beneficial way" (p2).

Ylvisaker and Feeney also echo Stuss and Benson's (1986) observation that "in the context of standardised assessment, the examiner and testing situation function as prosthetic frontal lobes" (p4). They therefore recommend "a distrust of clinical programs that fragment integrated aspects of human function and decontextualise the treatment" (p4), thus ..... 

"To be successful with any difficult task, children need to (a) know that it will be difficult (presupposing some awareness of strengths and limitations), (b) set a reasonable goal, (c) formulate (however unconsciously) a plan to achieve the goal, (d) initiate goal-directed action, (e) refrain from actions that interfere with success, (f) attend to and evaluate how well they are doing, and (g) try another plan or strategy if things are not going well, remaining optimistic about the possibility of success. In addition, they need to know that they can control the outcome of their efforts (at least to some degree) and take responsibility for that effort (ie. internal locus of control, Rotter, 1966)." (Ylvisaker and Feeney, 2003/2004 online, p4.)

14 - Adult Frontal Management Issues

The 1990s also saw tests increasingly being packed up as glossy and standardised commercial psychometrics products to sit alongside older packages such as the Halstead-Reitan and Luria-Nebraska batteries. A good example of this trend is Wilson et al's (1996) Behavioural Assessment of the Dysexecutive Syndrome (BADS) Test [glossary]. The package requires (a) the subject to complete six separate practical tests, and (b) both subject and carer(s) to complete a 20-item diagnostic questionnaire. The tests are as follows: (1) Temporal Judgement, (2) Rule Shifting, (3) Action Programme, (4) Key Search Task, (5) Zoo Map Task, and (6) Modified Six Elements Test [for the full "horse's mouth" history of the development of the BADS test, see Wilson et al (1998)]. Other commercially packaged assessments which wholly or partly address frontal processing include .....

Riddoch and Humphreys' (1993) Birmingham Object Recognition Battery (BORB)

Warrington's (1996) Camden Memory Test Battery

Langdon and Warrington's (1995) Verbal and Spatial Reasoning Test (VESPAR)

Dubois, Slachevsky, Litvan, and Pillon's (2000) Frontal Assessment Battery (FAB)

As summarised in Chayer (2002/2004 online), the designed-for-bedside FAB includes a similarities test, the WFT for the letter S, a motor imitation task, two Luria-type tapping tasks, and a particularly clever test of utilisation behaviour (QV).

As far as the generally "disinhibited" orbitofrontal patients are concerned, Varney and Menefee (1993) report the practical problems .....

"Patients with TBI, particularly when mild, may perform normally on a wide variety of neuropsychological measures and may appear relatively normal within the structure of standard psychological interviews. At the same time, they are often substantially impaired in independent self-determined 'adult' behaviours and activities of daily living. [.....] Patients with TBI may provide inaccurate histories, overreport or underreport symptomatology, and lack insight concerning their behaviour and its effects on others in their environment. [.....] even the most state-of-the-art testing fails to identify the manifestly disabled 50% of the time or more. Thus, it is essential that collateral informants be interviewed and vocational histories be obtained from sources other than the patient." (Varney and Menefee, 1993, pp33-41).

Jacobs (2004 online) is not happy that the Mini Mental Status Examination addresses frontal function, and suggests a "Maxi Mental" test to go with it. While this would need to evaluate the integrity of all four major cerebral lobes AND the lateralisation of their functions, its frontal aspects could be assessed using a combination of the Go/No-Go task, the WFT, and "Serial Seven Subtraction" tests, in conjunction with "general bedside and neuropsychological testing" for aphasia, dyspraxia, and neglect [see specific suggestions].

Unfortunately, nothing is ever easy in cognitive science, and clinicians will regularly face one essentially insoluble problem, namely that of deciding how much improvement to go for. The point is that not all "normal" adults attain Piagetian formal operational thought in the first place (Long, McCrary, and Ackerman, 1979; Shute, 1979), remaining concrete reasoners in adult bodies all their lives! Indeed, Shute and Huertas (1990) identify four specific formal operations which may have been more or less lacking in a frontal patient before their hospitalisation, namely (1) probabilistic reasoning, the ability to "reason past one's own experience", (2) propositional reasoning, the ability to "develop hypothetical solutions to presented problems", (3) combinatorial reasoning, the ability to "see the world in terms of possibilities rather than absolutes", and (4) proportional reasoning, the ability to "recognise the relationships between behaviours and the consequences of those behaviours" (p2). It follows that "if frontal lobe function spans a substantial range of performance among 'normal' individuals, the task of identifying frontal dysfunction is bound to be difficult" (p3).

There is also the care environment to take into account. Campbell, Duffy, and Salloway (1994) have argued for an element of "family therapy" when dealing with dysexecutive syndrome patients, thus .....

"Family therapy is an important and often neglected treatment modality in managing dysexecutive syndromes. The significant personality changes induced by frontal lobe impairment clearly destabilise the family system. When this is not recognised, optimal treatment cannot be achieved. A destabilised family system creates an ambiguous, emotionally charged, potentially toxic environment that affects the patient's behaviour in a decidedly negative way. Family therapy begins with education. Families must understand the patient's changed behaviour. Signs of executive dysfunction appear to the uninitiated as willful behaviour. Abulic [glossary] patients are often accused of being lazy or uncaring. Disinhibited patients appear insensitive. Disorganised patients with apparently normal cognitive abilities generate frustration. This adds considerably to the burden on family members who are struggling to cope with loss of the premorbid family system. The McMaster model of problem-centred systems family therapy provides a useful assessment and treatment tool for the families of patients with dysexecutive syndromes [Epstein, Bishop, and Levin (1978). This] model requires a careful assessment of six essential areas of family functioning: roles, problem solving, behaviour control, communication, affective involvement, and affective responsiveness [citation]. All six areas are affected by executive dysfunction. The model provides the basis for a structured treatment approach that focuses on the specific problems identified by the assessment. Active collaboration of the family is required, with the therapist acting as facilitator. The major objectives of therapy include family openness, clarity of communication, and the development of active problem solving skills. [..... Indeed,] the stepwise assessment of problem solving offered by the McMaster model clarifies this process for families in a logical way [and] disorganised patients respond well to the breakdown of problem solving into steps." (Campbell, Duffy, and Salloway, 1994, pp415-416.) [Click here for a McMaster Model slideshow, if interested.]

Finally, Wheatley and McGrath (1997/2004 online) warn that care staff should be aware that frontal patients' often all-pervading lack of initiative can easily lead to an unwarranted reputation for malingering. It is also important to remember that frontal patients - particularly the orbitofrontal ones - may have raised levels of anxiety, and that this itself may present management problems.

15 - The Cardiff Neurorehabilitation Conference, September 2002

For a week in September 2002, Cardiff City Hall played host to the great and good of frontal theory. Here are some of the points raised by the main speakers [in alphabetic order; page-numbered quotations from the Conference Abstracts; others from our personal session notes] .....

Paul Burgess (University College London, co-inventer of the Multiple Subgoal Task) agreed with Baddeley (1986) that the diagnostic term "frontal lobe syndrome" had had its day and should be replaced by "Dysexecutive Syndrome" (DES), because this latter better reflected the modern interest in the importance of function rather than the localisation of lesion. Names aside, though, his substantive point was that treatments can only really advance if we understand the system in question. Thus .....

"Considerable treatment advances have been made in this area in the last few years. However in order to develop new methods, and in some cases to explain the success or failure of existing ones, we need to understand the causes of the particular symptoms. For this reason rehabilitation can only proceed as fast as our knowledge about the basic brain systems that are damaged will allow." (Burgess, 2002, p7.)

Max Coltheart (Macquary University, co-author of the PALPA) set out to defend "the cognitive approach to rehabilitation" .....

"The theories of cognition which cognitive neuropsychology uses are modular: that is, they offer descriptions of what the particular information-processing components are that make up the cognitive system responsible for a person's performance in some particular cognitive domain. These descriptions are sufficiently explicit that they define what the actual functions of the components are, and so they tell us what tasks should be used to assess whether any particular component of the system is functioning normally or not. Cognitive neuropsychology thus automatically provides a guide to rational assessment. Examples of assessment batteries derived from theories in this way are PALPA (for assessing language; Kay, Lesser, and Coltheart, 1992) and BORB (for assessing visual perception and recognition; Riddoch and Humphreys, 1993). This kind of assessment allows targeted therapy programs to be devised. What it does not provide, at least not currently, are ideas regarding what form the targeted treatment should take. This is left up to the experience and ingenuity of the therapist." (Coltheart, 2002, p9)

Coltheart saw the primary clinical decision as being whether to go for "compensation" of a function or its "restoration". He then warned that this decision would never be easy until assessments were improved to the point of identifying whether neural resources for restoration were actually available.

John R. Crawford (University of Aberdeen) delivered a meta-analysis of a large number of frontal tests, including the WCST ("stressful and difficult") and the MCST. He expressed mild reservations about Shallice and Evans' (1978) CET, but was more positive about Shallice and Burgess's (1979) Brixton Spatial Anticipation Test and the BADS, both of which have large effect sizes. He, too, warned that the standard clinical tests were "too structured and examiner-led", and thus found it difficult "to capture the core problems of initiation, planning, and self-monitoring" (p9).

Jonathan Evans (MRC, Cambridge) addressed the question whether executive dysfunction could actually be restored or retrained. Like Burgess, he saw progress here as being constrained by "the lack of theoretical consistency in the concept of executive function" (p10). He then went on to review recent work attempting to remediate planning, problem solving, and goal management, before calling for "a theoretically coherent programme of methodologically rigorous research examining the biological, cognitive, and functional consequences of executive function retraining approaches" (ibid.). He was particularly enthusiastic about Lezak's work on goal management training [introduced in Section 6], and recommended recent applications of same by Brian Levine at the University of Toronto (eg. Levine et al, 2000 online abstract). As for the future, he foresaw a role for stem-cell based neural replacement therapies.

Elizabeth Glisky (University of Arizona) argued that modern approaches to memory rehabilitation showed a distinct improvement over remediation prior to the mid-1980s, "when the dominant approach to treatment focused on reducing or eliminating underlying memory impairment by repetitive drills and practice" (Glisky, 2002, p10). She was particularly insistent on the need for the "generalisation of training gains beyond the training context" (ibid.), but saw little value in simple repetitive practice unless it had day-to-day relevance. Moreover, although the nature of the brain's various memory systems implied that we often needed to stimulate the hippocampus, we actually had "no real idea" how to do so in practice, neither in terms of tasks which would "force episodic binding" nor of when to apply them if we had them. 

Like Coltheart, David Howard (University of Newcastle) spoke in defence of box-and-arrow modelling as an aid to clinical testing practice. Indeed, such approaches were more or less forced on us whenever processing took place in stages. However, he then added the caution that different patients had different breakdowns, but with only subtly different test results, making it difficult to target therapy appropriately. In summary .....

"..... both language production and comprehension involve complex and interacting brain systems, distributed over the cerebral cortex. The nature of the processing taking place in different brain regions is not yet fully understood." (p11)

Narinder Kapur (University of Southampton) reviewed current methods of memory assessment. As a clinician himself, he argued that it was vital for clinicians to grasp the theoretical differences between episodic [glossary], semantic [glossary], and procedural memory [glossary]. He also mentioned that disorientation for time was often a good index of severity of impairment. He was then asked what the best pack of three frontal tests would be, and recommended the WMS Paired Associate Learning subtest, the Camden memory tests, and a Face Recognition test.

ASIDE: To see how paired associate learning can be used as a screening task in the early detection of Alzheimer's disease, see Fowler et al (2002/2004 online)

Catherine Mateer (University of Victoria, British Columbia) pointed out that increased survival rates for TBI meant that these cases were now seen more often at the rehabilitation stage .....

"A number of basic assumptions and well-established principles for ethic and effective rehabilitation have been established. (1) Interventions that address cognitive impairments must be seen as a collaborative enterprise involving patients, family, professionals, and communities. (2) Interventions must be goal oriented and address practical and meaningful aspects of the person's everyday life. (3) Cognitive interventions are dynamic and often involve a combination of activities designed to maximise areas of cognitive functioning, to increase insight and awareness, and to identify and implement internal and external compensatory strategies. (4) Cognitive abilities are interlinked with behavioural, emotional, and psychosocial functioning and must be addressed in any effective treatment programme. (5) Effective neuropsychological rehabilitation relies on a broad theoretical base incorporating frameworks, models, and methodologies from many different fields of scientific, medical, neuropsychological, social, and ethical inquiry." (Mateer, 2002, p13.)

She went on to recommend that the critical elements for effective cognitive intervention were a broad range of activities, tailored to the individual, with multiple (but integrated) targets, and applied collaboratively with the carers involved. Cognitive behavioural interventions were only appropriate in cases where some insight and self-regulatory metacognition had been spared. 

One of Coltheart's co-workers, Lyndsey Nickels (Macquary University) reviewed the instruments available for assessing acquired language impairments. She saw the main purposes of assessment as differential diagnosis, subtype categorisation, and assessing quality of life, and pointed out that there would be big differences between the specific assessment tools chosen for each. She then recommended a "hypothesis testing" approach to client management. Clinicians should interact, observe, and then hypothesise; they "must have a theory", and they will regularly need to apply additional tests (chosen the many available). This might be anything from a formal test like the Boston to informal adhoc questioning. Moreover, it will often be necessary to do this "cyclically", that is to say, to keep repeating the process until "a focus for therapy" emerges. The best clinicians, she argued, are the ones who are most "acutely aware of the strengths and limitations of the assessment tools". 

Barbara Wilson (MRC, Cambridge, first author of the BADS package, and editor of the journal Neuropsychological Rehabilitation) discussed whether memory disabilities could ever be effectively treated .....

"It is these problems that should be targeted in rehabilitation. Although there is little evidence that rehabilitation can restore memory functioning, there is considerable evidence that disabilities can be treated effectively. For example, a randomised control trial allocating people to a paging system [..... found] convincing evidence that for the group as a whole and for the majority of people in the study, the paging system reduced everyday memory and planning problems." (Wilson, 2002, p16.)

She went on to stress that rehabilitation was a two-way interactive process .....

"No one model, theory, or framework, is sufficient to address the many and complex disabilities faced by people requiring cognitive rehabilitation. Models of cognitive functioning are necessary but not sufficient. We need to also refer to models of assessment, learning, behaviour, emotion, compensation, and recovery at the very least." (Wilson, 2002, p16.)

And finally, Andrew Worthington (Brain Injury Rehabilitation Trust, Birmingham) argued that the rehabilitation of executive disorders "remains in its infancy" (Worthington, 2002. p17), partly because cognitive neuropsychology "has been slow to embrace the complexity of executive functioning" .....

ASIDE: ..... which is fair comment, when one recalls that the large X-shaped psycholinguistic diagrams such as PALPA habitually and deliberately treat higher functions as an unanalysed black box. The authors did this deliberately, in order to make progress elsewhere, usually dwelling on the peripheral lexical processing routes implicated in dyslexia and speech production. The time has now come, in other words, to open up the black box once and for all, and it is because we fear that psychologists lack the technical modelling skills to do this that we have made available our e-tutorial on "How to Draw Cognitive Diagrams".

16 - References

See the Master References List

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