Course Handout - The Limbic System, Motivation, and Drive
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 15:00 BST 23rd September 2003, Copyright Derek J. Smith (Chartered Engineer). This version [HT.1 - transfer of copyright] dated 18:00 14th January 2010
Earlier versions of this material appeared in Smith (1996; Chapter 4) and Smith (1997; Chapter 4). It is simplified here and supported with hyperlinks.
1 - The Anatomy of the Diencephalon
The diencephalon (or "between" brain, because it is between the bulk of the forebrain and the midbrain) is the most rostral part of the brainstem, and projects upwards into the space beneath and between the cerebral hemispheres. At its highest point and separated by the third ventricle, are the left and right thalami. Beneath the thalamus is the hypothalamus. Four important arched structures run nearly full circle around the third ventricle to link up a host of diencephalic and deep telencephalic nuclei. (1) The arch of the fornix is the nearest to the midline. It begins rostrally at the mammillary body, ascends as the column of the fornix, passes backwards as the body of the fornix, and then descends to connect with the hippocampus. (2) The arch of the stria medullaris has the smallest radius of all. It begins rostrally in the septal nuclei (just in front of the anterior commissure), passes over the thalamus to the habenular nucleus, and then descends through the fasciculus retroflexus to the midbrain interpeduncular nucleus. (3) Between (1) and (2), the arch of the stria terminalis links the septal nuclei to the amygdala. (4) The arch of the longitudinal striae has the greatest radius of all. It also begins rostrally in the septal nuclei, but then loops around above the corpus callosum to help feed the hippocampus.
2 - The Functions of the Diencephalon
The tradition of studying the electrical activity of the brain with electrodes goes back to the late nineteenth century. Starting with such workers as Fritsch and Hitzig (1870) and Ferrier (1876), there were repeated studies of what happened when a voltage was applied to the exposed surface of the cerebrum. This changed in 1909 when Victor Horsley developed the stereotaxic frame which could be fixed to the outside of the subject's skull to allow precise angles of introduction for the electrodes. This allowed them to be inserted more deeply into the neural tissue without causing too much damage. The new method was used to map the nuclei of the thalamus and hypothalamus, and there were some notable successes in the 1940s and 1950s (see below). Nowadays, thanks to ever finer microelectrode technology, modern neurobiologists can go "inside" an organism at the moment that it is displaying an instinctive behaviour, and have begun to analyse the corresponding neural activity at the level of the individual neurons. In the following subsections, we look at the most important components.
2.1 The Amygdala
The amygdaloid nuclear complexes are pea sized/shaped clusters of nuclei situated at the base of each temporal lobe, and receiving inputs from the hypothalamus and the olfactory areas. They contribute to a variety of emotional and instinctive behaviours. Kluver and Bucy (1937) found a whole syndrome of behavioural changes following amygdaloid lesion, including decreased belligerence, reduction of fear to previously fear-inducing stimuli (such as humans), a tendency to investigate everything by mouthing it, and increased and inappropriate sexual behaviour. Pribram (1962) reported major changes in the dominance hierarchy of rhesus monkeys following amygdalectomy. Kling and Mass (1974) also investigated how these animals behaved when released into the wild, and observed rejection of positive social gestures from normal group members, with the result that they became solitary. Passingham (1993) points to a possible explanation:
"Both temporal cortex and prefrontal cortex are linked with the amygdala. The amygdala is involved in the process by which stimuli are associated with reward [Ref]. If the connections between the temporal cortex and the amygdala are cut, the animals are poor at learning associations between stimuli and reward....." (Passingham, 1993, p170; emphasis added.)
And McGaugh (1993) explains this in human terms as the ability to remember the emotional significance of a memory. Without the amygdala, you would be able to create new memories, but unable to remember why they were important. You might remember the fact of being insulted, say, but not its emotional impact.
2.2 The Thalamus
The thalami are egg-shaped (and nearly egg-sized) clusterings of nuclei situated on either side of the third ventricle. The rostral end of the complex is more pointed than the caudal, and the component nuclei are squeezed in together like a tightly compressed bunch of grapes. The large nucleus at the caudal end is called the pulvinar nucleus. Thalamic nuclei actually belong to three distinct categories. Firstly, there are sensory relay nuclei, which are relay points within the ascending sensory pathways (every one of the senses, except that of smell). They contain (depending upon which pathway you are talking about) either second or third order sensory neurons - the highest order neurons of those sensory pathways. They receive information from the lower order sensory neurons, before firing in turn and projecting that information up to the corresponding primary projection areas. Under the pulvinar nucleus, for example, lie the geniculate bodies. These consist of an inner (medial) and an outer (lateral) nucleus under each of the thalami. The medial geniculate bodies are relay points on the auditory pathway, and the lateral geniculate bodies are relay points on the visual pathway. Somaesthetic information ascending in the medial lemniscus relays in the ventroposterior lateral nucleus (the "VPL") before projecting to the primary sensory areas (Areas 1 to 3).
Secondly, there are a class of nuclei known as association nuclei. These are not related to sensory systems, but simply project to the association areas of the cerebral cortex. The pulvinar nucleus, for example, receives information from the inferior and superior colliculi, and transmits to the association areas of the parieto-temporal cortex. Similarly, the dorsomedial nucleus receives information from the amygdala and transmits to "practically the entire frontal cortex rostral to areas 6 and 32. After [prefrontal lobotomy] nearly all small cells of the [dorsomedial] nucleus degenerate" (Carpenter, 1991, p258). Similarly, Crosby, Humphrey, and Lauer (1962) describe thalamocortical radiations from the dorsomedial nucleus to prefrontal cortex (Areas 9 and 10), and argue that these convey affective tone from lower centres to consciousness. In truth, however, most of the cortex is in some way excited by the thalamus, and the thalami are heavily implicated by many state of the art theories of consciousness (typically, Crick, 1984, and Newman, 1997). Crick (1984) likens the thalamic reticular nuclei to an "internal attentional searchlight", constantly deciding which cortical areas need to be activated next.
And finally, there are a class of nuclei known as intrinsic nuclei. These, too, are not related to sensory systems, nor do they project to the cerebral cortex at all. Instead, they interconnect with other structures making up the limbic system, and seem to play a role in maintaining the EEG activity of the cortex. The anterior nuclear group falls into this category, receiving information from the fornix via the mammillothalamic tract, and transmitting to the cingulate gyrus.
2.3 - The Hypothalamus and the Pituitary Gland
The hypothalamus is a group of nuclei beneath and between the thalami, and forming the base of the third ventricle. Hypothalamic nuclei are small (the entire adult hypothalamus only weighs about 4gm), and are involved in what are known as "homeostatic" functions (see panel), namely temperature control, sexual behaviour, thirst, hunger, and other visceral, endocrine, and metabolic activities. In particular, the hypothalamus controls the activity of the pituitary gland, and thus the activity of the endocrine system.
Key Concept - Homeostasis: The task of maintaining a whole range of bodily variables (temperature, oxygen levels, water levels, blood glucose) within acceptable limits is known as homeostasis (Greek = "staying the same"). The hypothalamic nuclei are involved in many of these homeostatic duties.
The pituitary gland (or hypophysis) is a gland weighing about 0.5 gm situated beneath - and innervated by - the hypothalamus. It is heavily involved in the neural regulation of endocrine functions. (Indeed, it is the principle point of contact between the neural and the endocrine branches of the body's control systems.) It contains two embryologically, microstructurally, and functionally separate lobes, the anterior pituitary gland, and the posterior pituitary gland. The anterior pituitary gland (or adenohypophysis) derives embryologically from oral ectoderm, and constitutes about 75% of the total gland by weight. It is not innervated as such by the hypothalamus, but receives instructions hormonally via the hypophyseal portal system of capillaries. It secretes several important hormones in turn, controlling thyroids, gonads, adrenal cortex, and other endocrine system glands (see panel). The posterior pituitary gland (or neurohypophysis) derives embryologically from neural ectoderm. It is concerned with storage and release of vasopressin (the antidiuretic hormone, ADH, which regulates water balance via its action on the kidney, and blood pressure via its vasoconstrictive action on the blood vessels) and oxytocin (which controls various uterine and mammary functions).
Mini-Glossary - The Endocrine System
Adrenal Glands: A left-right pair of endocrine glands situated above the kidneys.
Adrenalin: One of the two possible secretions from the adrenal glands.
Adrenocorticotrophic Hormone (ACTH): The "stress" hormone. An anterior pituitary secretion - a 39 amino acid peptide - which (a) induces the adrenal glands to secrete corticosteroids such as cortisol, and (b) stimulates fat mobilisation.
Androgen: Any hormone which acts as a male sex hormone, inducing the production of spermatozoa.
Anti-Diuretic Hormone (ADH): See vasopressin.
Follicle Stimulating Hormone (FSH): A pituitary secretion - a glycoprotein - which induces enlargement of the ovarian follicles.
Gonadotrophic Hormones: The two pituitary secretions which act upon the gonads. See follicle stimulating hormone and luteinising hormone.
Growth Hormone: A pituitary secretion - a 190 amino acid protein - which induces skeleto-muscular growth.
Lactogenic Hormone: See prolactin.
Luteinising Hormone: A pituitary secretion which stimulates the corpora lutea of the ovary.
Oestradiol: An oestrogen. An ovarian follicle secretion which induces female secondary sex characteristics.
Oestrogen: Any hormone which acts as a female sex hormone.
Oxytocin: A hypothalamic secretion released via the posterior pituitary gland which induces uterine contractions and the delivery of milk.
Progesterone: An ovarian luteal secretion which prepares the uterus to receive the fertilised egg.
Prolactin: A pituitary secretion - a 198 amino acid protein - which induces the production of milk.
Thyrotrophic Hormone: An anterior pituitary secretion which stimulates the thyroid gland to produce the hormones thyroxine and tri-iodothyronine which enhance cellular oxygen metabolism.
Vasopressin: A hypothalamic secretion released via the posterior pituitary gland which inhibits the production of urine.
3 - The Limbic System
Although the diencephalon is a subcortical set of structures, its functions in higher animals are intimately linked with two of the phylogenetically older areas of the cerebral cortex, namely the cingulate and hippocampal gyri. The telencephalon and diencephalon are here anatomically separate but heavily interrelated functionally, and the region is sometimes known as the rhinencephalon (or "smell" brain) because it contains those brain areas concerned originally with olfaction. The limbic system in general serves instinctive, motivational, and emotional behaviour. It also shares structures with the brain's awareness and memory systems.
It was James W. Papez (1883-1958) who first properly emphasised the role of the diencephalon in emotional behaviour (Papez, 1937). He extended Broca's (1878) use of the term limbic lobe - the areas of cerebral cortex closest to the diencephalon - and argued that it would be more helpful to think in terms of neural "circuits" linking these telencephalic and diencephalic structures together. He called these circuits the limbic system. The structures most commonly identified as belonging to the limbic system are the limbic cortex (the cingulate and hippocampal gyri, the largely olfactory areas of cortex in the region of the uncus), the hippocampus, the fornix, the mammillary bodies, the hypothalamus, the septal region, the thalamus, and the amygdala.
Walter Hess (1881-1973) [timeline] was one of the pioneers of electrode studies of subcortical structures in general (various from 1928). Using a stimulation paradigm he obtained various manifestations of rage from many points within the brainstem (Hess, 1928) He also developed the technique of electro-coagulation, whereby tiny localised neural lesions are inflicted by heating an implanted electrode. This enables the activity of a given centre to be permanently suppressed rather than temporarily enhanced. In other words, the centre is switched off rather than on, and the behavioural effects of the switching off are typically the opposite of those of the switching on. Erich Von Holst carried out similar stimulation experiments (for example, Von Holst and Von Saint Paul, 1960) with chickens, and found that highly specific behaviours could be electrically elicited in the absence of the normal external stimulus. These behaviours fell into two distinct categories. Firstly, there were simple movements such as sitting, standing, preening, stretching, etc., and secondly, there were more complex behaviour sequences such as seeking and eating food, seeking and drinking water, escape behaviour, and (in roosters) the sequence of guiding a hen to the nest. The true complexity of the limbic system's involvement in emotional behaviour is brought out by Robinson (1976):
"A wide and at times bewildering variety of responses has been elicited from limbic structures . These responses defy simple categorisation but fall into three broad groups. First there are a number of simple or fragmentary responses that can be evoked from virtually all limbic tissue. Various autonomic reactions such as urination, defecation, penile erection, ejaculation, piloerection, salivation, and changes in heart rate, blood pressure, pupillary size, body temperature, and respiratory rate and depth are frequently seen.  Second, at a higher level of complexity, more organised behavioural patterns can emerge from limbic system activation, particularly if the animal is unrestrained and is in an appropriate environmental and social setting with other animals. Organised aggression, fighting, fear reactions, defensive and escape responses, sexual activity with mating and ejaculation, feeding, and drinking can all be seen in full natural complexity.  Third, an even more complex class of behaviours  is demonstrated by giving the experimental animal the ability to turn the electrical stimulation on or off. These motivational behaviours, termed self-stimulation, escape-from-stimulation, and avoidance-of-stimulation, may be related to feelings of pleasure or displeasure....." (Robinson, 1976:762.)
Robinson's third class of behaviours was discovered by another of the early workers, James Olds (eg. Olds and Milner, 1954). Olds discovered that animals would press a lever to deliver mild electrical excitation to certain brain loci. This indicated that these areas seemed in some way to be saying: "This is nice, do it again". They are where the reinforcement of operant behaviour seems to be controlled from. Olds called these areas reward centres. Such reward sites are common in the septal region of the diencephalon of the rat, and they are important because they allow an innate piece of circuitry to control all operant learning, thus massively influencing behaviour. The limbic system, in other words, not only mediates much innate behaviour but also chooses which of the enormous variety of possible acquired behaviours ought to be acquired!
Pribram and Kruger (1954, cited in Deutsch and Deutsch, 1966) carried Papez's analysis one step further, and identified three limbic subsystems as follows:
(a) Smell-Connected: These structures (the rhinal group) have direct connections to the olfactory bulb, and include the lateral and medial olfactory striae, the olfactory tubercle, the prepyriform cortex (an area of cortex lying rostral to the hippocampal gyrus), and parts of the amygdala.
(b) Smell-Related: These structures (the paleol group) have no direct connections to the olfactory bulb, but are closely connected to those which have. They include the subcallosal cortex, the fronto-temporal cortex, the septal nuclei of the amygdala, and parts of the basal ganglia.
(c) Other: These structures (the hippocampal-cingulate group) have no direct connections to either the olfactory bulb or the rhinal group, but are closely connected to the paleol group. They include the hippocampus itself, as well as the hippocampal gyrus (next to the hippocampus) and the cingulate gyrus.
Deutsch and Deutsch (1966) caution against over-classifying, however, on the grounds that, until the exact function of the component parts is known, all classifications are rather arbitrary. And, as emerges in several of the following subsections, the exact function of the component parts remains largely confused and contradictory.