Medical Hypotheses 4: 311-323, 1978.
TKE
ANATOMYOF FDIOTION
V3notion moves us, hence the word itself." - Sir Charles Sherrington (1) J,P, Crawford, Stone House Hospital, Dartford, Kent, ENGLAND.
APSTRACT &otion is seen as a function of an autonomic system which pervades the cerebrum as much as the rest of the body. An emotional centre, or organ of mood, seems to exist in the hypothalamus, at the upper end of a reticular core rising through the brainstem, which initiates and co-ordinates vital impulses. The reticular formation (which may be identical with the centrencephalic integrating system) appears to contain adrenergic and cholinergic fibres and these may be central nervous elements of the autonomic system. Supporting evidence for this whole concept is presented from findings in brain self stimulation reward, the syndrome of central pain, posture and movement accompanying mood change, epileptic convulsions and progressive refinements in pre-frontal leucotomy. The limbic system is considered to subserve "on going" memory rather than mood, which appears to reach consciousness in the lateral temporal convexity, as a rule independently of awareness of peripheral somatic accompaniments of emotion. Mood Centrencephalic Vegetative Horme Autonomy Affect Emotions Motivation Hypothalamus Reticular Formation Autonomic Nervous System Sympathetic Nervous System
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Mood or Memory "¬ion is such an important function that its mechanism, whatever it is, should be placed on a structural basis." Few engaged in activities requiring formal psychological understanding would disagree with this statement, made by Papez in 1937 (2) in the summary to his still much invoked Proposed He did himself none the less add that his interpretMechanism of botion. ation of the facts available to him would have to stand the test of experimental and clinical experience if it was to be useful to science. As it happens, his concept that the distribution of emotional colouring to consciousness takes place via the limbic lobe, does not seem to have fulfilled these criteria, and those who still appear to accept that it has, perhaps for want of as anatomically clear-cut an alternative, only seem to be able to do so by ignoring the conflicting clinical and experimental findings which have accumulated since. Even at the time, Paper admitted to not presenting negative and contradictory evidence, although this may not then have amounted to much, as compared say to that already tending to refute the olfactory function which had been attributed to the limbic lobe by some. 'Observationswhich have been made over the intervening years, however, reveal a more consistent relationship between the limbic lobe and memory, than one between it and emotion. Thus bilateral damage at almost any point in the limbic circuit, whether this be hippocampus, fornix, mammillothalamic tract, anterior nucleus of the thalamus or cingulate cortex, interferes with the ability to retain in long term memory, clearly registered current events (3,4,5). Long term memories established before such bilateral damage occurs, remain intact. Relatively isolated failure of this so-called "on going" memory, is probably encountered most often by clinicians for the first time, in patients with Korsakow psychosis. To get over the apparent flaw in the Papez theory, it has been suggested that memory and emotion are indissolubly linked in normal mental life (6), but abnormal emotional states also indicate, as clearly as does interference with%n going" memory, that structure underlying these two functions can be separated. Thus it is commonplace in psychiatric practice to observe the usual varieties of endogenous mood change, whether mania, depression, anxiety or rage, without associated disturbance of '*ongoing" memory, and this is true even when such affective disorder is symptomatic of circumscribed lesions of the hypothalamus (7) rather than idiopathic. When therefore this particular form of amnesia is accompanied for example by elation or euphoria, as in Korsakow psychosis, such mood change is probably not due to damage to those strictly limbic elements which causes loss of memory, such as the mammillary body but to damage to closely adjacent hypothalamic nuclei (8) (vide infra). HYPOTHALAMUS
AS A CENTREOR
ORCAN OFMITOD
Expression and Feeling in botion At the outset of his Proposed Mechanism of Emotion, Papez states that "The term 'emotion' as commonly used implies two conditions: a way of acting
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and a way of feeling. The former is designated as emotional expression; the latter as emotional experience or subjective feeling." Since in the human subject emotional expression and emotional experience may be dissociated phenomena, as in pseudobulbar palsy and allied states (9,10,11), emotion as a subjective state must, he felt, be referred upward from the hypothalamus to the cortex. For unlike Head and Holmes (12) who considered the thalamus contained an essential organ and centre of consciousness for affective states, Paper maintained that participation of the cortex is essential to subjective emotional experience. In so doing, he accepted that aspect of Bard's (13) adaptation of Cannon's diencephalic theory of emotion, in which the hypothalamus (rather than the thalamus) discharges downward the motor impulses which produce emotional behaviour, and at the same time upward to the cortex the impulses which throw into action the processes which underlie emotional consciousness. He may have preferred to implicate connexions from the hypothalamus, relayed via the readily identifiable mammillothalamic tract to the cingular gyrus, as the route for primary cortical reception of emotional experience (rather than accept Cannon's (14) proposed route via the thalamus direct to the lateral cerebral convexity) partly because at the time the mammillary body seemed to give origin through the former to the main hypothalamic projection to the cerebral cortex, and partly because evidence then available suggested that emotional consciousness was not located primarily in the lateral cortex of the cerebral hemispheres. Papez did however refer to secondary radiation from the gyrus cinguli, to the temporal lobe in particular, via a conspicuous system of association fibres seen passing laterally and ventrally across the internal capsule in an experimental monkey after bilateral temporal lobectomy. Lateral radiation to the temporal lobe in particular, does now appear to be more relevant, because a study of patients who experience emotion as an intrinsic part of their ictal episodes (15), has established that such emotion usually occurs as an aspect of epileptic discharge in the cortex of the lateral convexity of the temporal lobe, not in the medial or limbic lobe surface of the cerebral hemisphere. This very fact, however, suggests that emotion probably does not arrive at the temporal cortex via the cingular projection referred to by Papez mentioned above, or it would reach consciousness in the cingular gyrus and be an aspect of ictal dischargethere. Nor is it likely to arrive via the fornix through which fibres descend to the mammillary body, rather than ascend to the temporal lobe. The temporal localisation through ictal phenomena of the subjective experience of mood seems beyond dispute, since it could thus sometimes be pinpointed as part of a Jacksonian march of epileptic events across the lateral temporal cortical convexity (15). The moods experienced in this way were the basic ones of depression, fear, rage and elation, i.e. the same four moods which as already indicated are commonly seen in psychiatric practice and which can be aroused by selective stimulation or destruction of the hypothalamus (see also below). It may be objected that if subjective experience of such mood depends upon localised cortical function, then agnosia for mood should be a more commonly encountered clinical entity, but perhaps such agnosia has yet to be recognised as underlying relevant aspects of the Kluver-Bucy syndrome , e.g. docility, loss of natural fear (16).
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Centrencephalic Reticulum Since Papee wrote his Proposed Mechanism of IGnotion,it so happens that his later work, on the reticular formation (17),has provided a more direct route between subthalamic diencephalic processes and the lateral cerebral convexity than the one he originally suggested via the cingular gurus to the temporal lobe. This more direct route is in keeping with Cannon's (14) concept in which he almost anticipated that the intralaminar *non-specific' (18) thalamic nuclei would become recognised as relays z; the ascending reticular formation (17,18). For Cannon (19) referred to neurones within and near the thalamus lying close to the relay in the sensory path from periphery to cortex, which when discharging in a particular combination, excite afferent paths to the cortex by direct connection or by irradiation, and add emotion to simple sensation. Papez (17) however, like others in the same field of enquiry, emphasized the relationship of the reticular formation to consciousness in general rather than to awareness of emotion in particular. Nevertheless De Jong (20) does now consider that the reticular formation in corresponding closely to Penfield's (21) proposed centrencephalic integrating system, may not only regulate awareness, wakefulness and alert attention, but also play an important part in controlling emotional states and behaviour. Others feel moreover that the hypothalamus could be regarded as part of the reticular formation (22,23)or at least that the brainstem reticular formation extends into the hypothalamus (24), the full significance of which may become clearer below. Cerebral Autonomic Theory &otional expression is certainly recognisable in its diencephalic downward discharge in terms of autonomic activity (vide infra), and this is in line with the hypothalamus having long been regarded as the head ganglion of the autonomic nervous system (25,26). It now however seems possible that it is also autonomic components which may be similarly involved in the diencephalit upward discharge to the cortex underlying emotional experience (27), judging partly by the effects on emotional expression and experience, of hypothalamic stimulation and destruction. For in the case of somatic expression (as opposed to psychic experience), the postero-lateral hypothalamic nuclei have been considered sympathetic and anteromedial nuclei parasympathetic, from the autonomic characteristics of caudal effects accompanying their stimulation (28), and as far as emotional experience is concerned, destruction of the anterior hypothalamic nuclei led to mania (8,28),and of the posterior nuclei to depression (28). On such an anatomico-clinical basis (29) I suggested in 1960 (30), that mania is predominantlv a sympathetic pattern, and depression a main1.v parasympathetic one, proposals which were reiterated in 1972 on purely biochemical and pharmacological grounds, in the cholinergic-adrenergic hypothesis of mania and depression, propounded by Janowslcyand his colleagues (31). Under the term adrenergic these authors appeared to include the monoamines noradrenaline, dopamine and serotonin, as I had also implied earlier (32), no doubt accounting for some of the ever increasing complexity of psychotropic pharmacology which is rapidly approaching that of the peripheral autonomic system (33). Anxiety and anger 314
in that order - are probably organised topographically somewhere between the anterior hypothalamic site for depression and the posterior one for elation (1,16), in keeping with their more evenly mixed parasympatheticsympathetic nature (vide infra). A completely sympathetic pattern of autonomic discharge is only seen in uninhibited action, whether this be in the direction of fight or flight. That there is corticopetal structure involved in this, moreover, is suggested by a cephalic autonomic component, i.e. a centrifugal system of noradrenergic neurones (M), being implicated not only in excitation or arousal but also in the drive of exploratory behaviour. This system may be part of the ascending reticular formation which has been shown to have both monoaminergic and cholinergic divisions (35,36,37,38) and these may convey emotion to consciousness. For moods arise as mixed sympathetic-parasympatheticentities when uninhibited action is checked, the particular mood relating roughly speaking to whether flight and failure (anxiety and depression) or fight and success (anger and elation) are the drive and outcome (39). In the former, as an example of such mixed autonomic patterns in mood, anxiety may be "expressed" as tachycardia and hypertension (sympathetic) as well as diarrhoea and frequency of micturition (parasympathetic). Similarly in endogenous depression one may get constipation and tears. The hypothalamic arrangements thus indicated may be thought of perhaps as autonomic neurones regrouped as a mood centre or organ to subserve emotion, somewhat as sensory fibres regroup on reaching the thalamus before they leave to subserve the cortical function of sensory discrimination (12). Whether, however, such upward autonomic discharge does convey emotional colouring to consciousness, either by the direct *non-specific' thalamic reticular route (17 18), or by less direct diffusion through the specific thalamic nuclei (24j, i.e. the pulvinar in the case of the temporal cortical convexity (40) remains to be established. In this task, introspective testimony does not help by enabling us for example to analyse emotional feeling (as opposed to emotional "expression") into recognisable components from which it may have been built up, in the way that sensory modalities like touch, vision and hearing (which mood may accompany) can be subjectively recognised as leading through stages of hierarchical association to the stream of consciousness in general (41). Nor does introspective testimony appear to indicate how we subjectively discriminate between one emotion and another, even though these may reach consciousness in areas of the lateral temporal cortex which are distinct from each other if adjacent and overlapping (15). The situation seems rather, to be comparable to that in drives like hunger, in which as a rule peripheral caudal accompaniments such as the pangs associated with gastric contractions are not essential to 'central' awareness of the drive (42). Such peripheral somatic accompaniments of drive, or of mood, e.g. abdominal sinking feelings (43), may be more concerned with the conscious locating of consummating organs (3), or with indicating the direction of appropriate action (39), e.g. sinking out of sight and harm's way.
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Drain Self Stimulation Despite the difficulties of grasping how it may enable mood to reach consciousness, additional supporting evidence for the cerebral autonomic basis of emotional experience as re-outlined here, does none the less come from a number of sources. Thus animal experiments in brain self stimulation reward seem to have established that pleasure or a sense of reward is associated with stimulation of mainly monoamine nerve fibre systems (44), and alarm, displeasure or a sense of punishment with stimulation of mainly cholinergic ones (37). Such apparently "pleasurable" activity in animals is presumed to have affective tone (45) and has been pharmacologically equated with hedonic states in human beings (37). The monoeminergic-cholinergic nerve fibre systems in question are moreover apparently focussed on the hypothalamus and its outposts from which they fan out, for as the stimulating probes were planted closer and closer to the lateral hypothalamus, the rewarding effects (for example) of self stimulation became more intense by all measures, and the thresholds were lowered (37). This suggests that it is the central springs of emotion which are being indirectly stimulated (through a diffuse system converging centripetally and perhaps antidromically from above) and not the circumscribed cortical area for consciously experiencing subjective emotion, which may however itself become aroused secondarily from those stimulated hypothalamic springs. Central Pain Such a lateral fanning out of fibres from the hypothalamus would also provide a better basis than would a limbic affective theory, for understanding the sensory phenomena in the syndrome of central pain when that is related to emotion (46). In that syndrome it may be recalled, lesions at any level of the sensory nervous system, from peripheral nerve to the convexity of the cerebral cortex (46), can lead to bouts of pain being experienced without peripheral stimulus to originate them. The nearer the lesion is to the thalamus, however, whether converging on it from peripheral nerve below or from discriminative cortex above (46), the more constantly is the clinical picture of such central pain found (47), and in its most marked degree it becomes a part of thalamic syndrome. The topography of this frequency distribution of central pain is understandable on the basis of a "partial lesion" (47) at the point of nervous injury, leading to an "artificial synapse" (48) between on the one hand radiating centrifugal hypothalamic affective efferents (49,50), and on the other pain fibres which in ascending converge centripetally on the thalamus, before centrifugally diverging from it again on their way to the cortex. "Sprouting* (51) of axons (even in the central nervous system) after partial lesions, could provide a suitable anatomical basis for such artificial synapses, "spontaneous" outbursts of central pain being precipitated through them by central excitation or emotion, for some element of drive or mood is seldom entirely absent or neutral in most people when awake, let alone those on tenterhooks in fear of another painful paroxysm. Interestingly in both the dysaesthetic syndromes of central pain and in self stimulation experiments, pleasure and displeasure can be mutually exclusive. In dysaesthetic syndromes discomfort is usually prepotent, although still capable of being 316
abolished or controlled by the arousal of massive enough pleasurable feelings (46). Mood, Posture and Movement Fanning out of fibres from the hypothalamus towards the lateral cerebral convexity would similarly provide a basis on which to account for certain motor accompaniments of mood change. Thus the generally flexed posture of dejection, and the weakness, slowness, reduced range and diminished spontaneity of movement seen in retarded depression, are all also characteristics of Parkinsonism (16). Depressive stupor may similarly be difficult to distinguish from akinetic mutism (52) and reticular connexion to the relevant thalemic nuclei and basal ganglia (53,54) may provide the structure upon which such motor accompaniments of mood change depend, contrary to the implications of Bard's adaptation of Cannon's diencephalic theory, namely that emotional "expression" or behaviour is always the outcome of hypothalamic downward discharge. Monoaminergic-cholinergic balance may not only be involved here in affective functions of the reticular formation, but also in the dopaminergic nigrostriatal pathway and its antagonists (55), for some instances of Parkinsonian rigidity and tremor respond either to dopamine or to anticholinergic drugs. The dopaminergic nigrostriatal pathway seems to have been accepted as an ascending tract of the brainstem reticular formation in the cat (23,56) and Bannister (57) has pointed out that the suebstantia nigra is part of a continuous column of pigmented monoaminergic cells, following the line of the general visceral efferent column extending upwards from the lateral horn of grey matter in the cord and including the locus coeruleus. Epileptiform Convulsions The relationship which exists between affect and epileptiform convulsions, whether of the idiopathic or therapeutic sort, also supports the concept of a centrencephalic origin for the changes in posture and movement which may accompany emotion. Loss and return of consciousness, as in petit ma1 or anaesthesia, on its own is not usually accompanied by a durable change of mood. Nor are the purely skeletal muscular aspects of a convulsion, since these can be almost totally eliminated in electroplexy by the use of muscle relaxants, without adversely influencing the therapeutic effect on mood. The central nervous clonic aspects of a convulsion do however seem essential to a reasonably durable change in mood, and such clonus is suggestive of alternating discharge or rebound in neural systems in opposing balance, e.g. perhaps those underlying decorticate and decerebrate postures respectively. It cannot however even be the central neural motor changes of the somatic as opposed to autonomic (28) division of the nervous system evident in emotion, which are in themselves responsible for the alteration in mood, since not all patients for example with Parkinsonism (45), are endogenously depressed. It is suggested therefore that in such affective disorder, it may be the proposed hypothalamo-reticular autonomic 'quickening' (58) of the somatic motor (e.g. extrapyramidal and pyramidal) amongst other neural systems which exhibits imbalance, and that this reaches a better overall 317
vegetative (vegeo = quicken) redistribution on rebound to consciousness after a convulsion. It may seem a logical inference at first sight from the somatic neural motor nature of clonic convulsions, that the affective illnesses most likely to respond to electroplexy are those with marked motor accompaniments, i.e. the retarded, mute and stuporose, or the overactive, garrulous patient; but whilst this may be true, in a convulsion there is probably also some readjustment of the autonomic balance in reticular *enlivening* (58) of the sensorium (parieto-occipito-temporalcortex). As already indicated, some of the dissociation which may be observed in disease of the human subject, between emotional expression and emotional experience, may thus lie in the motor role of the frontal lobes being distinct from the sensory functions of the parieto-occipito-temporal ones. Leucotomy The concept of fibres fanning out from the hypothalamus towards the frontal lobes to account for the postural motor aspects of mood, may likewise explain the direction which progressive refinements in prefrontal leucotomy procedures have taken. For as far as swinging the balance of endogenous mood towards elation in its drive is concerned, these refinements have gradually narrowed down the significant part of the prefrontal region to the postero-medial orbital cortex, thus progressively converging as it were from the white matter of the frontal convexity, downwards and medially towards the anterior hypothalamus. Martin's elated patient (10) who had a small meningioma between the lower parts of her frontal lobes, provides a comparable clinico%natomical narrowing of localisation within the frontal lobe, from the more diffuse frontal involvement by disease seen in say the grandiose elated forms of G.P.I. Limbic leucotomy (cingulectomy) on the other hand is more effective in relieving the symptoms of severe obsessional neurosis than those of affective disorder (59), again emphasizing the relation between the limbic lobe and memory rather than between it and emotion. For obsessional personality disorder has a relationship with memory (60), and by definition obsessive compulsive symptoms are as it were the very stuff of exaggerated retention, being exceptionally vivid, persistent, learned elements of consciousness which resist attempts to discard or forget them, only in the case of phobiae regularly containing the affective element of anxiety. In the circumstances, it may not be surprising that cingulectomy is often followed by a transient Korsakow confusional state (6), and the interference with "on going" memory which accompanies it.
Although the obvious relationship which exists between memory and emotion in normal mental life, may not usually depend largely on limbic lobe circuits, it may do so sometimes. For anxiety seems to have a special relationship to retention and recall, which may account for its particular presence in the phobic aspects of obsessional phenomena. Thus intense terror can lead to a panoramic recall or review of the events of a person's past in retrograde succession, and in vivid pictorial detail, right back from childhood
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in rapid sequence, as if unwinding a recording reel, or living one's life over again (61). This special relationship which exists between memory and anxiety may be phylogenetic in origin. It could have arisen perhaps, through special development of the mammillary bodies from hypothalamic anxious alerting mechanisms, much as in olfaction, which also exhibits a special relationship with memory, it may be through retained rhinencephalic limbic connexions. Certainly smell remains remarkably potent in awakening visual and other memories although the reverse is not true (61). CONCLUSION Central tiotive Horme There is nothing new in general about the basic concept running through this paper, namely that the cerebral hemispheres contain and are influenced by autonomic nervous elements. Thus J?ulton(28) reviewed the evidence for autonomic representation at all levels of the central nervous system, including thalamic, striatal and cortical. There is in the brain as he repeatedly states, much overlapping, intermingling and dovetailing of autonomic and somatic nervous function, these two divisions of the nervous system being interdependent. The interconnexion at all functional levels, which exists between specific and reticular 'non-specific* afferent systems (54) may be as much a manifestation of such dovetailing, even though it has been customary to date to exclude visceral afferents from the autonomic nervous system by definition. What does constitute a relatively new departure, is the pattern or anatomical whole into which I have once more assembled the detail re-outlined here, as well as additional material, outmoding decerebrate diagrams of the autonomic nervous system. In this, cerebral autonomic elements are not considered to represent significant encephalisation of autonomic function, in the sense that the hypothalamus is not seen as diminishing in size and importance as the same aspects of the cerebrum increase up the phylogenetic scale (62). For it seems'more likely that the hypothalamus maintains its central autonomic, emotive and hormic position of importance, with a remarkable uniformity of complex differentiation throughout the vertebrate series, particularly in mammals (63,64),as part of the reticular core (27,29). This reticulum seems to lie at the heart (car) of each individual or personality (30,7)and provides the neural equivalent in such multicellular organisms (17) of the chemical initiation of and integrating communication between life processes which must occur in the 'plasm' (archiplasm, kinoplasm, ergastoplasm) of unicellular ones (29). In the medulla, parts of this core, e.g. the respiratory centre (28,18), although automatic may only be related to the autonomic system in the sense that rhythmically beating heart muscle may in myology be akin to unstriped muscle, action in both being involuntary. Towards the upper end of the brainstem however even this distinction becomes blurred, since there are some parts of the core which are essential to adaptive response by a functioning mind (65), or to the attentive responsiveness which denotes the presence of a sentient being. Here central nervous reticular autonomy (27) seems almost to become synonymous with the independent activity of individual creatures, which does involve volition (66,58),perhaps through a neural (as opposed to endocrine) "cascading amplifier system" (67) of some kind. 319
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A
Princeton University Press,
TKE
ANATOMYOF FDIOTION
V3notion moves us, hence the word itself." - Sir Charles Sherrington (1) J,P, Crawford, Stone House Hospital, Dartford, Kent, ENGLAND.
APSTRACT &otion is seen as a function of an autonomic system which pervades the cerebrum as much as the rest of the body. An emotional centre, or organ of mood, seems to exist in the hypothalamus, at the upper end of a reticular core rising through the brainstem, which initiates and co-ordinates vital impulses. The reticular formation (which may be identical with the centrencephalic integrating system) appears to contain adrenergic and cholinergic fibres and these may be central nervous elements of the autonomic system. Supporting evidence for this whole concept is presented from findings in brain self stimulation reward, the syndrome of central pain, posture and movement accompanying mood change, epileptic convulsions and progressive refinements in pre-frontal leucotomy. The limbic system is considered to subserve "on going" memory rather than mood, which appears to reach consciousness in the lateral temporal convexity, as a rule independently of awareness of peripheral somatic accompaniments of emotion. Mood Centrencephalic Vegetative Horme Autonomy Affect Emotions Motivation Hypothalamus Reticular Formation Autonomic Nervous System Sympathetic Nervous System
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Mood or Memory "¬ion is such an important function that its mechanism, whatever it is, should be placed on a structural basis." Few engaged in activities requiring formal psychological understanding would disagree with this statement, made by Papez in 1937 (2) in the summary to his still much invoked Proposed He did himself none the less add that his interpretMechanism of botion. ation of the facts available to him would have to stand the test of experimental and clinical experience if it was to be useful to science. As it happens, his concept that the distribution of emotional colouring to consciousness takes place via the limbic lobe, does not seem to have fulfilled these criteria, and those who still appear to accept that it has, perhaps for want of as anatomically clear-cut an alternative, only seem to be able to do so by ignoring the conflicting clinical and experimental findings which have accumulated since. Even at the time, Paper admitted to not presenting negative and contradictory evidence, although this may not then have amounted to much, as compared say to that already tending to refute the olfactory function which had been attributed to the limbic lobe by some. 'Observationswhich have been made over the intervening years, however, reveal a more consistent relationship between the limbic lobe and memory, than one between it and emotion. Thus bilateral damage at almost any point in the limbic circuit, whether this be hippocampus, fornix, mammillothalamic tract, anterior nucleus of the thalamus or cingulate cortex, interferes with the ability to retain in long term memory, clearly registered current events (3,4,5). Long term memories established before such bilateral damage occurs, remain intact. Relatively isolated failure of this so-called "on going" memory, is probably encountered most often by clinicians for the first time, in patients with Korsakow psychosis. To get over the apparent flaw in the Papez theory, it has been suggested that memory and emotion are indissolubly linked in normal mental life (6), but abnormal emotional states also indicate, as clearly as does interference with%n going" memory, that structure underlying these two functions can be separated. Thus it is commonplace in psychiatric practice to observe the usual varieties of endogenous mood change, whether mania, depression, anxiety or rage, without associated disturbance of '*ongoing" memory, and this is true even when such affective disorder is symptomatic of circumscribed lesions of the hypothalamus (7) rather than idiopathic. When therefore this particular form of amnesia is accompanied for example by elation or euphoria, as in Korsakow psychosis, such mood change is probably not due to damage to those strictly limbic elements which causes loss of memory, such as the mammillary body but to damage to closely adjacent hypothalamic nuclei (8) (vide infra). HYPOTHALAMUS
AS A CENTREOR
ORCAN OFMITOD
Expression and Feeling in botion At the outset of his Proposed Mechanism of Emotion, Papez states that "The term 'emotion' as commonly used implies two conditions: a way of acting
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and a way of feeling. The former is designated as emotional expression; the latter as emotional experience or subjective feeling." Since in the human subject emotional expression and emotional experience may be dissociated phenomena, as in pseudobulbar palsy and allied states (9,10,11), emotion as a subjective state must, he felt, be referred upward from the hypothalamus to the cortex. For unlike Head and Holmes (12) who considered the thalamus contained an essential organ and centre of consciousness for affective states, Paper maintained that participation of the cortex is essential to subjective emotional experience. In so doing, he accepted that aspect of Bard's (13) adaptation of Cannon's diencephalic theory of emotion, in which the hypothalamus (rather than the thalamus) discharges downward the motor impulses which produce emotional behaviour, and at the same time upward to the cortex the impulses which throw into action the processes which underlie emotional consciousness. He may have preferred to implicate connexions from the hypothalamus, relayed via the readily identifiable mammillothalamic tract to the cingular gyrus, as the route for primary cortical reception of emotional experience (rather than accept Cannon's (14) proposed route via the thalamus direct to the lateral cerebral convexity) partly because at the time the mammillary body seemed to give origin through the former to the main hypothalamic projection to the cerebral cortex, and partly because evidence then available suggested that emotional consciousness was not located primarily in the lateral cortex of the cerebral hemispheres. Papez did however refer to secondary radiation from the gyrus cinguli, to the temporal lobe in particular, via a conspicuous system of association fibres seen passing laterally and ventrally across the internal capsule in an experimental monkey after bilateral temporal lobectomy. Lateral radiation to the temporal lobe in particular, does now appear to be more relevant, because a study of patients who experience emotion as an intrinsic part of their ictal episodes (15), has established that such emotion usually occurs as an aspect of epileptic discharge in the cortex of the lateral convexity of the temporal lobe, not in the medial or limbic lobe surface of the cerebral hemisphere. This very fact, however, suggests that emotion probably does not arrive at the temporal cortex via the cingular projection referred to by Papez mentioned above, or it would reach consciousness in the cingular gyrus and be an aspect of ictal dischargethere. Nor is it likely to arrive via the fornix through which fibres descend to the mammillary body, rather than ascend to the temporal lobe. The temporal localisation through ictal phenomena of the subjective experience of mood seems beyond dispute, since it could thus sometimes be pinpointed as part of a Jacksonian march of epileptic events across the lateral temporal cortical convexity (15). The moods experienced in this way were the basic ones of depression, fear, rage and elation, i.e. the same four moods which as already indicated are commonly seen in psychiatric practice and which can be aroused by selective stimulation or destruction of the hypothalamus (see also below). It may be objected that if subjective experience of such mood depends upon localised cortical function, then agnosia for mood should be a more commonly encountered clinical entity, but perhaps such agnosia has yet to be recognised as underlying relevant aspects of the Kluver-Bucy syndrome , e.g. docility, loss of natural fear (16).
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Centrencephalic Reticulum Since Papee wrote his Proposed Mechanism of IGnotion,it so happens that his later work, on the reticular formation (17),has provided a more direct route between subthalamic diencephalic processes and the lateral cerebral convexity than the one he originally suggested via the cingular gurus to the temporal lobe. This more direct route is in keeping with Cannon's (14) concept in which he almost anticipated that the intralaminar *non-specific' (18) thalamic nuclei would become recognised as relays z; the ascending reticular formation (17,18). For Cannon (19) referred to neurones within and near the thalamus lying close to the relay in the sensory path from periphery to cortex, which when discharging in a particular combination, excite afferent paths to the cortex by direct connection or by irradiation, and add emotion to simple sensation. Papez (17) however, like others in the same field of enquiry, emphasized the relationship of the reticular formation to consciousness in general rather than to awareness of emotion in particular. Nevertheless De Jong (20) does now consider that the reticular formation in corresponding closely to Penfield's (21) proposed centrencephalic integrating system, may not only regulate awareness, wakefulness and alert attention, but also play an important part in controlling emotional states and behaviour. Others feel moreover that the hypothalamus could be regarded as part of the reticular formation (22,23)or at least that the brainstem reticular formation extends into the hypothalamus (24), the full significance of which may become clearer below. Cerebral Autonomic Theory &otional expression is certainly recognisable in its diencephalic downward discharge in terms of autonomic activity (vide infra), and this is in line with the hypothalamus having long been regarded as the head ganglion of the autonomic nervous system (25,26). It now however seems possible that it is also autonomic components which may be similarly involved in the diencephalit upward discharge to the cortex underlying emotional experience (27), judging partly by the effects on emotional expression and experience, of hypothalamic stimulation and destruction. For in the case of somatic expression (as opposed to psychic experience), the postero-lateral hypothalamic nuclei have been considered sympathetic and anteromedial nuclei parasympathetic, from the autonomic characteristics of caudal effects accompanying their stimulation (28), and as far as emotional experience is concerned, destruction of the anterior hypothalamic nuclei led to mania (8,28),and of the posterior nuclei to depression (28). On such an anatomico-clinical basis (29) I suggested in 1960 (30), that mania is predominantlv a sympathetic pattern, and depression a main1.v parasympathetic one, proposals which were reiterated in 1972 on purely biochemical and pharmacological grounds, in the cholinergic-adrenergic hypothesis of mania and depression, propounded by Janowslcyand his colleagues (31). Under the term adrenergic these authors appeared to include the monoamines noradrenaline, dopamine and serotonin, as I had also implied earlier (32), no doubt accounting for some of the ever increasing complexity of psychotropic pharmacology which is rapidly approaching that of the peripheral autonomic system (33). Anxiety and anger 314
in that order - are probably organised topographically somewhere between the anterior hypothalamic site for depression and the posterior one for elation (1,16), in keeping with their more evenly mixed parasympatheticsympathetic nature (vide infra). A completely sympathetic pattern of autonomic discharge is only seen in uninhibited action, whether this be in the direction of fight or flight. That there is corticopetal structure involved in this, moreover, is suggested by a cephalic autonomic component, i.e. a centrifugal system of noradrenergic neurones (M), being implicated not only in excitation or arousal but also in the drive of exploratory behaviour. This system may be part of the ascending reticular formation which has been shown to have both monoaminergic and cholinergic divisions (35,36,37,38) and these may convey emotion to consciousness. For moods arise as mixed sympathetic-parasympatheticentities when uninhibited action is checked, the particular mood relating roughly speaking to whether flight and failure (anxiety and depression) or fight and success (anger and elation) are the drive and outcome (39). In the former, as an example of such mixed autonomic patterns in mood, anxiety may be "expressed" as tachycardia and hypertension (sympathetic) as well as diarrhoea and frequency of micturition (parasympathetic). Similarly in endogenous depression one may get constipation and tears. The hypothalamic arrangements thus indicated may be thought of perhaps as autonomic neurones regrouped as a mood centre or organ to subserve emotion, somewhat as sensory fibres regroup on reaching the thalamus before they leave to subserve the cortical function of sensory discrimination (12). Whether, however, such upward autonomic discharge does convey emotional colouring to consciousness, either by the direct *non-specific' thalamic reticular route (17 18), or by less direct diffusion through the specific thalamic nuclei (24j, i.e. the pulvinar in the case of the temporal cortical convexity (40) remains to be established. In this task, introspective testimony does not help by enabling us for example to analyse emotional feeling (as opposed to emotional "expression") into recognisable components from which it may have been built up, in the way that sensory modalities like touch, vision and hearing (which mood may accompany) can be subjectively recognised as leading through stages of hierarchical association to the stream of consciousness in general (41). Nor does introspective testimony appear to indicate how we subjectively discriminate between one emotion and another, even though these may reach consciousness in areas of the lateral temporal cortex which are distinct from each other if adjacent and overlapping (15). The situation seems rather, to be comparable to that in drives like hunger, in which as a rule peripheral caudal accompaniments such as the pangs associated with gastric contractions are not essential to 'central' awareness of the drive (42). Such peripheral somatic accompaniments of drive, or of mood, e.g. abdominal sinking feelings (43), may be more concerned with the conscious locating of consummating organs (3), or with indicating the direction of appropriate action (39), e.g. sinking out of sight and harm's way.
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Drain Self Stimulation Despite the difficulties of grasping how it may enable mood to reach consciousness, additional supporting evidence for the cerebral autonomic basis of emotional experience as re-outlined here, does none the less come from a number of sources. Thus animal experiments in brain self stimulation reward seem to have established that pleasure or a sense of reward is associated with stimulation of mainly monoamine nerve fibre systems (44), and alarm, displeasure or a sense of punishment with stimulation of mainly cholinergic ones (37). Such apparently "pleasurable" activity in animals is presumed to have affective tone (45) and has been pharmacologically equated with hedonic states in human beings (37). The monoeminergic-cholinergic nerve fibre systems in question are moreover apparently focussed on the hypothalamus and its outposts from which they fan out, for as the stimulating probes were planted closer and closer to the lateral hypothalamus, the rewarding effects (for example) of self stimulation became more intense by all measures, and the thresholds were lowered (37). This suggests that it is the central springs of emotion which are being indirectly stimulated (through a diffuse system converging centripetally and perhaps antidromically from above) and not the circumscribed cortical area for consciously experiencing subjective emotion, which may however itself become aroused secondarily from those stimulated hypothalamic springs. Central Pain Such a lateral fanning out of fibres from the hypothalamus would also provide a better basis than would a limbic affective theory, for understanding the sensory phenomena in the syndrome of central pain when that is related to emotion (46). In that syndrome it may be recalled, lesions at any level of the sensory nervous system, from peripheral nerve to the convexity of the cerebral cortex (46), can lead to bouts of pain being experienced without peripheral stimulus to originate them. The nearer the lesion is to the thalamus, however, whether converging on it from peripheral nerve below or from discriminative cortex above (46), the more constantly is the clinical picture of such central pain found (47), and in its most marked degree it becomes a part of thalamic syndrome. The topography of this frequency distribution of central pain is understandable on the basis of a "partial lesion" (47) at the point of nervous injury, leading to an "artificial synapse" (48) between on the one hand radiating centrifugal hypothalamic affective efferents (49,50), and on the other pain fibres which in ascending converge centripetally on the thalamus, before centrifugally diverging from it again on their way to the cortex. "Sprouting* (51) of axons (even in the central nervous system) after partial lesions, could provide a suitable anatomical basis for such artificial synapses, "spontaneous" outbursts of central pain being precipitated through them by central excitation or emotion, for some element of drive or mood is seldom entirely absent or neutral in most people when awake, let alone those on tenterhooks in fear of another painful paroxysm. Interestingly in both the dysaesthetic syndromes of central pain and in self stimulation experiments, pleasure and displeasure can be mutually exclusive. In dysaesthetic syndromes discomfort is usually prepotent, although still capable of being 316
abolished or controlled by the arousal of massive enough pleasurable feelings (46). Mood, Posture and Movement Fanning out of fibres from the hypothalamus towards the lateral cerebral convexity would similarly provide a basis on which to account for certain motor accompaniments of mood change. Thus the generally flexed posture of dejection, and the weakness, slowness, reduced range and diminished spontaneity of movement seen in retarded depression, are all also characteristics of Parkinsonism (16). Depressive stupor may similarly be difficult to distinguish from akinetic mutism (52) and reticular connexion to the relevant thalemic nuclei and basal ganglia (53,54) may provide the structure upon which such motor accompaniments of mood change depend, contrary to the implications of Bard's adaptation of Cannon's diencephalic theory, namely that emotional "expression" or behaviour is always the outcome of hypothalamic downward discharge. Monoaminergic-cholinergic balance may not only be involved here in affective functions of the reticular formation, but also in the dopaminergic nigrostriatal pathway and its antagonists (55), for some instances of Parkinsonian rigidity and tremor respond either to dopamine or to anticholinergic drugs. The dopaminergic nigrostriatal pathway seems to have been accepted as an ascending tract of the brainstem reticular formation in the cat (23,56) and Bannister (57) has pointed out that the suebstantia nigra is part of a continuous column of pigmented monoaminergic cells, following the line of the general visceral efferent column extending upwards from the lateral horn of grey matter in the cord and including the locus coeruleus. Epileptiform Convulsions The relationship which exists between affect and epileptiform convulsions, whether of the idiopathic or therapeutic sort, also supports the concept of a centrencephalic origin for the changes in posture and movement which may accompany emotion. Loss and return of consciousness, as in petit ma1 or anaesthesia, on its own is not usually accompanied by a durable change of mood. Nor are the purely skeletal muscular aspects of a convulsion, since these can be almost totally eliminated in electroplexy by the use of muscle relaxants, without adversely influencing the therapeutic effect on mood. The central nervous clonic aspects of a convulsion do however seem essential to a reasonably durable change in mood, and such clonus is suggestive of alternating discharge or rebound in neural systems in opposing balance, e.g. perhaps those underlying decorticate and decerebrate postures respectively. It cannot however even be the central neural motor changes of the somatic as opposed to autonomic (28) division of the nervous system evident in emotion, which are in themselves responsible for the alteration in mood, since not all patients for example with Parkinsonism (45), are endogenously depressed. It is suggested therefore that in such affective disorder, it may be the proposed hypothalamo-reticular autonomic 'quickening' (58) of the somatic motor (e.g. extrapyramidal and pyramidal) amongst other neural systems which exhibits imbalance, and that this reaches a better overall 317
vegetative (vegeo = quicken) redistribution on rebound to consciousness after a convulsion. It may seem a logical inference at first sight from the somatic neural motor nature of clonic convulsions, that the affective illnesses most likely to respond to electroplexy are those with marked motor accompaniments, i.e. the retarded, mute and stuporose, or the overactive, garrulous patient; but whilst this may be true, in a convulsion there is probably also some readjustment of the autonomic balance in reticular *enlivening* (58) of the sensorium (parieto-occipito-temporalcortex). As already indicated, some of the dissociation which may be observed in disease of the human subject, between emotional expression and emotional experience, may thus lie in the motor role of the frontal lobes being distinct from the sensory functions of the parieto-occipito-temporal ones. Leucotomy The concept of fibres fanning out from the hypothalamus towards the frontal lobes to account for the postural motor aspects of mood, may likewise explain the direction which progressive refinements in prefrontal leucotomy procedures have taken. For as far as swinging the balance of endogenous mood towards elation in its drive is concerned, these refinements have gradually narrowed down the significant part of the prefrontal region to the postero-medial orbital cortex, thus progressively converging as it were from the white matter of the frontal convexity, downwards and medially towards the anterior hypothalamus. Martin's elated patient (10) who had a small meningioma between the lower parts of her frontal lobes, provides a comparable clinico%natomical narrowing of localisation within the frontal lobe, from the more diffuse frontal involvement by disease seen in say the grandiose elated forms of G.P.I. Limbic leucotomy (cingulectomy) on the other hand is more effective in relieving the symptoms of severe obsessional neurosis than those of affective disorder (59), again emphasizing the relation between the limbic lobe and memory rather than between it and emotion. For obsessional personality disorder has a relationship with memory (60), and by definition obsessive compulsive symptoms are as it were the very stuff of exaggerated retention, being exceptionally vivid, persistent, learned elements of consciousness which resist attempts to discard or forget them, only in the case of phobiae regularly containing the affective element of anxiety. In the circumstances, it may not be surprising that cingulectomy is often followed by a transient Korsakow confusional state (6), and the interference with "on going" memory which accompanies it.
Although the obvious relationship which exists between memory and emotion in normal mental life, may not usually depend largely on limbic lobe circuits, it may do so sometimes. For anxiety seems to have a special relationship to retention and recall, which may account for its particular presence in the phobic aspects of obsessional phenomena. Thus intense terror can lead to a panoramic recall or review of the events of a person's past in retrograde succession, and in vivid pictorial detail, right back from childhood
318
in rapid sequence, as if unwinding a recording reel, or living one's life over again (61). This special relationship which exists between memory and anxiety may be phylogenetic in origin. It could have arisen perhaps, through special development of the mammillary bodies from hypothalamic anxious alerting mechanisms, much as in olfaction, which also exhibits a special relationship with memory, it may be through retained rhinencephalic limbic connexions. Certainly smell remains remarkably potent in awakening visual and other memories although the reverse is not true (61). CONCLUSION Central tiotive Horme There is nothing new in general about the basic concept running through this paper, namely that the cerebral hemispheres contain and are influenced by autonomic nervous elements. Thus J?ulton(28) reviewed the evidence for autonomic representation at all levels of the central nervous system, including thalamic, striatal and cortical. There is in the brain as he repeatedly states, much overlapping, intermingling and dovetailing of autonomic and somatic nervous function, these two divisions of the nervous system being interdependent. The interconnexion at all functional levels, which exists between specific and reticular 'non-specific* afferent systems (54) may be as much a manifestation of such dovetailing, even though it has been customary to date to exclude visceral afferents from the autonomic nervous system by definition. What does constitute a relatively new departure, is the pattern or anatomical whole into which I have once more assembled the detail re-outlined here, as well as additional material, outmoding decerebrate diagrams of the autonomic nervous system. In this, cerebral autonomic elements are not considered to represent significant encephalisation of autonomic function, in the sense that the hypothalamus is not seen as diminishing in size and importance as the same aspects of the cerebrum increase up the phylogenetic scale (62). For it seems'more likely that the hypothalamus maintains its central autonomic, emotive and hormic position of importance, with a remarkable uniformity of complex differentiation throughout the vertebrate series, particularly in mammals (63,64),as part of the reticular core (27,29). This reticulum seems to lie at the heart (car) of each individual or personality (30,7)and provides the neural equivalent in such multicellular organisms (17) of the chemical initiation of and integrating communication between life processes which must occur in the 'plasm' (archiplasm, kinoplasm, ergastoplasm) of unicellular ones (29). In the medulla, parts of this core, e.g. the respiratory centre (28,18), although automatic may only be related to the autonomic system in the sense that rhythmically beating heart muscle may in myology be akin to unstriped muscle, action in both being involuntary. Towards the upper end of the brainstem however even this distinction becomes blurred, since there are some parts of the core which are essential to adaptive response by a functioning mind (65), or to the attentive responsiveness which denotes the presence of a sentient being. Here central nervous reticular autonomy (27) seems almost to become synonymous with the independent activity of individual creatures, which does involve volition (66,58),perhaps through a neural (as opposed to endocrine) "cascading amplifier system" (67) of some kind. 319
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