amygdala functions within the alimentary system · and basolateral parts, but in the cat the fibers...

ACTA NEUROBIOL. EXP. 1974, 3 4 : 435-466

Lecture delivered at Symposium "Brain and behavior" held in Jablonna near Warszawa

July 1972

AMYGDALA FUNCTIONS WITHIN THE ALIMENTARY SYSTEM

E. FONBERG

Department of Neurophysiology, Nencki Institute of Experimental Biology Warszawa, Poland

Abstract. The arnygdaloid complex plays an important role in various defensive, sexual and metabolic functions of the organism. Our previous experiments on the defensive functions demonstrated that the amygdala may be divided into dorsomedial excitatory and basolateral inhibitory parts. Our recent experiments showed that this division is true also for alimentary mechanisms. The dorsomedial part of the amygdala acts as a facilitatory "center" and the lateral part as an inhibitory alimentary "center". These functions of the amygdala are parallel to those of the hypothalamic feeding centers. Bilateral damage to either the dorsomedial amygdala or to the lateral hypothalamus produced aphagia with adipsia, decrease of body weight and impairment of both classhcal and instrumental reactions. These changes were accompanied by low general arousal, atonia, catatonic like positions, negavitism and loss of positive emotional reactions. Damage to the lateral amygdala, on the other hand, produces a syndrome similar to damage to the ventromedial hypothalamus, 1.e. hyperphagia and an increase of body weight. Slight increase of both classical and instrumental reactions and disinhibition of responses during intertrial intervals were found in both cases. Combined damage of the dorsomedial amygdala and lateral hypothalamus enhanced the symptoms attributable to each and prolonged the period of aphagia. Damage to the lateral amygdala subsequent to lesions of the dorsomedial amygdala and/or the lateral hypothalamus produced restoration of food intake, instrumental reactions and general arousal.

ANATOMICAL AND ELECTROPHYSIOLOGICAL INTRODUCTION

The amygdaloid complex is a symrn&ical structure situated in the ventral, medial part of the rostra1 poles of the temporal lobes. It belongs to the forebrain but derives from archi- and paleocwtex. Its phylogene-

436 E. FONBERG

tic origin can be traced as early as cyclostcmes and in vertebrakes it is quite well developed. In reptiles and fish i t is already possible to distin- guish two main divisions of the amygdaloid complex, i.e., the corticomedial and basolateral components. The basolateral part is younger both in phylogenetic and ontogenetic development (74). In higher species the basolateral part is developed pl.ogressively with the phylogenetic development. In mammals such as cats, dogs and rats, which are most widely used in experimental work, the main components of the amygdaloid complex are mlore or less the same. In these species the cmticomedial part is composed of medial, central and cortical nuclei, and the basolateral part of the nucleus basalis parvocellularis, magnocellularis and lateralis. The division of the amygdala into two basic parts is commonly accepted (18, 54). Nevertheless, there exists solme c~ontroversy as to the classification of particular nuclei. Thus the nucleus of the olfactory tract is sometimes included in the corticmedial p a ~ t of the amygdalfoid complex, although acc~rding to a recent point of view (151) it does not belang to it. The anterior amygdaloid area is also included by same authors and subjected to investigations concerning the physiological role of the amygdaloid complex. On the o t h e ~ hand, the cortical nucleus is sometimes ascribed to the piriform cortex and excluded from the corticomedial division. Therefore, instead of "corticomedial" some authors use the term "centromedial" (60, 150), although the central nucleus has developed later than the other nuclei of this division (72). I use in my papers the term "dorsomedial" to designate a particular region of the arnygdaloid complex rather than the specific nuclei. The parvocellular part of the basal nucleus is lately ascribed to the corticromedial (or dorsomedial) rather than to the baslolateral division (83, 84) or classified as a transition zone between these two regions (21, 66).

In primates the amygdaloid complex has developed further and the whole complex has rotated, resulting in the disl'mation of particular nuclei. The lateral part takes a more ventral position and the medial part has moved dorsally. Therefore, the parvocellular part of the basal nucleus comes to lie medial to the magnocellular part instead of being ventral as in subprimates. This rotation is even more p~onounced in the human brain (72). In addition, the amygdaloid complex of man has been subjected to further development. The nuclei are further subdivided, particularly the basal nuclei. After years of study the functions of the particular nuclei of the amygdaloid complex in experimental animals have still not been precisely defined and understanding the functions of the most complicated human amygdaloid complex is even more re- mote. This problem become parbcularly important in view of the recent development of human amygdalar surgery (15, 19, 96, 97, 102, 154).

Fig. 1. Frontal sections of the amygdala of cat (A) and dog (B). Abbreviations: Bm, nucleus basalis magnocellularis; Bp, nucleus basalis parvocellularis; Ce, nucleus centralis; Co, nucleus corticalis; L, nucleus lateralis; M, nucleus medialis; OT,

tractus opticus.

Fig. 2. Frontal section of the brain of representative dog A90, with ty- pical small lesion in dorsomedial amygdala, which produced the behavioral syndrome described in the

text.

Fig. 3. Dog A170 after dorsomedial amygdala lesion, aphagic, depressed (A) and negativistic (B).

AMYGDALA FUNCTIONS AND ALIMENTARY SYSTEM 437

The main projections from the amygdala are the stria terminalis and ventral amygdalofugal system of fibers (64, 65, 103, 104, 151). The first conducts impulses mainly from the corticomedial division and the second mainly from the basolateral area. I t was at first thoughit that these pathways carry only efferent fibers. However, it has recently been shown that they cmduct impulses in both directions and involve bath amygdalofugal and amygdalopetal fibers (67, 70, 88, 105).

In spite of these differences in anatolmical classifications of particular amygdalar nuclei or even their parts, the division of the amygdaloid omplex into two basic pclrtions, medial and lateral, is generally accepted frcm the structural point of view. On the other hand, although such division is valid for most of the species, one cannot overlook the existence of anatcmical differences among them. Thus, in rat (17, 91) and rabbit (8) f m example, the stria terminalis gets fibers from both cmticomedial and basolateral parts, but in the cat the fibers belonging to the stria terminalis almmt exclusively derive from the corticomedial part (57, 65, 73, 151). In,the dog, used in the present experiments, the particular nuclei of the amygdaloid complex are rather similar in relative size and spatial localization to the nuclei of the amygdaloid complex of the cat (Fig. 1). However, recently it was s h m on dog (87) that the fiber projections are different to some extent in this species, especially from the basolateral part. Projections f ~ o m this last part to the neocortex are in dog more developed than in rat and cat. This may be significant for differences in behavior patterns between species.

The connections between amygdala and hypothalamus are obviously of the greatest importance, considering the physiological correlation of these two structures. Most studies concern the stria terminalis, which, is divided further into cornmissural, postcommissural and supracommis- s~ural components. Acemding to Heimer and Nauta (68), the postocom- missural component ends mainly in the rostra1 part of the hypothalamus, with some fibers joining the medial forebrain bundle, whereas the supracommisswal component terminates more caudally around the ventromedial nucleus and to a lesser degree in the ventral premammillary nucleus. These authors suggest that the endings of the stria terminalis fmm strong synaptic connections with both dendrites and cell bodies of the ventromedial neurons. Murphy and Renaud (100) recently showed that in rthe ventromedial hypothalamus there exist two types of neurons of different size. They suggest that smaller bipolar neurons may be involved in inhibition. Both the stria terminalis and the ventral system contribute terminals to these neurons; therefore one system may inhibit them, and the other one excite. In addition, Fernandez De Molina and Garcia-Sanchez (26) found that in stria terminalis there exist two kinds

8 - Acta Neurobiologiae Exper imental is

438 E. FONBERG

of fibers with two different conduction velocities. Slower conduction may be relevant to inhibitory influences. On the other hand, the ventral diffuse system of fibers ends predominantly in the lateral hypothalamus or joins the medial forebrain bundle through the longitudinal association bundle (65, 73, 103, 104, 151). The connections between hypothalamus and amygdala may col~sist therefore in cross relations. The ventral system derived from the basolateral part may have an excitatory influence on the venrh-omedial hypothalamus and an inhibitory influence on the lateral hypothalamus, whereas the stria terminalis (at least some of its fibers) might exert an inhibitory effect on ventriomedial hypothalamus and an excitatory effect on the anterior lateral hypothalamic area. Such a scheme is, however, too simplified, and differences in distribution of these two systems of the amygdala between various species suggest that they may possess specific behavioral meaning in different patterns of behavioral reacting of particular species depending on She different biological needs. This problem requires, however, further elucidation.

The amygdalopetal fibers from the hypothalamus are derived mainly from the rostra1 hypothalamus (17) going through stria terminalis as well as through the medial forebrain bundle and ventral system. There are also many indirect ways from amygdala to hypothalamus via pyriform cortex, hippocamps and fornix.

Amygdalo-cortical connections and connections with other parts of the limbic system seem Do be less important in relation to the alimentary role of the amygdala. The oonnedim with the midbrain may be of greater importance. Although a direct arnygdalc-mesencephalic pathway is traced only in birds and reptiles, the impulses from amygdala may go both through the medial-forebrain bundle and other indirect pathways. Electrophysiological studies give evidence for strong amygdalo- midbrain connections (58).

Electrophysiological findings also give support for the division of the amygdaloid complex into two parts, demonstrated in the anatomical studies. Kreindler and Steriade (89) found that electrical stimulation of the medial part of the amygdala produced cortical arousal, whereas stimulation of the lateral part produced slow, sleeplike waves. According to Dreifuss and Murphy (20) stimulation of the cortricmedial part, which was conducted by s t i a terrninalis, elicited in ventromedial hypothalamic neurms responses consisting in monophasic evoked potentials, and stimulation of the basolateral arnygdala, which was conducted by the ventral sywtem, produced biphasic waves in the same structure. In addition, the responses mediated by these two systems are in antagonistic relation, inhibiting each other reciprocally. Oomura et al. (108, 109)


found that stimulation of the lateral amygdala inhibits the spontaneous activity of the lateral hypothalamic neurons and increases the activity of the ventromedial neurons. Their findings strongly speak for the existence of two opposite physiological systems. Also the afferent input studied electrophysiologically show similar differentiation. Thus, Happel and Bach (67) found that stimulation of stria terminalis inhibits the activity of the basal part of the amygdala whereas the stimulation of the ventral system has a facilitatory effect. In addition experiments of Kraczun (88), showed that stimulation of either ventromedial or anterior and lateral hypothalamus gives responses with different latencies and characteristics of electrcxphysiological effects, which are also dependent on whether they are recorded in the corticomedial or basolateral area. These results give additional support for the division of the amygdala into two systems.

PHYSIOLOGICAL INTRODUCTION

Although the anatomical differentiation of the amygdaloid complex was well-known long ago, the functional role of ithe particular nuclei is not fully elucidated yet. Both ablation and stimulation methods enco- unter several difficulties in delimination of the laclalizing of particular functions. The amygdaloid oomplex lies deep in the temporal lobe and near the base of the brain. Therefore access to i t is rather difficult. Dur- ing surgical ablations care must be taken not to destroy vessels of the circle of Willis, such caution sometimes sparing the most dormmedial part of the amygdaloid complex. It is very difficult to limit the damage to a particular nucleus. In stereotaxic electrolysis or stimulation, which is more precise, the e l e c t d e tract must pass through almost the entire brain, or at least the temporal lobe, if the electrode is introduced in horizontal plane. During stimulation, especially when its intensity increases, various groups of neurons with different functions may be involved. In addition, the fibers of the tracts passing through might have lower thresholds than neurons of this area.

Further complications me produced by the fact that the amygdala is very susceptible to seizure activity. Because of the very low threshold for afterdischarges, which propagate widely to other pants of the brain, the results of stimulation may reflect the activity of distant areas. Re- cording the electroencephalogram during stimulation a€ the amygdala, in order to exclude the existence of epileptic discharges, is described in only a few papers. Various motor reactions were observed during stimulation of the amygdala, e.g., sniffing, chewing, turning the head etc., which, in my experience, often proceed to generalized mator seizures and are accompanied by EEG after discharges.

440 E. FONBERG

There exist multiple internuclear connections within the amygdaloid complex. Variety of connections among the nuclei and between them and surrounding structures complicate even more the problem of functional localization. Even by small lesions not only the particular area is impaired but also the fibers transversing i t from other regions. There- fore the effect may be due to the impairment of conneations directed to these more distant areas and not to the area of the lesion itself. This is, for example, the danger when the lesion is situated in the dorso~medial part of the amygdala. Most authors interested in the amygdalar functions have made rather large lesions, involving several amygdaloid nuclei. Thlerefore, dy each particular .operation different sets of nuclei and different nuclear portions might be damaged which in effect might produce various symptoms.

A second cause of the discrepancy of some results is the limited aim of the particular investigators. Obviously, it is quite impossible to study everything at once. But the automatization of investigatolry methods built further limit, to free observations of unexpected events. The amygdaloid complex takes part in controlling various and multiple reactions. Therefore if only one test is applied and one response observed, the amygdalar lesion may, ol. may not influence this particular response, and other effects may be overlooked. For example, Rosvold, Mirsky and Pribram (118) observed that an amygdalectomized baboon was ag- gressive in a cage, but submissive in the colony within a group with definite hierarchy. If this animal had been observed by others investigators separately in each of these situations, the ccmclusions would have been clmtradictory. F'urthemore, no effect will be found if a large lesion impairs two antagonistic functional systems of the amygdaloid complex at once, totally or in equal parts.

Beginning from Papez (110, 111) and MacLean (94, 95) the role of the amygdala in drive and emotions has been widely recognized. Most explored is the role of the amygdala in fear and defense mechanisms. Fernandez DeMolina and Hunsperger (27, 28) showed that the dorsomedial region of the amygdala is the upper part of the defensive system going down through the hypolthalamus to the mesencephalic defensive centers. Several other authors (e.g., 32, 48, 59, 71, 75, 113, 115, 148-150, 152) were also interested in the role of the amygdala in defensive mechanisms and studied either the effects of ablation of the amygdala on defensive reactions or the effect of amygdalar stimulation in evoking or inhibiting fear, aggression and avoidance performance. My previous investigations also concerned the problem of the role of the amygdala in defensive mechanisms. In the previous work (48, 51) we showed that surgical ablation of the amygdala in dogs differently affected avoidance


and classical defensive reactions. Later, I showed that electrical stimulation a€ the corticmedial division of the amygdala evokes fear reactions in dogs (30, 33, 34, 36, 39) whereas electrical stimulation of the lateral and basolateral part inhibits fear but not avoidance (29, 31, 39). Partial lesions of the amygdaloid complex impair avoidance reactions (34, 35).

Other groups of authors, like Green et al. (62). Elwers and Critchow (24, 25), Kling (77, 79), Koikegami (84, 85), Shealy and Peele (134), Schrei- ner and Kling (126), Sawyer (124), Yamada and Greer (162) found that stimulation or lesions of the amygdala in cats affect sexual reactions and take part in their behavioral and humoral regulati~on.

Cognitive and discriminatory functions of the amygdala were stres- sed by several authors. This point of view derives f r m the pioneer work of Kliiver and Bucy (82) on the ablation of the amygdala and surrounding parts of the temporal lobe. They found after such lesions, besides variolus other symptoms, the symptom called by them "visual agnosia" - which consisted in not recognizing the significance of objects. This was the pioneer work in dealing with the functions of the amygdala and the variety of intriguing symptoms observed in the effect of temporal lobe lesions, including the amygdaloid complex, attracted interest toward the latter structure and opened a new area of further investigations. The work of Kliiver and Bucy became a classic in the literature on amygdalectomy. However, the lesion in this experiment was very large and also probably involved visual association fibers perhaps accounting for the lack of visual discrimination.

Several authors (7, 9, 23, 114, 115, 130-133, 140, 149, 152), described the deficits in learning, me-mory and attention as the results of amygdalar lesions. However, the impairment of task solving and memory deficits may be caused by several different factors. One of them might be the presence of epileptic after-discharges. Goddard (59) and Kesner and Doty (76) observed amnesia after epileptogenic stimulation of the amygdala. On the other hand, Levine et al. (92) during stimulation producing seizures of inferotemporal co~ tex observed retrograde amnesia to visual stimuli paired with shock but they did not notice such an effect during amygdalar seizures. They suggested that the amygdaloid complex plays no essential role in the storage of informations following CS-US events and if an effect were found it could be attributed to the connections with inferotemporal cortex or hippcampus. The lack of overt seizure activity cannot exclude the presence of EEG afterdischarges if the eleectrical activity of the brain is not recorded. Even with the lack of EEG afterdischarges the various disturbances in problem solvings attributed to memory or learning deficits may be secondary and reflect motivational or emotional changes. First, they may due to

the low general arousal, which produces indifference and low concentra- tian in problem solving. It may be due to lowered hunger drive as was probably the case in St~ollw's experiments (140). It may also, result from increase of the hunger drive producing errors due to diskhibition (128, 129). Disturbances in avoidance learning, transfer and extinction might be as well due to the increase or decrease of fear drive, changes in general arousal, and either impairment or enhancement of inhibitory mehanism. A predoaninance of another drive upon the drive under study may a h produce a decrease in solving different types of tasks.

ALIMENTARY FUNCTIONS

Another aspect of amygdala~ functi~ons is the regulation of alimentary mechanisms. Several authors observed changes in alimentary behavior following amygdalar lesions (1, 2, 4-6, 13, 14, 16, 55, 78, 80, 81, 84, 99, 100, 114, 118, 125, 127, 134, 140, 155). H w w e r , in comparison with studies on the alimenta~y functions of the hypothalamus, the arnygdala has been much less investigated. There is common agreement that the hypothalamus is much more important in respect to alimentary functions than the amygdala (4, 16, 62, 63, 78, 81, 98, 99, 107, 117, 125, 129, 137, 142, 156-160). t

In recent wolrk I have concentrated on the functions of the amygdala in alimentary reactions a s compared with similar functions of the hypothalamus. We tried to mtake small lesions circumscribed to particular nuclei or at least to a limited region, taking as the basis the physiological and morphological differentiation into dorsomedial and basolateral systems.

These investigations were performed on several groups of dogs, using electrolytic lesions made by stereotaxically directed electrodes. The lesions were placed bilaterally and as a rule two points were coagulated in the anterior pwterior plane. The food intake and body weight was measlured before and after the operation and the general behavior tho- roughly observed. Different groups of dogs were trained preoperatively in instrumental reactions; others were trained after the operation. The salivary conditioned reactions were elaborated before the operation. The details of surgical and behavioral p c e d u r e s are described in the previous papers of Fonberg (39, 42, 46), and Rozkowska and Fonberg (120- 123).

Effects of lesions of dorsomedial amygdala

After damage to the dorsomedial amygdala (Fig. 2) striking changes in general behavior of the dogs occurred (33, 40, 41, 53). The dogs were apathetic, atcmic and negativistic (Fig. 3AB), lying dovim in the first


few days, then standing motionless where placed, or sitting down sometimes taking bizarre positions or cataleptic-like postures. They also walk- ed around aimlessly, especially at night. They were not interested in

0 Before operation

) After operation

1 month later

68 70 1 Zmonths later

1 3 months later

C, 79 104 735 151 755

Fig. 4. Effects of lesions in dorsomedial amygdala on food intake in individual dogs, divided into five groups. A, short lasting aphagia (less than 10 days) with subsequent long lasting and increasing hypophagia; B, pronounced aphagia with long lasting hypophagia; C, short aphagia with long lasting hypophagia; D, pronounced aphagia with subsequent recwery of food intake. E, short aphagia with subsequent recovery. Bars represent mean food intake from 10 days before the operation and during different postoperative periods. Number below bars denote individual dogs.

Arrows indicate operation.

444 E. FONBERG

food, aphagic and adipsic, and vomited several times daily (37). Total aphagia and adipsia lasted for a few days (up to 3 weeks). ?*hen prolonged hypphagia was observed and in some dogs it lasted several weeks or months. The duration of the hypophagia was not dependent on the duration of the period of initial aphagia. As seen on Fig. 4, in group A the hypcphagia enhanced with time, although the postoperative aphagia lasted only a few days. On the other hand, in group D the recovery of food intake occurred to a great extent within 1-2 months after the operation, in spite of the fact that the initial aphagia lasted about 2 weeks. During the period of hypophagia the dogs ate by themselves; nevertheless they as a rule had to be baited to the food bowl and showed different food preferences to special kinds of food. In most cases they preferred sweet, semiliquid food over raw meat.

Postoperative initial istrumental training was in some dogs completely unsuccessful. In others it was possible to teach them to perform the proper instrumental movement, but the reactions were unstable and fluctuating (40).

The retention of the instrumental reactions trained before the operation was also severely impaired after dorsomedial amygdalar lesions. In some dogs the instrumental reactions were completely abolished, and the retraining, which in some cases was continued up to 4 months, was completely unsuccessful. In some other dogs the instrumental reactions reappeared spontaneously after the operation during the first few experimental sessions, or after brief retraining, which usually started after 5 days retention test. The first retention test was usually performed 10-12 days postoperatively. Nevertheless, the instrumental performance

Fig. 5. Effect of lesions of dorsomedial amygdala on retention of instrumental reactions in three dogs. Notice the fluctuations of the instrumental performance.

20- L?

S 8 16-

\

P 5 12 s 8 h

8 -

k 9

s 4 - t

7 - Z - - -

-

- f

O ; ----- 10 1 25

Experimental sessions

Fig. ,esion in lateral amygdala in representative dog A60. This lesion hyperphagia and increase of body weight.

Fig. 8. Dog A179 after operation of lateral amygdala, lively (A) hyperphagic (B) and playful (C).


of most subjects was unstable and fluctuating, and showed a tendency to extinction. Figure 5 demonstrates the instrumental performance in three individual dogs in which the instrumental reaction was not completely abolished. In two of them the proper instrumental reaction reappeared before the retraining started and in another one in the first days of retraining. 1-Iowever, although the dogs performed the proper kind of reaction to the conditioned stimulus, the performance was below 100°/o. Retraining resulted in improvement of the performance in one dog and reappearance of the reaction in the third. Nevertheless, after a few days the instrumental reactions spontaneously decreased in all dogs. The fact that the instrumental reactions trained preoperatively may appear after the operation spontaneously before retraining, at least in some dogs, and that the dogs performed the same kind of movement as was trained before the operation, seems to show that the lesion in the dorsomedial amygdala does not produce the memory impairment. These experiments as well as the experiments on pstoperative initial training (40) suggest that the ability to learn is also not destroyed by this operation. Never- theless, the performance of instrumental reactions was in both cases unstable ar.d fluctuating. The most simple explanation is that this low level of performance reflects the low hunger drive. On the other hand, the decrement of instrumental perfmmance might be as well caused by the decrease of reinforcing values of food. It may be also due to the changed taste or smell, feeling of nausea, painful gastric contractions or other disturbances in gastric activity (56). The deep metabolic changes which may evoke simply a state of general sickness, should also be taken into account. The central general atony and low arousal as well as peri- pheral muscular atony and weakness may be another cause of decreased instrumental performance. These last disturbances may be also dependent on the metabolic changes.

Effects of lesions of lateral amygdalar region

The opposite effects to these produced by damage in the dorsomedial amygdala were found after lesions of the lateral amygdala (Fig. 6). The dogs were hyperphagic (Fig. 7 and 9A). Some of them just being awa- kened from anesthesia ate at once 3-4 kg of food. However, most of the dogs did not eat more than 150°/a of their preolperative portion. The most striking changes occurred in their behavior. The dogs were much more interested in food than before the operation (Fig. 8A); they followed the technician who prepared it, looked for the food blow1 ancl de- voured the food voraciolusly (Fig. 8AB). Their instrumental reactions were transiently disinhibited during intertial intervals (Fig. 9B) and also to the inhibitory stimuli (Fig. 9D). The reactions the CS+ were not chan-

446 E. FONBERG

ged (Fig. 9C), or performed more vigorously. In general, the dogs were mare lively, friendly and playful, like puppies (43) (Fig. 8AC).

Fig. 7. Increase in food intake after lateral arnygdalar lesions in individual dogs. Bars represent mean food intake in 5 day periods. White bars, 5 days immediately prior to operation; black bars, days 1-5 and days 6-10 after operation; striped bars, 5 day periods 1,2 and 3 months later. Numbers below bars denote individual dogs.

From Fonberg (43).

The argumentation of the food intake and disinhbition of alimentary reactions after lateral amygdala lesions seems to furnish further support f.or my hypothesis that the role of this structure is inhibitory (29, 31, 32, 34, 38), and that among other functions it exerts an inhibitory influence also upon the alimentary reactions (41, 43, 44). These results fit well with previous experiments cm electrical stimulation of the lateral amygdala in cats and dogs (29, 31, 49, 50), which showed that stimulation of this area produces inhibition of food intake and instrumental alimentary reactions.

Comparison of the role of hypothalamus and amygdala in alimentary mechanisms

The above described experiments show that the dorsomedial part of the amygdaloid complex functions as a positive alimentary "center" and that the lateral amygdaloid nucleus serves as an inhibitory or satiation "center". It seems therefore that the amygdalar "centers" are duplicating the functions of the well known hypothalamic "centers". According to previous suggestion (31, 34, 36, 39) the amygdala would


be somehow secondary to the hypothalamus in this regard. I thought primarily that the amygdala would exert only some slight modulatory influence upon the hypothalamic feeding centers, and that these last play much more important and basic role in the alimentary mechanisms.

A Dog A 88

C Dog A 179

's"[ O\-

-

F - 4 4 4

I0 Experimental sessions

~xperimental sessions l5

Fig 9. Effects of lesions of lateral amygdala on food intake and instrumental performance. Note postoperative hyperhagia (A) increase of number of intertrial reactions (B) and disinhibitian of reactions to the CS- (D), with no obvious change in reactions to CS+ (C). Black circles, before operation; white circles, after operation.

Moreover, our experiments show that the effect of both dorsomedial and lateral amygdalar lesions in dogs are not persistent. Aphagia lasted no more than 3 weeks after dorsomedial amygdalar damage (Fig. 4) and also the lateral amygdalar hyperphagia decreased in time (Fig. 7). On the other hand, the studies of various authors on other species (mostly on rats) on the effect of lateral hypothalamic lesions on food intake showed more pronounced effects relected in longlasting aphagia (3, 98, 141, 143, 145, 146). The comparison of our results on amygdalar aphagia on dogs and the results of others concerning hypothalamic aphagia in rats and cats seem to support the view that the hypothalamus is mare basi- cally involved in feeding mechanisms and amygdaloid complex is an additional upper level of the alimentary system. However, further studies on the hypothalamic feeding centers performed with Rozkowska (41,

445 E. FONBERG

52, 120-123) showed that in dogs the effects of lesions of definite areas in the hypothalamus are almost identical to the reciprocal areas of the amygdala.

Lesions of the lateral hypothalamus produced effects similar to the lesions of the dorsomedial amygdala and lesions of the ventromedial hypothalamus are colmparable to lesions of the lateral amygdala. Al- though some differences were observed between the individual dogs, we -

did not find convincing differences between the groups of dogs with lesions either in dorsomedial amygdala or lateral hypothalamus (i.e., positive "centers"). We did not find also the differences of the syndromes produced by lesions of lateral amygdala or ventromedial hypothalamus (i.e., inhibitmy "centers"). ,

Table I shows the effects of these four types of lesions on different aspects of behavior. Lesions situated in the lateral hypothalamus as well as lesions of the dorsomedial amygdala produced aphagia with

Comparison of the syn~ptoms produced by lesions of hypothalamus and amygdalar synergic and antagonistic "centers". The direction of the arrows denotes the increase (up) or decrease (down)

of symptoms

I Dorsomed~al amygdala 1 @MA) J L !

I

I I

- - - - - - - I - -- - I I I

Lesioned structures

Lateral amygdala (LA) -- - - - -

Lateral i hypothalamus (LH) i

1 Ventromedial~ hypothala-

- - - - -

take

Food and Water in-

I I I vomiting, food

I I I I preference, nega-

tivism, cataleptic-like postures,

I thin and shinless

j hair - - - -

Salivary reactions

Body weight

* ? T I lively playfulness behavior,

vomiting, food I preference, nega-

humans I reactions

1 tivism, catalep- 1 tic-like postures,

motility

Instru-

I thin and shinless I hair - - - I

Social relations

with

General arousal

and Other symptoms

un. i ,-hanged T T T i ! ~ agitation before

meals, late taste

- - 1 - -- I preference - --


adipsia, which lasted in both cases from a few days to a few weeks, and was followed by a longlasting period of hypophagia. During the period of aphagia the dogs had to be either force fed or fed by intuba- tion. In spite of the forced feeding the body weight drapped significantly. Both hypothalamic and amygdalar dogs vomited (37, 52). Vomiting was observed not only during the period of aphagia, when they were fed "by force", they also vomited during the subsequent period of h y p e phagia, in spite of the fact that they ate the food voluntarily. They were however still not interested in obtaining food, they ate less than before the operation and showed different food preferences. Both hypothalamic and amygdalar dogs as a rule preferred the sweet semiliquid food over the raw meat in contrast with normal dogs in which meat is usually their favorite meal.

The general level of arousal was also similarly changed after both lateral hypothalamic and dorsomedial amygdalar lesions. The dogs were atonic, restless and not interested in the environment. They lost their friendly attitude toward man. Both lateral hypothalamic and dorsomedial amygdalar dogs showed negativism, did not obey commands, o p posed all manipulations and took bizarre, catatonic-like positions (41, 45, 17). The instrumental reactions trained before operation were ccm- pletely abolished or impaired after both operations (33, 45, 120, see also 157). The postoperative training of naive dogs was also greatly impaired as compared with normal dogs (40, 120). Classical salivary reactions, both conditioned und unconditioned, were greatly diminished. In particular, after lateral hypothalamic lesions the ccnditionecl salivary ~,eact- ions were in most dogs completely abolished during the period of aphagia (122). Salivary reactions in dorsolmedial amygdalar dogs were also diminished although less than in lateral hypothalamic dogs. They were postoperatively very labile and irregular (93).

These experiments indicate that in the dorsomedial amygdala there exists an area with similar functions to those of the lateral hypthala- mic feeding center. Therefore, it seems that positive alimentary mecha- n i s m are doubled in lateral hypothalamus and dorsomedial amygdala.

Parallel relations were also found in ventromedial hypothalamus and lateral amygdala. The experiments on ventromedial hypothalamic lesions in dog (121) reproduced the very well-.known syndrome of hyperphagia and obesity (2, 3, 10-12, 69, 144). Sirnilar effects were produced by lateraI amygdalar lesions (43, 44). In both groups of dogs the instrumental performance to the positive CS was undisturbed and it was disinhibited only transiently during the presentation of negative stimuli and in the intertrial intervals (Fig. 9) (121). The salivary reactions were also disinhibited (123). The ventromedial hypothalamic and

450 E. FONBERG

lateral amygdalar dogs differed however in their general behavior. The amygdalar dogs were very friendly, lively and playful like puppies (see Fig. 8A-C). The hypothalamic dogs, although extremely excited before feeding, were very quiet and sleepy after meals (121, 123). This may be caused by the fact that ventroxnedial hypothalamic dogs consumed more food than amygdalar dogs although judging by their approach to the food bowl both groups seemed similarly voracious. The amygdalar dogs ceased to eat before being oversatiated and ventromedial hypothalamic dogs seem not to be able to stop eating. This fact may be ex- plained in such a way that in amygdalar dogs, although other inhibitory mechanisms were abolished, the presence of glucoreceptms in ventromedial hypothalamus (which in this group of dogs was intact) guaranteed the sensitivity to satiation and by this way regulation of food intake. The differences between ventromedial hypothalamic and lateral amygdalar syndromes are, however, smaller than the similarities of s y m p toms and therefore it seems that there exists, at least some duplication of the inhibitory alimentary functions within these two structures.

Our results showing the similar effects of lesions of the lateral hypothalamus and dorsomedial amygdala on the one hand and the ventromedial hypothalamus and lateral amygdala on the other were striking and quite unexpected. It is reasonable to think that t h e ~ e must be some distinctive differences between the role of hypothalamus and arnygdaloid complex, even taking into account only the alimentary functions. The similarities may be superficial. Anand et al. (6), Anand (2) assumed that the hypothalamus deals with hunger and the amygdala with appetite. Konorski (86) proposed that the hypothalamus is involved in unconditioned and the amygdala in conditioned instrumlental alimentary reactions. Other authors, like Gray (61), assume that the amygdala deals with emotions, the hypothalamus with internal drives. These authors as well as some others stress the differenc~es between the roles of hypothalamus and amygdala. In our experiments we used several experimental pro- cedures with the aim of differentiating the effects of hypothalamic lesions, but we found the further similarities, instead.

Our data from various series of experiments did not supply the evidence for these differences and only sho~wed once more that amygdala and hypothalamus functionally belong to a common system. Anatiolnical studies described above as well as various electrophysiological and behavioral findings substantiate this point of view.

Effects of double lesions: in the amygdala and the hypothalamus

The doubling of the alimentary centers may explain why the effect on food inta!ke by either dwsornedial amygdala or lateral hypothalamus


alone is not permanent but transient. It may be due to the fact that these structures reciprocally overcompensate the function of each other. In order to secure such basic function as feeding, the duplication of centers mediating this functions is important from the biological point of view. Few papers deal with the relations of amygdalar and hypothalamic lesions (100, 125, 153), and in addition their interest is mainly concentrated o n the relations between the amygdala and ventromedial hypothalamus. As shlown by our recent experiments (G. Szwejkowska and E. Fonberg, in preparation) combined, successive lesions of both positive alimentary centers (lateral hypothalamus and dorsomedial amygdala) produce more pronounced changes than separate lesions of each and in some dogs they produce even permanent aphagia. Figure 10A-E

Fig. 10. Food intake (left ordinate) and body weight (right ordinate) in dog A151 subjected to three operations. A, in normal state; B, after dorsomedial lesion of amygdala; C. before second operation; D, after subsequent lesion of lateral hypothalamus; E, before third operation; F, after subsequent lesion of lateral amygdala. Note initial aphagia after first operatian, then recovery of feeding, long lasting aphagia (75 days) after lateral hypothalamic damage and the recovery of feeding after

lateral arnygdalar lesion.

shows the daily food intake in dog A151 in his normal state, after dm- somedial amygdalar damage and after subsequent damage to the lateral hypothalamus. The first operation was followed by aphagia. Later the recovery of f d intake occurred. Further operation on the lateral hypothalamus produced again the aphagia. This time the aphagia was permanent. The total aphagia lasted 75 days, i.e., until the third operation (see below). During this period the dog was force fed twice a day in order to keep him alive.

There are not yet enough data to make any definite conclusions from these results. The only clear effect of these double operations is that

452 E. FONBERG

the subsequent lesion of the lateral hypothalamus enhances the effects of the previous damage tu the dorsmedial amygdala. It may be postula- ted that after the damage b the dorsomedial amygdala, the lateral hypothalamus compensated for its function by increased activity and therefore the recovery of feeding occurred. Further damage to the lateral hypothalamus eliminated its functions altogether with the compensatory mechanisms and therefore impairment produced by this operation was more severe.

It is possible that in dogs the compensatory mechanisms are more developed than in rats and that this is the cause of the transient aphagia if cmly 'one of the feeding centers (either in dorsomedial amygdala, or in lateral hypothalamus) is destroyed. On the other hand, in our experiments with lateral hypothalamic lesions which abolished the cingu- late self-rewarding bar-pressing in rats, aphagia was also transient (E. Fonberg, E. E. Coons, and N. E. ILlille~, unpublished data).

When the first operatilon is situated in the inhibitory structure (lateral amygdala) and the subsequent in the positive one, the effect of the second operation prevails as shown by our preliminary experiments (Fig. 11).

Fig. 11. Effect of lateral amygdalar and subsequent lateral hypothalamic damage in dog A67. Bars represent mean food intake in 10 days. A, normal intake; B, C , after lateral amygdala damage; D, after lateral hypothalamic damage. Note increase of food intake after first operation and decrease after subsequent lesion

" A C of lateral hypothalamus.

The compensation of impaired functions in some period after the operation may be due, in general, to the fact that the lesions do not totally destroy the crucial area and the residual or marginal neurons may assume the functions disturbed by the damage. It may also be due to the increased activity of the other parts of the alimentary system involved in feeding regulatiion, i.e., amygdala in the case of hypothalamic lesions and vice versa. Other structures also involved in feedmg, e.g., the posterior hypothalamus (161), midbrain (112, 135-138, 143) anid other brain structures (90, 117) might be responsible for compensation of the alimentary functions.

AMYGDALA FUNCTIONS AND ALIMENTARY SYSTEM 453 ,

The reversing effects of lateral amygdalar lesions upon the effects of dorsomedial lesions

In the next s e~ ie s of experiments the first lesion was placed in the dorsomedial amygclala (which produces aphagia and loss of instrumental reactions) and then a few weeks later a subsequent lesion was placed in the lateral amygdala. After this last operation the effect of the first was greatly reduced, and the behavior normalized (41, 42, 45-47).

After the second lateral amygdalar operation the dogs started to eat eagerly again (Fig. 12) which showed that their feeding mechanisms were restored, and they again became lively and interested in their surroundings, which showed that their general arousal is also raised.

Fig. 12. Food intake in arnygdalar dogs subjected to double stage operations of DMA and LA. Bars represent mean amount of food consumed by dogs during 10 meals (two meals daily) ad lib. Before DMA operation (A), after the DMA operation (B), next 10 meals (B,), 1 month later (C), just before the LA operation (C,), just after the LA operation (D), next 10 meals (Dl), and 1 month later (E). Perpen-

dicular lines, standard errors. Adapted from Fonberg (43).

They again started to recognize the technician, respond to calling by name and obeyed commands. They come back to their normal old habits, which indicates that their "stupid" behavior after the first operation was not due to memory impairment. This last suggestion is also con- aordant with the following facts: the dogs not only were generally a r e used but the instrumental reactions, which had been impaired by DMA lesions, were again restored after the lateral amygdalar operation (Fig. 13). The possibility of restoring the reactions impaired by dorsomedial amygdalar lesions seems to show that the reflex arcs for instrumental reaction or neurons indispensible for patterning alimentary reactions were not impaired by the dorsomedial lesion, as this lesion still remains

9 - Acta Neurobiologiae Experimentalis

454 E. FONBERG

and the reacrtim is restored, but that all sympbps observed after dorsmedial damage were caused by the overflow of inhibition deriving from lateral amygdala (46).

Fig. 13. Effects of DMA and subsequent LA operations, on the instrumental performance of three representative dogs. Bars represent perdnt of performance from 10 day performance. A, M o r e DMA operation; B, after DMA operation; C, before LA operation (620 weeks after DMA operation); D, after LA operation, and E, 6-10 weeks later. Note the recovery of completely abolished performance (above) and impaired performance (below). Between B and C elapse 1-2 months and bet-

ween C and D 5-10 days.

We also have some evidence that changes in f d intake, as well as apathy caused by lateral hypothalamic lesions, aTe normalized after lateral amygdalar lesions (41). Moreover, our recent experimmts show that lesions of the lateral amygdala may at least partly dispel the total aphagia produced by combined, two-stage lesions of both lateral hypothalamus and dormmedial amygdala (see Fig. 10EF). The lateral amygdala, in view of these experiments, would possess the strong inhibitory influence upon the whole alimentary system, as its removal may ba- lance, at least partly, the effect of double damage to the dorsmedial amygdala and lateral hypothalamus.

In mder to verify whether the normalizing effect of the lateral amygdalar lesion results from the decrease of inhibition which follows the impairment of this region, I performed the next series iof experiments cm the effects of dorsomedial and lateral arnygdalar lesions m the dif-


ferentiation of instrumental reactions to two acoustic co'nditional stimuli. The results are presented in Fig. 14. The dorsomedial operation prduced decrease of instrumental performance to both stimuli. The subsequent lesion to lateral amygdala resulted, similarly as in previous work, in restoration of positive reactions. In most of these dmogs in addition tran-

00 CS+ H CS-

I 20 fiperimen fa1 sessions

Fig. 14. Effects of double (DMA and subsequent LA) operation on differentiartion in representative dog. Notice lack of instrumental reactions to both positive and negative CSi after DMA operation and restoration of instrumental performance to positive stimulus (CS+) with transient disinhibition of reaction to negative sti-

mulus (CS-).

sient disinhibitilon of instrumental reactions to the negative (inhibitory) conditioned stimulus was observed. Figure 14 is an illustration of this effect on representative dog.

This disinhibition of instrumental differentiation which goes in parallel with the restoration of positive instrumental reactions in the effect of subsequent lesions of the lateral amygdala also strongly speaks for the inhibitory functions of the lateral amygdala. After such lesions the removal of excess inhibition produces release of excitation which reflects both in restoration of =pressed positive reactions and transient disinhibitilon of inhibitory ones. These results support mce more my hypothesis first put forward in 1963 (29, 31, 32, 39, 43), that the lateral amygdala is an inhibitory center. Since that time the hypothesis has received further support from electrophysiological studies d Oomura et al. (108, log), Oniani et al. (107), Oniani and Naneishvili (106). Experiments of Morgane and Jalcolbs (98) and Willkinson and Peele (155) indicate that the inhibitory influences of the lateral amygdala are not limited to food intake but also concern reward mechanisms.

Recent anatorlnical studies of Thlbol and Szafranska-Kosmal (147), who found specific cells in the basolateral part of amygdala, i.e., cells Golgi IIa and neurogLioform cells, which, as suggested by these authors,

456 E. FONBERG

are Likely to have an inhibitory function, furnish further support for my hypothesis that the lateral amygdala is strongly involved in inhibitory mechanisms.

The alimentary system is not a simple one. Although the neocotex also exerts some influence over alimentary functions, the main mechan- i w s seems to be subcortical. The upper level of this system is probably the amygdala. Not knowing yet which are the specific functions of each or all of the amygdalar nuclei, I take now into consideration only the dormmedial positive and lateral inhibitory parts. Their functions are negatively correlated, although there is only indirect electrophysiologic- a1 proof for this (20, 88, 89). It is not certain, whether the antagonistic influences of medial and lat~eral amygdaloid areas act upon each other directly. They may be as well mediated indirectly through the hypstha- laniic feeding centers. In any event hypothalamic and amygdalar functions are strongly connected anatomically and mutually interdependent. Stimulation of the lateral amygdala produces an increase of spontaneous activity of the ventromedial hypothalamus and a decrease in the lateral hypothalamus (108, 109). Therefore, by these two opposite mechanisms the inhibition of feeding by lateral part of amygdala might be mediated either by excitation of the ven t~med ia l hypothalamic satiation center or by inhibition of the positive alimentary center in the lateral hypothalamus. The latter is indicated by the work of Oniani and Naneishvili (106), who showed that the frequency of evoked responses poduced by stimulation of lateral amygdala are higher in lateral hypothalamus and their threshold for stimulation lower than of those evoked in ventromedial hypothalamus.

The dmomedial part of the amygdala may also influence both lateral and ventromedial hypothalamus. It is connected by efferent fibers going by the ventral, diffuse system traced by Nauta (103, 104) and Val- verde (151) to lateral hypothalamus and medial forebrain bundle and secondly through the supracommissural component of the stria terminalis, ending in the lateral anterior part of the hypothalamus, and postcommissural components of the stria, which in dogs also terminates in the anterior la te~a l h p t h a l a m u s similarly as in rats (68). Fibers of the postcolnmissural component of the stria ending in the vicinity of the ventromedial hypothalamus were also found in dogs (87). This may be the way of inhibiting the latter and therefore indirectly ("second hand") securing the high level of excitation of the lateral hypothalamus. Ex- periments of White and Fisher (153) support this concept. A similar point of view was expressed by Murphy and Renaud (101) and Egger (21). Assuming, in view of experiments of Dreifuss et al. (20), that the dorsomedial amygdala by way of the stria terminalis mediates inhibi-

AMYGDALA FUNCTIONS AND ALIMENTARY SYSTEM 45 7

tion of the ventromedial hypothalamus, lesions of the dorsomedial amygdaloid area may produce release of activity of ventromedial neurons and in this way produce an increase of inhibitory influences upon the lateral hypothalamus. The behavioral effect of this increase of inhibition nlay be aphagia or hypophagia as observed in our experiments. Very important for alimentary mechanisms may be also the amygdalar influences on midbrain alimentary centers (112, 135-137, 161). The con- nection with these centers may go through ventromedial hypothalamus via the bundle of Schutz (dorsal longitudinal fasciculus) and also through the lateral hypothalamus via the medial forebrain bundle. There are also the direct fibers from amygdala. to medial forebrain bundle which may go to the midbrain. It is also pcssible that the way from amygdala to midbrain, omitting the hypothalamus, goes through polysynaptic pathways (57). The fact that damage to lateral amygdala produces an increase in previously depressed alimentary functions, even in the ab- sence (as the result of previous lesions) of both domomedial amygdala and lateral hypothalamus (as it was the case of dog A151) may indicate that there exist direct and strong connections between the lateral amygdala and positive alimentary midbrain centers. After lateral amygdalar damage these centers, released from its inhibitory influences, become active and are able to sustain the alimentary functions.

r l lOnS The problem which needs further elucidation concerns the rel. t' between alimentary functions of dorsomedial and basolateral amygdala and other functions, defensive particularly, mediated by the same areas. The dorsomedial OT corticomedial area is known to act as a positive defensive center (27, 28, 30, 32, 34, 39), whereas the basolateral portion exerts strong inhibitory influence also on defensive functions such as fear and rage (22, 29, 31, 39). Therefore functions of the d m m e d i a l or basolateral amygdala may be nonspecifically excitatory or inhibitory, respectively. On the other hand, it might be assumed that alimentary and defensive functions are mediated by separate neurons, interspersed with each other or having different localizations within these two amygdaloid divisions, which might be detectable by throughly designed tests. This suggestion seems to be more probable, especially in view of one of my last experiments. In this case, in which the effect of amygdalar lesions on performance of dogs trained in avoidance - alimentary differentiation (for procedure, see 38) was observed, the same lesion in the same animal differently affected avoidance and alimentary instrumental performance. This seems to indicate that although the dorsomedial part is probably the main locus of excitatory functions and the basolateral of inhibitory functions, further specificity and differentiation exists within these two amygdaloici systems.

458 E. FONBERG

The author is indebted to Mrs. H. Kurzaj, Mrs. M. Raurowicz and Miss U. Miq- czyxiska for their technical assistance. This investigation was supported by Project 09.4.1. of the Pd i sh Academy of Sciences and by Foreign Research Agreement 05.2'75.2 of the U.S. Department of Health, Education and Welfare unmder PL 480.

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Received 15 April 1973

Elibieta FONBERG, Department of Neurophysiology, Nencki Institute of Experimental Biology, Pasteura 3, 00-913 Warszawa, Poland.

amygdala functions within the alimentary system · and basolateral parts, but in the cat the fibers...

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