AMYGDALA 



141 



may result from amygdaloid lesions. Some authors 

 (148) describe rather severe atrophic changes in the 

 anterior pituitary, the thyroid, the adrenal cortex 

 and the Langerhans cells of the pancreas, with con- 

 sequent weight loss and growth deficiency, in puppies 

 with bilateral amygdaloid lesions. Yet in adult ani- 

 mals no endocrine changes suggestive of such atrophic 

 lesions were reported to occur following bilateral 

 amygdalectomy. On the contrary, although the 

 glycemic response to emolional stress is abolished 

 after bilateral amygdaloid lesions (200), there is no 

 evidence that such lesions affect the ACTH secretion 

 in response to stress (16, 200; Guillemin, personal 

 communication). There is however some, although 

 not entirely unequivocal, evidence that amygdaloid 

 lesions may produce an increase or imijalance in 

 the secretion of gonadotrophic and sex hormones 

 (142, 223, 224). 



Transient disturbances in the sleep-wakefulness 

 cycle with prolonged sleeplike states (199, 223, 227, 

 228, 240) as well as more persistent disturbances of a 

 narcoleptic character (204) are sometimes observed 

 after bilateral amygdaloid lesions. 



All these changes are however insignificant when 

 compared with the very dramatic alterations in be- 

 havior produced by bilateral amygdaloid lesions. 

 These behavioral changes were first described in 

 1888 by Brown & Schafer (35). They then fell into 

 oblivion until rediscovered in 1937 by Kliiver & Bucy 

 (143). According to these authors (36, 140-145), 

 the following syndrome develops in monkeys after 

 bilateral anterior temporal lobectomy, including the 

 amygdala; a) visual agnosia; h) hypermetamorphosis, 

 a strong urge to attend and react to every visual 

 stimulus; c) oral compulsive behavior; d) profound 

 changes in emotional behavior with loss of fear and 

 of aggressiveness; e) hypersexuality; /) changes in 

 dietary habits with acceptance of meat as food; and 

 g) increased and peculiar spontaneous motor activity. 



Although the lesions in these monkeys included 

 far more than the amygdaloid complex, most of these 

 disturbances have since been described with more 

 restricted anteromesial temporal lesions including 

 little, if anything, more than the amygdala. Although 

 from study of the effects of small temporal lobe lesions 

 it appears that some aspects of the behavioral dis- 

 turbances are more critically related to certain parts 

 of the temporal lobe than to others, it is nevertheless 

 not possible to arrive at a neat classification of be- 

 havioral components by assigning to each of them a 

 well-defined anatomical localization. Obviously all 

 these behavioral mechanisms are intimatelv inter- 



locked and the full syndrome is more than the sum of 

 individual deficits attributable to individual anatomi- 

 cal structures (141, 249). 



Disturbances of emotional behavior are the most 

 consistent results of such lesions and it seems that the 

 amygdala is the structure, involvement of which is 

 critical in the production of these emotional changes. 

 Most frequently animals with such bilateral amygda- 

 loid lesions become placid and display no reactions of 

 fear, rage or aggression (10, 17, 29, 72, 187, 199, 200, 

 204, 217, 222-224, 234, 241, 245, 249, 252, 254). 

 Not only is the rage threshold considerably increased, 

 but prey is no longer attacked (223) and the "social' 

 integration of the individual within a group is greatly 

 altered. Thus previously dominant individuals in a 

 monkey colony become the outcasts, subjected to 

 unremitting abuse against which they do not re- 

 taliate (218). These emotional changes are also re- 

 flected in alterations of conditioned avoidance be- 

 havior, including impairment of its acquisition in 

 cats; its retention was however unaltered (29), a 

 fact suggesting that amygdaloid lesions depress the 

 motivational facilitation for the acquisition of con- 

 ditioned avoidance. Somewhat diff"erent results were 

 however obtained in monkeys (252) where acquisi- 

 tion was only slightly slowed, but extinction of a 

 preoperatively acquired conditioned avoidance re- 

 sponse became more rapid than in normal controls. 

 Furthermore it seems that the motixational impact 

 of frustration was also diminished. 



Entirely opposite results to those so far reviewed 

 were however reported by Spiegel et al. (236) and 

 by Bard & Mountcastle (24) who found that bi- 

 lateral amygdalectomy in cats transforms a placid 

 animal into a savage beast reacting to the most 

 trifling stimuli with an outburst of well-directed 

 rage. The discrepancies of these findings with those 

 previously summarized cannot be explained on the 

 basis of a species difi^erence since amygdalectomy in 

 cats is also apt to produce placidity (186, 222-224). 

 Schreiner & Kling (223, 224) attempt to explain this 

 discrepancy by pointing out that amygdaloid lesions 

 produce savage behavior in carnivores only after 

 an initial period of docility and that aggressiveness 

 reappears with the onset of increased sexual behavior. 

 Since sexual excitement in carnivores is normally 

 associated with combative behavior, the return to 

 savageness may thus be part of the hypersexual 

 syndrome, a view corroborated by their observation 

 that subsequent castration will both abolish hyper- 

 sexuality and restore docility. It should however be 

 recalled that the cats in the experiments of Spiegel 



