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HANDBOOK OF PHYSIOLOGY 



NEUROPHYSIOLOGY III 



mousl) with limbic system in referring to forebrain 

 participants in affective processes lout should be re- 

 Stricted to those structures subserving; olfactory func- 

 tions, including the olfactory bulb and tubercle, 

 prcpyriform and periamygdaloid cortex, some of the 

 nuclei of the amygdaloid complex, and the bed 

 nucleus of the stria tcrminalis. 



Almost simultaneously with the 1937 publication 

 of Papez' theoretical effort, Kliiver & Bucy reported 

 their most striking demonstration of the important 

 participant role which rather extensive "limbic sys- 

 tem' components could be expected to play in the 

 balancing, integration and elaboration of critically 

 profound motivational-emotional behavior patterns. 

 These now classic experiments (217-219), defining 

 dramatic behavioral changes in monkeys following 

 temporal neocortical and paleocortical lesions in- 

 volving the frontotemporal cortex, pyriform lobe, 

 amygdaloid complex, presubiculum and hippocam- 

 pus, are now too well known to require detailed 

 review. The broad range of behavioral alterations 

 observed in these preparations, however, can be 

 seen to bear directly upon the central problem of 

 nervous system participation in affective processes. 

 The formerly wild and intractable rhesus macaques 

 used in these experiments became tame and docile, 

 showing signs of neither fear nor anger, following 

 this rather extensive involvement of the limbic sys- 

 tem. They would not light or retaliate when abused 

 by other monkeys and also displayed what the authors 

 refer to as 'psychic blindness,' oral tendencies and 

 hypermetamorphosis, a kind of compulsive behavior. 

 They behaved as if they could no longer discrimi- 

 nate between objects that were either potentially 

 dangerous or useful to them Such an animal would, 

 as il by compulsion, smell and mouth everything 

 (dirt, feres, nails, food) thai captured its attention. 

 Unless the objeel wen- edible, it was immediately 

 dropped. If presented with a nail 100 times in suc- 

 cession, the animal would smell and mouth it each 

 time as though he had not examined ii before. 

 Finally, these animals showed striking changes in 

 sexual behavior; thev appeared hypcrsexed, mastur- 

 bated excessively, sought partnership with male or 

 female indiscriminately, and manifested bizarre oral 

 sexual behavior. ( )l particular interest, too, was the 

 fa< 1 that when unilateral excision of only one lobe 

 was accomplished, or when bilateral lesions were 

 restricted to the temporal neocortex and spared the 

 limbic system structures, the animals failed to show 

 ;ni\ of these dramatic changes in behavior. 



Vgainsl the background oi these earl) experimental 



and theoretical efforts, a host of important subse- 

 quent neurophysiological and neuropsychological 

 developments have continued to broaden the base 

 for a more thorough understanding of extensive 

 limbic system components involved in the mediation 

 of emotional behavior. Within a few short months of 

 these first reports, Spiegel and his co-workers (355) 

 clearly demonstrated the dramatic participation of 

 the more rostral portions of the limbic system (in- 

 cluding the olfactory tubercle and septal region) in 

 rather complicated motivational-emotional behavior 

 patterns. 'Sham-rage' reactions were observed by 

 these authors following bilateral lesions confined 

 to the olfactory tubercle and septal region in both 

 cats and dogs, while similar effects resulted from 

 involvement of the anterior amygdaloid nuclei, 

 parts of the hippocampus, and the fornix. Indeed, 

 a somewhat earlier report by Fulton & Ingram (135) 

 had described similar "rage" reactions in cats follow- 

 ing bilateral prechiasmal lesions at the base of the 

 brain, and more recent reports by Brady & Xaut.i 

 (53, 54) confirm these findings in the rat. In addition, 

 a recent publication by Heath et al. (168) further 

 reflects the participant role of these more rostral 

 limbic system components in the elaboration of 

 emotional behavior, and the most dramatic demon- 

 strations of rewarding effects consequent upon direct 

 electrical stimulation of these same anteriorly placed 

 limbic structures (including the orbital surface of 

 the frontal lobes, the head of the caudate nucleus and 

 the anterior hypothalamus I (4b, 300, 301, 342 1 

 would seem to establish firmly their involvement in 

 affective processes. 



The most extensive and systematic research pro- 

 gram initiated by Bard & Mountcastle (15, 16) 

 within the decade following the report by Kliiver 

 & Bucy represents an important landmark in the 

 further experimental analysis of limbic system rela- 

 tionships and emotional behavior. Concerned pri- 

 marily with the role of forebrain mechanisms in the 

 expression of "rage' and 'angry behavior,' their 

 initial experiments with cats showed that removal 

 of all neocortex, while sparing the paleocortical, 



juxtallocortical and related subcortical compo- 

 nents of the limbic- svstcm, produced a markedly 

 placid and emotionally unresponsive animal. In 

 the authors' view, these results indicated (hat por- 

 tions of the limbic system, either singly or in con- 

 cert, could exert a restraining influence upon lower 

 brain mechanisms ol demonstrated prepotence in 



the mediation of gross affective expression. More- 

 over, subsequent experiments in this same scries 



