brain stimulation and affective behavior: a note on an early demonstration of a “reward center”

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Journal of the Hrrtory o/ the Behovloral Scirncer I7 (1981) 174-175 BRAIN STIMULATION AND AFFECTIVE BEHAVIOR: AiNOTE ON AN EARLY DEMONSTRATION OF A “REWARD CENTER’, JOHN KENYON The note concerns the “rescue” of an early study describing the “rewarding” effects of brain stimulation. “The history of a science is cumulative. . . . Despite the cumulative character of the history of psychology, the view that all that is potentially valuable survives into the pres- ent is false on several counts. . . . As new ideas are introduced a heretofore neglected, isolated point, not part of the contemporary picture, may need to be rescued from oblivion.”’ The present note concerns the rescue of an early study describing the effects of brain stimulation upon autonomic responses which is important in the historical account of physiological psychology.* At the same time it also serves to illustrate the shift towards operational definition in psychology as a result of new techological advances. The specification of a ‘reward center’ in the brain was given in 1954 when James Olds and Peter M. Milner showed that rats would bar-press at high rates for electrical, intracranial brain stimulation.8 Michel Victor Pachon and Valentin-Alfred-Paul Delmas-Marsalet, faced with a somewhat different problem, reported in 1924 their observations of an evident satisfaction (une satisfaction tvidente) following electrical stimulation of the caudate nucleus in the dog.‘ As they stated the problem: the physiology of the caudate nuclei was uncertain, and the nuclei were considered to be unresponsive to electrical stimulation (“la physiologie des noyaux caudes demeure assez incertaine, et I’opinion classique tend A les considtrer comme electriquement inexcitables”). Two reasons are offered for this state of affairs, one theoretical and the other methodological. First, the criterion for an effect of stimula- tion was judged on the basis of similarity to the effect of stimulating the motor cortex (“. . . la tendance que l’on a exiger, comme crittre de leur excitabilite, la production de mouvements comparables a ceux que determine une excitation tquivalenta de la zone motrice corticale.”) Second, the subjects were either anesthetized or suffered operative trauma (“le fait que les animaux sur lequels on optrait etaient anesthbiks ou avaient subi des traumatismes operatories considerables. . ,”) They decided to use a procedure, in- volving a minimum of trauma, for the stimulation of an awake animal. Two enameled copper electrodes were implanted unilaterally in the caudate nucleus of the dog. (After the experiment lesions were made using the same electrodes and the locations verified histologically.) A mild intermittent galvanic current, at the rate of twenty to thirty per second, was used for stimulating. The results on two dogs are reported. This research was supported in part by Grant AP-17 from the National Research Council of Canada to McGill University. JOHN KENVON is Associate Professor and Head of the Education Sainte-Anne. Church Point, Digby County. Nova Scoria. BOW IMO. Canada. He teaches courses in psychology and education. His main research interests in psychology are comparative-physiological I and history. 174

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Journal of the Hrrtory o/ the Behovloral Scirncer I7 (1981) 174-175

BRAIN STIMULATION AND AFFECTIVE BEHAVIOR: AiNOTE ON AN EARLY DEMONSTRATION OF A “REWARD CENTER’,

JOHN K E N Y O N

The note concerns the “rescue” of an early study describing the “rewarding” effects of brain stimulation.

“The history of a science is cumulative. . . . Despite the cumulative character of the history of psychology, the view that all that is potentially valuable survives into the pres- ent is false on several counts. . . . As new ideas are introduced a heretofore neglected, isolated point, not part of the contemporary picture, may need to be rescued from oblivion.”’

The present note concerns the rescue of an early study describing the effects of brain stimulation upon autonomic responses which is important in the historical account of physiological psychology.* At the same time it also serves to illustrate the shift towards operational definition in psychology as a result of new techological advances.

The specification of a ‘reward center’ in the brain was given in 1954 when James Olds and Peter M. Milner showed that rats would bar-press at high rates for electrical, intracranial brain stimulation.8 Michel Victor Pachon and Valentin-Alfred-Paul Delmas-Marsalet, faced with a somewhat different problem, reported in 1924 their observations of an evident satisfaction (une satisfaction tvidente) following electrical stimulation of the caudate nucleus in the dog.‘

As they stated the problem: the physiology of the caudate nuclei was uncertain, and the nuclei were considered to be unresponsive to electrical stimulation (“la physiologie des noyaux caudes demeure assez incertaine, et I’opinion classique tend A les considtrer comme electriquement inexcitables”). Two reasons are offered for this state of affairs, one theoretical and the other methodological. First, the criterion for an effect of stimula- tion was judged on the basis of similarity to the effect of stimulating the motor cortex (“. . . la tendance que l’on a exiger, comme crittre de leur excitabilite, la production de mouvements comparables a ceux que determine une excitation tquivalenta de la zone motrice corticale.”) Second, the subjects were either anesthetized or suffered operative trauma (“le fait que les animaux sur lequels on optrait etaient anesthbiks ou avaient subi des traumatismes operatories considerables. . ,”) They decided to use a procedure, in- volving a minimum of trauma, for the stimulation of an awake animal.

Two enameled copper electrodes were implanted unilaterally in the caudate nucleus of the dog. (After the experiment lesions were made using the same electrodes and the locations verified histologically.) A mild intermittent galvanic current, at the rate of twenty to thirty per second, was used for stimulating. The results on two dogs are reported.

T h i s research was supported in part by Grant AP-17 from the National Research Council of Canada to McGill University.

JOHN KENVON is Associate Professor and Head of the Education Sainte-Anne. Church Point, Digby County. Nova Scoria. BOW IMO. Canada. He teaches courses in psychology and education. His main research interests in psychology are comparative-physiological I and history.

174

BRAIN STIMULATION AND AFFECTIVE BEHAVIOR 175

The stimulation would arouse a sleeping dog. The face on the contralateral side became more expressive; the lips would begin to move, and then the animal would make chewing movements. Soon the dog began to lick its lips with evident satisfaction, in- dicating an agreeable affective state (“Bientdt la langue se montre entre les arcades den- taires et, passant sur les lkres et le museau, realise un net pourlkhage, qui indique une kvidente satisfaction, et il semble bien que l’on determine chez I’animal un &at affectif d’un caractere agreable non douteux.”) Swallowing and slow contralateral head rolling occurred. With prolonged stimulation the animal would get up and make walking movements on the contralateral side. Respiration was noticeably accelerated. No choreic or athetoid movements were observed.

Pachon and Delmas-Marsalet concluded that the caudate nucleus plays a role in the expression of affective states as well as in the automatic movements of walking. No histology is presented in this early paper.

Clearly the behavioral technology of the Skinner-box type would have strengthened their interpretation of the dogs’ “affective” responses, but apart from this one aspect the report fits remarkably well the picture found in current documents of the rewarding effects of electrical brain stimulation.6

Using a combination of stimulation and lesion techniques A. M. Laursen has shown that the “affective” responses are due to the spread of stimulation from electrodes placed in the caudate nucleus.6

NOTES

I . Robert I. Watson, “The Role and Use of History in the Psychology Curriculum,” Journal ofrhe Hirrory of rhe Behavioral Sciences 2 (1966): 64-69. 2. In a personal communication (1967) Professor Valentin-Alfred-Paul Delmas-Marsalet wrote that “depuis 1925, de nombreux auteurs ont retrouvt ce que j’avais h i t ” but the emphasis has been upon determining the locus for the movements elicited and not upon the importance of the study in the historical context of affective behavior. See, e.g., Arne Mosfeldt Laursen, “Movements Evoked from the Region of the Caudate Nucleus in Cats,” Acia Physiologica Scandinavica 54 (1962): 175-184. 3. James Olds and Peter M. Milner. “Positive Reinforcement Produced by Electrical Stimulation of Scptal Area and Other Regions of Rat Brain,”Journal of Comparative and Physiological Psychology 47 (1954): 419- 421. 4. Michel Victor Pachon and Valentin-Alfred-Paul Delmas-Marsalet, “Effets Produits par I’Excitation El=- trique des Noyaux CaudC chcz le Chien Eveilk,” Compre Rendu de la SociDle de Eiologie 91 (1924): 558-560. The work was later published in greater detail by Delmas-Marsalet as a thesis: “Contribution Exphimentalc B I’Etude des Fonctions du Noyau Caudt (These de I’Universitt de Bordeaux, Facultt de Medecine et de Phar- macie 108 [ 1924- 19251). 5 . 6. Laursen, “Movements Evoked.”

See Olds and Milncr. “Positive Reinforcement.”