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Changes in Emotionality Following Simultaneous Lesions of the Septal Region and Limbic Cortex

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Changes in Emotionality Following Simultaneous Lesions of the Septal Region and Limbic Cortex This dissertation has bean 6 6 -1 8 6 8 microfilmed exactly as received YUTZEY, David Alan, 1938- CHANGES IN EMOTIONALITY FOLLOWING SIMULTANEOUS LESIONS OF THE SEPTAL REGION AND LIMBIC CORTEX. The Ohio State University, Ph.D., 1965 Psychology, experimental University Microfilms, Inc., Ann Arbor, Michigan Copyright by David Alan Yutzey 1966 CHANGES IN EMOTIONALITY FOLLOWING SIMULTANEOUS LESIONS OF THE SEPTAL REGION AND LIMBIC CORTEX DISSERTATION Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy in the Graduate School of The Ohio State University By David Alan Yutzey, B. A., M. A. ******* The Ohio State University 1965 Approve* Adviser Department of Psycho' ACKNOWLEDGMENTS The author gratefully acknowledges his adviser, Professor Donald R. Meyer, for his aid and encouragement in all phases of the present study. 1 also wish to thank Professors William C. Howell and Raymond C. Miles, members of my reading committee, for their helpful comments concerning the early draft of this dissertation. Finally, to Dr. Patricia M. Meyer, for her participation in the rating of the animals and her suggestions during the conduct of the experiment, and to Mr. John Lauber, for his assistance in preparing the histological mate­ rials, I wish to express my appreciation. The author was supported under National Institute of Health Training Grant MH-6748 during the course of this research. ii VITA July 31, 1938 Born - Glendale, West Virginia 1960 ........ B. A., Ohio Wesleyan University, Delaware, Ohio 1960-1961 . Research Assistant, Laboratory of Aviation Psychology, The Ohio State University Research Foundation, Columbus, Ohio 1961-1965 . National Institute of Health Training Fellow, Laboratory of Comparative and Physiological Psychology, The Ohio State University Research Foundation, Columbus, Ohio 1963 ......... H. A., The Ohio State University, Columbus, Ohio 1963-1964 . Assistant Instructor, Department of Psychology, The Ohio State University, Columbus, Ohio PUBLICATIONS "Precedence effects in discrimination learning by normal and frontal monkeys." J. comp, physiol. Psychol.. 1964, 58, 472-474. (with Meyer, D. R . , Treichler, F. R. and Meyer, Patricia M.) "Emotionality changes following septal and neocortical ablations in rats." J. comp, physiol. Psychol.. 1964, 58, 463-465. (with Meyer, Patricia M. and Meyer, D. R.) "Effects of neocortical ablations on relearning of a black-white dis­ crimination habit by two strains of rats." J. comp, physiol. Psychol. (in press), (with Meyer, D. R., and Meyer, Patricia, M.) iii FIELDS OF STUDY Major Field: Physiological Psychology Studies in emotionality and learning after lesions of the neocortex and limbic system. Professor Donald R. Meyer Studies in discrimination learning and deficits in learning after lesions of the frontal neocortex in monkeys. Professor Donald R. Meyer Studies in sequential behavior in several species and after lesions of the frontal cortex. Professor Raymond C. Miles Studies in decision making and information processing behavior. Professor George E. Briggs iv CONTENTS Acknowledgments ...................................................... 11 Vita - Publications............... ............................. .. iii Fields of S t u d y ................................................... iv Introduction ........................................................ 1 Method .............................................................. 5 R e s u l t s ....................................................... 7 D i s c u s s i o n ....................................................... 10 Appendix I. Statistical Analysis and Average Emotionality Scores . 12 Appendix II. Analysis of Thalamic Degeneration and Discussion . 20 R e f e r e n c e s ....................................................... 23 v TABLES Table 1. Analysis of Variance for Groups, Days, and Groups by Days Interaction Effects ................................. 14 2. Analysis of Variance for Differences between Groups on Day 1 of Post-operative Ratings ............................ 15 3. Analysis of Variance for Differences between Groups on Day 2 of Post-operative Ratings ................................... 15 4. Newman-KueIs Studentized Range Tests on Differences between Pairs of Means on Day 1 of Post-operative Ratings ........... 16 5. Maim-Whitney U Tests between Pairs of Means of Interest . 17 6. Mean Emotionality Ratings for All Groups by D a y s ........... 18 7. Median Emotionality Ratings for All Groups by D a y s ......... 19 vi INTRODUCTION A forebear of much of the current research on the neural correlates of emotional behavior is the theoretical paper by James W. Papez (1937) entitled "A proposed theory of emotion." Based primarily on anatomical considerations, the "Papez theory of emotion" suggested that the limbic system of the forebrain, a group of interconnected structures previously regarded as functionally related to olfaction, had an equally important role in emotional behavior. Within a decade, the effect of this proposal was evident both in a revival of theoretical interest in the limbic system and in the advent of several programs of experimental research designed to investigate the effects of destruction or stimulation of various components of the system upon emotional behavior. Some of the most valuable discoveries in this field were made in a series of experiments by Bard and Mountcastle (1948) upon the neural correlates of emotional behavior in cats. These workers found that a complete neocortical ablation produced a placid animal, but that a subsequent lesion of the old cortex, either the transitional cortex of the midline or the pyriform-amygdaloid complex, led to a complete rever­ sal of Sjs response tendencies. Cats with neocortical ablations could be roughly handled without danger to the experimenter, but after the second lesion, these animals displayed extreme rage at the slightest provocation. The authors' interpretation of this phenomenon was that 1 2 the neocortex normally acted as a facilitator of emotional behavior and that the function of the old cortex was to inhibit this phylogenetically newer system. Although the implications of the Bard and Mountcastle study for a theory of emotion were significant, of equal importance was the demonstration of the usefulness of the sequential lesion procedure. Using this method, a behavior tendency produced by one lesion could be cancelled or even completely reversed by a second ablation of a function­ ally antagonistic system. Using the sequential lesion procedure as a research tool, several investigators began to study other functional relationships within the limbic system. Of clinical as well as theoretical interest was the possibility of surgically taming an animal in which a prior lesion had produced a propensity for angry behavior. One such hyperemotional prep­ aration was the septal rat (Brady and Nauta, 1953; King 1958, 1959) which exhibited striking hyperreactivity in response to tactile or audi­ tory stimulation. On the basis of research in which lesions of the amygdala were found to dampen emotional reactivity, King and Meyer (1958) suspected that septal hyperemotionality could be reduced by lesions of the amygdala. These workers found that the septal syndrome was indeed suppressed inmediately following bilateral destruction of the antagonistic system. Acting upon the suggestion of the King and Meyer experiment, that the removal of a facilltory system could reduce septal hyperemotionality, Yutzey, Meyer, and Meyer (1964) produced both sequen­ tial and simultaneous lesions of the septal region and of the neocortex, the structure which when completely removed in cats, had produced 3 placidity in the Bard and Mountcastle experiments. Due to the fact that a relatively long (21-days) recovery period was used in this experiment, animals with septal lesions had returned to normal levels of emotional­ ity by the time the surgical removal of the neocortex was accomplished, and Yutzey, Meyer, and Meyer were unable to obtain results comparable with the King and Meyer septal-amygdaloid study. However, an unexpected finding by the former workers was that animals with simultaneous septal- complete neocortical ablations were just as hyperemotional as rats with septal lesions observed within two days following surgery. In other words, the neocortical ablations apparently prevented the “spontaneous" attenuations of septal hyperemotionality during the 21-day recovery period. Since this first experiment, these investigators have also obtained maintained states of hyperemotionality with simultaneous septal- anterior neocortical and -posterior neocortical ablations in which less than 50% of the neocortex was removed (Meyer, Yutzey, and Meyer, in preparation). These results raised the question of whether the phenomenon of unattenuated hyperemotionality after the removal of the septal region and the neocortex could be replicated with lesions of other structures which, when destroyed alone, produced calming effects. Anatomical and functional similarities between limbic and neocortices suggested that comparable effects upon emotional behavior could be obtained with mid­ line cortex. Like the neocortex, the anterior cingulate (Area 24), posterior cingulate (Area 23), and the retrosplenial (Area 29 and 30) cortices are richly supplied with afferents from the thalamus, 4 respectively the anteromedial, anteroventral, and anterodorsal nuclei (Rose and Woolsey, 1948). In addition, on the basis of several anatom­ ical methods of
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