The Science of Sentiment: The Problem of the Cerebral Localization of Emotion

  • John R. Durant


This chapter considers the problem of the localization of specific functions within the central nervous system, by means of a detailed examination of the development of the idea of the “limbic system” with reference to a group of functionally interrelated forebrain structures subserving emotion. The origins of the idea of the limbic system are traced in a number of overlapping scientific disciplines in the first part of this century, including neuroanatomy, neurophysiology, and psychophysiology, together with several closely related medical specialities, including neurology and psychiatry. The chapter identifies a number of key evolutionary and psychological assumptions underlying the idea of the existence of emotional centers in the brain, and it argues that these illustrate some of the limitations inherent in the idea of functional localization itself. At best, this idea represents an early stage in the development of a mature theory of the relationship between brain and behavior; at worst, it represents a poor substitute for it.


Frontal Lobe Limbic System Functional Localization Bodily Change Brain Science 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Bard, P. (1928). A diencephalic mechanism for the expression of rage with special reference to the sympathetic nervous system. Am. J. Physiol. 84:490–513.Google Scholar
  2. Bard, P. (1934). Emotion: 1. The neurohumoral basis of emotional reactions. In Murchison, C. A. (ed.), A Handbook of General Experimental Psychology, Clark University Press, Hanover, pp. 264–311.Google Scholar
  3. Barnett, S. A. (1981). Modern Ethology. The Science of Animal Behavior, Oxford University Press, Oxford.Google Scholar
  4. Brain, W. R. (1927). On the significance of the flexor posture of the upper limb in hemiplegia, with an account of a quadrupedal extensor reflex. Brain 50:113–137.Google Scholar
  5. Broca, P. (1878). Anatomie comparée des circonvolutions cérébrales. Le grand lobe limbique et la scissure limbique dans la série des mammifères. Rev. Anthropol. 1:285–498.Google Scholar
  6. Cannon, W. B. (1911). The Mechanical Factors of Digestion, Longmans, Green, & Co., New York.Google Scholar
  7. Cannon, W. B. (1915). Bodily Changes in Pain, Hunger, Fear, and Rage, Appleton, New York.Google Scholar
  8. Cannon, W. B. (1927). The James-Lange theory of emotions. Am. J. Physiol. 39:106–124.Google Scholar
  9. Cannon, W. B., and Britton, S. W. (1925). Studies on the conditions of activity in endocrine glands. XV. Pseudaffective medulliadrenal secretion. Am. J. Physiol. 72:283–294.Google Scholar
  10. Chorover, S. L. (1976). The pacification of the brain: From phrenology to psychosurgery. In Morley, T. P. (ed.), Current Controversies in Neurosurgery, Saunders, Philadelphia, pp. 730–767.Google Scholar
  11. Cobb, S. (1946). Borderlands of Psychiatry, Harvard University Press, Cambridge, Massachusetts.Google Scholar
  12. Cobb, S. (1949). Human nature and the understanding of disease. In Faxon, N. W. (ed.), The Hospital in Contemporary Life, Harvard University Press, Cambridge, Massachusetts, pp. 108–136.Google Scholar
  13. Cobb, S. (1950). Emotions and Clinical Medicine, Norton, New York.Google Scholar
  14. Cools, A. R. (1981). Aspects and prospects of the concept of neurochemical and cerebral organization of aggression: Introduction of new research strategies in “Brain and Behaviour” studies. In Brain, P. F., and Benton, D. (eds.), The Biology of Aggression, Sijthoff and Noordhoff, Alphen aan den Rijn, The Netherlands, pp. 405–425.Google Scholar
  15. Crawford, M. P., Fulton, J. F., Jacobsen, C. F., and Wolfe, J. B. (1948). Frontal lobe ablation in chimpanzee: A resume of “Becky” and “Lucy.” Res. Pub. Assoc. Nerv. Ment. Dis. 27:3–58.Google Scholar
  16. Dawkins, R. (1976). Hierarchical Organisation: A candidate principle for ethology. In Bateson, P. P., and Hinde, R. A. (eds.), Growing Points in Ethology, Cambridge University Press, London.Google Scholar
  17. Delgado, J. M. R. (1964). Free behavior and brain stimulation. Int. Rev. Neurobiol. 6:349–449.PubMedGoogle Scholar
  18. Delgado, J. M. R. (1965). Evolution of Physical Control of the Brain, American Museum of Natural History, New York.Google Scholar
  19. Delgado, J. M. R. (1969). Physical Control of the Mind: Toward a Psycho-Civilized Society, Harper and Row, New York.Google Scholar
  20. Denny-Brown, D. (1951). The frontal lobes and their functions. In Feiling, A. (ed.), Modern Trends in Neurology, Butterworth, London, pp. 13–89.Google Scholar
  21. Freeman, W., and Watts, J. W. (1950). Psychosurgery, 2nd ed., Blackwell, Oxford.Google Scholar
  22. Friedman, E. D. (1920). On a possible significance of the Babinski reflex. J. Nerv. Ment. Dis. 51:146–149.Google Scholar
  23. Fritsch, G., and Hitzig, E. (1870). Über die elektrische Erregbarkeit des Grosshirns. Arch. Anat. Physiol. Wiss. Med. 37:300–332.Google Scholar
  24. Fulton, J. F. (1932). New horizons in physiology and medicine: The hypothalamus and visceral mechanisms. N. Engl. J. Med. 207:60–68.Google Scholar
  25. Fulton, J. F. (1933–1934). Paralyses of cortical origin. A physiological analysis of flaccid and spastic states in monkeys and chimpanzees. Proc. Calif. Acad. Med. 1933–1934:1–20.Google Scholar
  26. Fulton, J. F. (1937–1939). The chimpanzee in experimental medicine. Trans. Kansas City Acad. Med. 1937–1939:1–12.Google Scholar
  27. Fulton, J. F. (1938). Physiology of the Nervous System, Oxford University Press, London.Google Scholar
  28. Fulton, J. F. (1939). Levels of autonomic function with particular reference to the cerebral cortex. Res. Publ. Assoc. Nerv. Ment. Dis. 19:219–236.Google Scholar
  29. Fulton, J. F. (1949). Functional Localization in the Frontal Lobes and Cerebellum, Clarendon Press, Oxford.Google Scholar
  30. Fulton, J. F. (1951). Frontal Lobotomy and Affective Behavior. A Neurophysiological Analysis, Norton, New York.Google Scholar
  31. Fulton, J. F. (1952). The Frontal Lobes and Human Behaviour, University of Liverpool Sherrington Lectures (2), Liverpool.Google Scholar
  32. Fulton, J. F., and Ingraham, F. D. (1929). Emotional disturbances following experimental lesions of the base of the brain (pre-chiasmal). J. Physiol. 67:xxvii–xxviii.Google Scholar
  33. Fulton, J. F., and Jacobsen, C. J. (1935). The functions of the frontal lobes, A comparative study in monkeys, chimpanzees and man, Adv. Mod. Biol. (Moscow) 4:113–123.Google Scholar
  34. Fulton, J. F., and Keller, A. D. (1932). The Sign of Babinski. A Study of the Evolution of Cortical Dominance in Primates, Bailliere, Tindall, and Cox, London.Google Scholar
  35. Fulton, J. F., and Kennard, M. A. (1932). A study of flaccid and spastic paralyses produced by lesions of the cerebral cortex in primates. Proc. Assoc. Res. Nerv. Ment. Dis. 13:158 – 210.Google Scholar
  36. Gould, S. J. (1977). Ontogeny and Phylogeny, Harvard University Press, Cambridge, Massachusetts.Google Scholar
  37. Head, H. (1920). Studies in Neurology, Hodder and Stoughton, London.Google Scholar
  38. Head, H., and Holmes, G. (1911–1912). Sensory disturbances from cerebral lesions. Brain 34:102–254.Google Scholar
  39. Head, H., and Riddoch, G. (1918). The autonomic bladder, excessive sweating and some other reflex conditions, in gross injuries of the spinal cord. Brain 40:188–263.Google Scholar
  40. Hess, W. R. (1932–1938). Beiträge zur Physiolgie des Hirnstammes, I. G. Thieme, Leipzig.Google Scholar
  41. Hinde, R. A. (1982). Ethology. Its Nature and Relations with Other Sciences, Collins, Glasgow.Google Scholar
  42. Jackson, J. H. (1932). Selected Writings of John Hughlings Jackson (Taylor, J., ed.), Hodder and Stoughton, London.Google Scholar
  43. Jacobsen, C. F., Wolfe, J. B., and Jackson, T. A. (1935). An experimental analysis of the functions of the frontal association areas in primates. J. Nerv. Ment. Dis. 82:1–14.Google Scholar
  44. James, W. (1884). What is an emotion? Mind 9:188–205.Google Scholar
  45. James, W., and Lange, C. G. (1922). The Emotions, Williams and Wilkins, Baltimore.Google Scholar
  46. Knorr-Cetina, K. D. (1981). The Manufacture of Knowledge; An Essay on the Constructivist and Contextual Nature of Science, Pergamon Press, Oxford.Google Scholar
  47. Knorr-Cetina, K. D., and Mulkay, M. (1983). Science Observed. Perspectives on the Social Study of Science, Sage, London.Google Scholar
  48. Koestler, A. (1967). The Ghost in the Machine, Hutchinson, London.Google Scholar
  49. Koestler, A., and Smythies, J. R. (eds.) (1969). Beyond Reductionism: New Perspectives in the Life Sciences, Hutchinson, London.Google Scholar
  50. Livingstone, K. E., and Hornykiewicz, O. (eds.) (1978). Limbic Mechanisms. The Continuing Evolution of the Limbic System Concept, Plenum Press, New York.Google Scholar
  51. Long, M. (1980). Ritual and deceit. Sci. Digest 1:86–91, 121.Google Scholar
  52. Lovejoy, A. O. (1936). The Great Chain of Being, Harvard University Press, Cambridge, Massachusetts.Google Scholar
  53. MacLean, P. D. (1949). Psychosomatic disease and the “visceral brain.” Recent developments bearing on the Papez theory of emotion. Psychosom. Med. 11:338–353.PubMedGoogle Scholar
  54. MacLean, P. D. (1952). Some psychiatric implications of physiological studies on fronto-temporal portions of the limbic systems (visceral brain). Electroencephalogr. Clin. Neu-rophysiol. 4:407–418.Google Scholar
  55. MacLean, P. D. (1954). The limbic system and its hippocampal formations. Studies in animals and their possible application to man. J. Neurosurg. 11:29–44.PubMedGoogle Scholar
  56. MacLean, P. D. (1958a). Contrasting functions of limbic and neocortical systems of the brain and their relevance to psychophysiological aspects of medicine. Am. J. Med. 25:611–626.PubMedGoogle Scholar
  57. MacLean, P. D. (1958b). The limbic system with respect to self-preservation and the preservation of the species. J. Nerv. Ment. Dis. 127:1–11.PubMedGoogle Scholar
  58. MacLean, P. D. (1962). New findings relevant to the evolution of psychosexual functions of the brain. J. Nerv. Ment. Dis. 135:289–301.Google Scholar
  59. MacLean, P. D. (1964). Mirror display in the squirrel monkey, Saimiri sciureus. Science 146:950–952.Google Scholar
  60. MacLean, P. D. (1967). The brain in relation to empathy and medical education. J. Nerv. Ment. Dis. 14:180–182.Google Scholar
  61. MacLean, P. D. (1968). Alternative neural pathways to violence. In Ng, L. (ed.), Alternatives to Violence, Time-Life Books, New York, pp. 24–34.Google Scholar
  62. MacLean, P. D. (1969). The paranoid streak in man. In Koestler, A., and Smythies, J. R. (eds.), Beyond Reductionism: New Perspectives in the Life Sciences, Hutchinson, London, pp. 258–278.Google Scholar
  63. MacLean, P. D. (1970). The triune brain, emotion, and scientific bias. In Schmitt, F. O. (ed.), The Neurosciences: Second Study Program, Rockefeller University Press, New York, pp. 336–349.Google Scholar
  64. MacLean, P. D. (1972a). Implications of microelectrode findings on exteroceptive inputs to the limbic cortex. In Hockman, C. H. (ed.), Limbic Mechanisms and Autonomic Function, C. C. Thomas, Springfield, Illinois, pp. 115–136.Google Scholar
  65. MacLean, P. D. (1972b). Cerebral evolution and emotional processes: New findings on the striatial complex. Ann. N.Y. Acad. Sci. 193:137–149.PubMedGoogle Scholar
  66. MacLean, P. D. (1973a). A triune concept of the brain and behavior. In Boag, T., and Campbell, D. (eds.), The Hincks Memorial Lectures, 1969, University of Toronto Press, Toronto, pp. 4–66.Google Scholar
  67. MacLean, P. D. (1973b). The brain’s generation gap: Some human implications. Zygon 8:113–127.Google Scholar
  68. MacLean, P. D. (1978a). Challenges of the Papez heritage. In Livingston, K. E., and Hornykiewicz, O. (eds.), Limbic Mechanisms. The Continuing Evolution of the Limbic System Concept, Plenum Press, New York, pp. 1–15.Google Scholar
  69. MacLean, P. D. (1978b). On the evolution of three mentalities. In Washburn, S. L., and McCown, C. R. (eds.), Human Evolution; Biosocial Perspectives, Benjamin Cummings, Menlo Park, California, pp. 33–57.Google Scholar
  70. MacLean, P. D. (1981). Letter to the editor. Sci. Digest, April 1981(April):10.Google Scholar
  71. MacLean, P. D. (1982). On the origin and progressive evolution of the triune brain. In Armstrong, E., and Falk, D. (eds.), Primate Brain Evolution: Methods and Concepts, Plenum Press, New York, pp. 291–316.Google Scholar
  72. MacLean, P. D., and Delgado, J. M. R. (1953). Electrical and chemical stimulation of frontotemporal portion of limbic system in the waking animal. Electroencephalogr. Clin. Neurophysiol. 5:91–100.PubMedGoogle Scholar
  73. Mark, V. H., and Ervin, F. R. (1970). Violence and the Brain, Harper and Row, New York.Google Scholar
  74. Masserman, J. H. (1942). The hypothalamus in psychiatry. Am. J. Psychiatr. 98:633–637.Google Scholar
  75. Miller, J. (1972). The dog beneath the skin. Listener 1972(20 July):74–76.Google Scholar
  76. Moniz, E. (1936). Tentatives opératoires dans le traitement de certaines psychoses, Masson, Paris.Google Scholar
  77. Nauta, W. J. H. (1979). Expanding borders of the limbic system concept. In Rassmussen, T., and Marino, R. (eds.), Functional Neurosurgery, Raven Press, New York, pp. 7–23.Google Scholar
  78. Nauta, W. J. H., and Domesick, V. B. (1982). Neural associations of the limbic system. In Beckman, A. (ed.), Neural Basis of Behavior: Proceedings of the Dupont Symposium on Neural Substrates of Behavior, MTP Press, Lancaster, pp. 175–206.Google Scholar
  79. O’Callaghan, M. A. J., and Carroll, D. (1982). Psychosurgery. A Scientific Analysis, MTP Press, Lancaster.Google Scholar
  80. Papez, J. W. (1937). A proposed mechanism of emotion. Arch. Neurol. Psychiatr. 38:725–743.Google Scholar
  81. Ploog, D. (1970). Social communication among animals. In Schmitt, F. O. (ed.), The Neurosciences: Second Study Program, Rockefeller University Press, New York, pp. 349–361.Google Scholar
  82. Ploog, D. (1971). Neurological aspects in social behavior. In Eisenberg, J. F., and Dillons, W. S. (eds.), Man and Beast, Comparative Social Behavior, Smithsonian Institution Press, Washington, pp. 95–125.Google Scholar
  83. Ploog, D. (1976). Similarities and differences of behavior as a function of cerebral evolution and dissolution. In von Cranach, M. (ed.), Methods of Inference from Animal to Human Behavior, Aldine, Chicago, pp. 143–163.Google Scholar
  84. Ploog, D., and MacLean, P. D. (1963). Display of penile erection in squirrel monkey (Saimiri sciureus). Anim. Behav. 11:32–39.Google Scholar
  85. Ranson, S.W. (1934). The hypothalamus: Its significance for visceral innervation and emotional expression. Trans. Coll. Physic. Philad. 2:222–242.Google Scholar
  86. Riese, W. (1959). A History of Neurology, MD, New York.Google Scholar
  87. Rivers, W. H. R. (1922). Instinct and the Unconscious. A Contribution to a Biological Theory of the Psycho-Neuroses, 2nd ed., Cambridge University Press, Cambridge.Google Scholar
  88. Sagan, C. (1977). The Dragons of Eden. Speculations on the Evolution of Human Intelligence, Hodder and Stoughton, London.Google Scholar
  89. Shepherd, G. M. (1983). Neurobiology, Oxford University Press, Oxford.Google Scholar
  90. Sherrington, C.S. (1898). Decerebrate rigidity, and reflex coordination of movements. J. Physiol 22:319–332.PubMedGoogle Scholar
  91. Sherrington, C.S. (1900). Experiments on the value of vascular and visceral factors for the genesis of emotion. Proc. R. Soc. 66:390–403.Google Scholar
  92. Spencer, H. (1855). The Principles of Psychology, Longman, Brown, Green, and Longmans, London.Google Scholar
  93. Stepansky, P. E. (1977). A History of Aggression in Freud, International Universities Press, New York.Google Scholar
  94. Sulloway, F. J. (1979). Freud, Biologist of the Mind, Basic Books, London.Google Scholar
  95. Sydney Smith, J., and Kiloh, L. G. (1977). Psychosurgery and Society, Pergamon Press, Oxford.Google Scholar
  96. Temkin, O. (1947). Gall and the phrenological movement, Bull. Hist. Med. 21:275–321.PubMedGoogle Scholar
  97. Tinbergen, N. (1951). The Problem of Instinct, Clarendon Press, Oxford.Google Scholar
  98. Valenstein, E. S. (1973). Brain Control: A Critical Examination of Brain Stimulation and Psychosurgery, Wiley, New York.Google Scholar
  99. Valenstein, E. S. (ed.) (1980). The Psychosurgery Debate. Scientific, Legal, and Ethical Perspectives, Freeman, San Francisco.Google Scholar
  100. Welker, W. (1976). Mapping the brain. Historical trends in functional localization. Brain Behav. Evol. 13:327–343.PubMedGoogle Scholar
  101. Young, R. M. (1970). Mind, Brain and Adaptation in the Nineteenth Century. Cerebral Localization and its Biological Context from Gall to Ferrier, Clarendon Press, Oxford.Google Scholar

Copyright information

© Plenum Press, New York 1985

Authors and Affiliations

  • John R. Durant
    • 1
  1. 1.Department of External StudiesUniversity of OxfordOxfordEngland

Personalised recommendations