Abstract
A sophisticated ability both to generate displays of emotion and to respond to expressive behaviors of other individuals has emerged as a specialization in the course of primate evolution. Studies of the social behavior of nonhuman primates, especially those most related to ourselves, indicate that monkeys and apes are able to interpret social signals so as to assess the motivations of others. Studies of brain activity in monkeys looking at pictures of faces, facial expressions, and body movements, reveal regions of apparent specialized responsiveness to visual social stimuli. The existence of a discrete neural system in humans for cognition which generates a psychological model of others is suggested by patterns of deficit seen in certain neurologic syndromes. Empathy has several components and appears to lie on an evolutionary continuum.
Similar content being viewed by others
References
Allman, J. (1982). Reconstructing the evolution of the brain in primates through the use of comparative neurophysiological and neuroanatomical data. In E. Armstrong & D. Falk (Eds.),Primate brain evolution: Methods and concepts. New York: Plenum Press.
Ardila, A. & Rosseli, M. (1988). Temporal lobe involvement in Capgras syndrome.International Journal of Neuroscience, 43, 219–224.
Attwood, A., Frith, U., & Hermelin, B. (1988). The understanding and use of interpersonal gestures by autistic and Down's syndrome children.Journal of Autism and Developmental Disorders, 18; 241–57.
Bachevalier, J. (in press). Memory loss and socio-emotional disturbances following neonatal damage of the limbic system in monkeys: An animal model for childhood autism. In C. A. Tamminga & S. C. Schulz, (Eds.),Advances in neuropsychiatry and psychopharmacology. Vol. 1. Schizophrenia research (pp. 129–140). New York: Raven Press.
Basch, M. F. (1983). Empathic understanding: A review of the concept and some theoretical considerations.Journal of the American Psychoanalytic Association, 31, 101–126.
Bauman, M. L. & Kemper, T. L. (1985). Histoanatomic observations of the brain in early infantile autism.Neurology, 35, 866–874.
Baylis, G., Rolls, E. T., & Leonard, C. M. (1985). Selectivity between faces in the responses of a population of neurons in the cortex in the superior temporal sulcus of the monkey.Brain Research, 342, 91–102.
Bouckoms, A., Martuza, R., & Henderson, M. (1986). Capgras syndrome with subarachnoid hemorrhage.Journal of Nervous and Mental Disease, 174, 484–488.
Brothers, L. (1990). The social brain: A project for integrating primate behavior and neurophysiology in a new domain.Concepts in Neuroscience, 1, 27–51.
Brothers, L., Ring, B., & Kling, A. (1990). Response of neurons in the macaque amygdala to complex social stimuli.Behavioural Brain Research, 41, 199–213.
Bruce, C., Desimone, R., & Gross, C. G. (1981). Visual properties of neurons in a polysensory area in superior temporal sulcus of the macaque.Journal of Neurophysiology, 46, 369–384.
Byrne, R., & Whiten, A. (Eds.). (1988).Machiavellian intelligence: Social expertise and the evolution of intellect in monkeys, apes, and humans. Oxford, England: Clarendon Press.
Cheney, D. L. & Seyfarth, R. (1990).How monkeys see the world. Chicago: University of Chicago Press.
Darwin, C. (1872).The expression of the emotions in man and animals (p. 12). New York: D. Appleton.
DeWaal, F. (1989).Peacemaking among primates. Cambridge, MA: Harvard University Press.
Desimone, R., Albright, T. D., Gross, C. G., & Bruce, C. (1984). Stimulus-selective properties of inferior temporal neurons in the macaque.Journal of Neuroscience, 4, 2051–2062.
Eslinger, P. J., & Damasio, A. R. (1985). Severe disturbance of higher cognition after bilateral frontal lobe ablation: Patient EVR.Neurology, 35, 1731–1741.
Fishbain, D. A., & Rosomoff, H. (1986/1987). Capgras syndrome associated with metrizamide myelography.International Journal of Psychiatry in Medicine, 16, 131–136.
Gloor, P. (1986). Role of the human limbic system in perception, memory, and affect: Lessons from temporal lobe epilepsy. In B. K. Doane & K. E. Livingston (Eds.),The limbic system: Functional organization and clinical disorders. New York: Raven Press.
Hasselmo, M. E., Rolls, E. T., & Baylis, G. C. (1989). the role of expression and identity in the face-selective responses of neurons in the temporal visual cortex of the monkey.Behavioural Brain Research, 32, 203–218.
Hobson, R. P. (1986). The autistic child's appraisal of expressions of emotion.Journal of Child Psychology and Psychiatry, 27, 321–342.
Humphrey, N. (1983).Consciousness regained. Oxford, England: Oxford University Press.
Joseph, A. B. (1985). Bitemporal atrophy in a patient with Fregoli syndrome, syndrome of intermetamorphosis, and reduplicative paramnesia [letter to the editor].American Journal of Psychiatry, 142, 146–147.
Kling, A., & Brothers, L. (1990). The amygdala and social behavior. In J. Aggleton (Ed.),The amygdala. New York: John Wiley and Sons.
Kling, A., Lloyd, R., & Perryman, K. (1987). Slow-wave changes in amygdala to visual, auditory, and social stimuli following lesions of the inferior temporal cortex in squirrel monkey (Saimiri sciureus).Behavioural and Neural Biology, 47, 54–72.
Kling, A., & Steklis, H. D. (1976). A neural substrate for affiliative behavior in nonhuman primates.Brain Behavior and Evolution, 13, 216–238.
LeBon, G. (1903).The crowd. London: Fisher Unwin.
Mundy, P., Sigman, M., Ungerer, J., & Sherman, T. (1986). Defining the social deficits of autism: The contribution of non-verbal communication measures.Journal of Child Psychology and Psychiatry, 27, 657–669.
Perrett, D. I., Harries, M. H., Chitty, A. J., & Mistlin, A. J. (1990). Three stages in the classification of body movements by visual neurones. In H. B. Barlow, C. Blakemore, & M. Weston-Smith (Eds.),Images and Understanding, Cambridge, England: Cambridge University Press.
Perrett, D. I., & Mistlin, A. J. (1990). Perception of facial characteristics by monkeys. In M. Berkeley & W. Stebbins (Eds.),Comparative perception. New York: John Wiley and Sons.
Perrett, D. I., Mistlin, A. J., Harries, M. H., & Chitty, A. J. (1990). Understanding the visual appearance and consequence of hand actions. In M. A. Goodale (Ed.),Vision and action: The control of grasping. Norwood, NJ: Albex.
Perrett, D. I., Rolls, E. T., & Caan, W. (1982). Visual neurons responsive to faces in the monkey temporal cortex.Experimental Brain Research, 47, 329–342.
Perrett, D. I., Smith, P. A. J., Potter, D. D., Mistlin, A. J., Head, A. S., Milner, A. D., & Jeeves, M. A. (1984). Neurones responsive to faces in the temporal cortex: Studies of functional organization, sensitivity to identity and relation to perception.Human Neurobiology, 3, 197–208.
Perrett, D. I., Smith, P. A. J., Potter, D. D., Mistlin, A. J., Head, A. S., Milner, A. D., & Jeeves, M. A. (1985). Visual cells in the temporal cortex sensitive to face view and gaze direction.Proceedings of the Royal Society of London B, 223, 293–317.
Premack, D. ‘Does the chimpanzee have a theory of mind?’ revisited. In R. Byrne & A. Whiten (Eds.),Machiavellian intelligence: Social expertise and the evolution of intellect in monkeys, apes, and humans. Oxford, England: Clarendon Press.
Price, J. L., Russchen, F. T., & Amaral, D. G. (1987). The amygdaloid complex. In L. W. Swanson, A. Bjorklund, & T. Hokfelt (Eds.),Handbook of chemical neuroanatomy: Vol. 5. Integrated systems, part 1. New York: Elsevier.
Provine, R. R. (1986): Yawning as a stereotyped action pattern and releasing stimulus.Ethology, 72 109–122.
Signer, S. F. (1987). Capgras' syndrome: The delusion of substitution.Journal of Clinical Psychiatry, 48, 147–150.
Wing, L. (Ed.). (1988).Aspects of Autism: Biological research. Oxford, England: Alden Press.
Yamane, S., Kaji, S., & Kawano, K. (1988). What facial features activate face neurons in the inferotemporal cortex of the monkey?Experimental Brain Research, 73, 209–214.
Author information
Authors and Affiliations
Additional information
Based on a presentation given in New Orleans on February 17, 1990, at the AAAS symposium “Empathy in Infancy and Later Development.” Supported by the Department of Veterans Affairs.
Rights and permissions
About this article
Cite this article
Brothers, L. The neural basis of primate social communication. Motiv Emot 14, 81–91 (1990). https://doi.org/10.1007/BF00991637
Issue Date:
DOI: https://doi.org/10.1007/BF00991637