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Love hurts: The evolution of empathic concern through the encephalization of nociceptive capacity

Published online by Cambridge University Press:  01 November 2005

DON M. TUCKER ,
PHAN LUU  and
DOUGLAS DERRYBERRY
DON M. TUCKER
Affiliation:
Electrical Geodesics, Inc., University of Oregon
PHAN LUU
Affiliation:
Electrical Geodesics, Inc., University of Oregon
DOUGLAS DERRYBERRY
Affiliation:
Oregon State University
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Abstract

Empathic concern for others is an essential motive for challenges of self-regulation at all developmental stages. A child who never develops the capacity for empathic concern may become an ineffective parent, such that developmental psychopathology propagates across generations. We draw on evidence and theory by Panksepp and associates that indicates that infant–mother bonding is mediated by opiate mechanisms. We review the neural systems of pain perception and find these are closely aligned with those for attentional and cognitive self-regulation. Analysis of the limbic and neocortical representations for interpersonal reasoning suggests there are important contributions from visceral, affective, and somatic and cognitive levels. We draw on modern learning theory to propose a critical role for frustration training in development to allow the child to achieve the capacity for tolerating psychological pain that allows effective empathic concern in later relationships.

Type
Research Article
Information
Development and Psychopathology , Volume 17 , Issue 3 , September 2005 , pp. 699 - 713
Copyright
© 2005 Cambridge University Press

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References

REFERENCES

Albe–Fessard, D., Berkley, K. J., Kruger, L., Ralston, H. J., & Willis, W. D. (1985). Diencephalic mechanisms of pain sensation. Brain Research Reviews 9, 217–296.Google Scholar
Amsel, A., & Stanton, M. (1980). Ontogeny and phylogeny of paradoxical reward effects. Advances in the Study of Behavior 11, 227–274.Google Scholar
Baldwin, D. A. (1993). Infants' ability to consult the speaker for clues to word reference. Journal of Child Language 20, 395–418.Google Scholar
Barr, C. S., Newman, T. K., Lindell, S., Shannon, C., Champoux, M., & Lesch, K. P. (2004). Interaction between serotonin transporter gene variation and rearing condition in alcohol preference and consumption in female primates. Archives of General Psychiatry 61, 1146–1152.Google Scholar
Barr, C. S., Newman, T. K., Schwandt, M., Shannon, C., Dvoskin, R. L., & Lindell, S. G. (2004). Sexual dichotomy of an interaction between early adversity and the serotonin transporter gene promoter variant in rhesus macaques. Proceedings of the National Academy of Science of the United States of America 101, 12358–12363.Google Scholar
Cicchetti, D., & Tucker, D. M. (1994). Development of self-regulatory structures of the mind. Development and Psychopathology 6, 533–549.Google Scholar
Decety, J., & Jackson, P. L. (2004). The functional architecture of human empathy. Behavioral & Cognitive Neuroscience Review 3, 71–100.Google Scholar
Dehaene, S., Posner, M. I., & Tucker, D. M. (1994). Localization of a neural system for error detection and compensation. Psychological Science 5, 303–305.Google Scholar
Derbyshire, S. W. G., Jones, A. K. P., Devani, P., Friston, K. J., Feinmann, C., & Harris, M. (1994). Cerebral responses to pain in patients with atypical facial pain measured by positron emission tomography. Journal of Neurology, Neurosurgery, and Psychiatry 57, 1166–1172.Google Scholar
Derryberry, D., & Tucker, D. M. (1991). The adaptive base of the neural hierarchy: Elementary motivational controls of network function. In A. Dienstbier (Ed.), Nebraska Symposium on Motivation (pp. 289–342). Lincoln, NE: University of Nebraska Press.
Frith, U., & Frith, C. D. (2001). The biological basis of social interaction. Current Directions in Psychological Science 10, 151–155.Google Scholar
Gabriel, M., Burhans, L., Talk, A., & Scalf, P. (2002). Cingulate cortex. In V. S. Ramachandran (Ed.), Encyclopedia of the human brain (pp. 775–791). New York: Elsevier Science.
Guze, S. B., Woodruff, R. A., & Clayton, P. J. (1971). Hysteria and antisocial behavior: Further evidence of an association. American Journal of Psychiatry 127, 133–136.Google Scholar
Haertzen, C. A., & Hooks, N. T. (1969). Changes in personality and subjective experience associated with the chronic administration and withdrawal of opiates. Journal of Nervous and Mental Disease 148, 606–614.Google Scholar
Harlow, H. F. (1986). In C. M. Harlow (Ed.), From learning to love: The selected papers of H. F. Harlow. New York: Praeger.
Herrick, C. J. (1948). The brain of the tiger salamander. Chicago: University of Chicago Press.
Hoffman, M. L. (1984). Interaction of affect and cognition in empathy. In C. E. Izard, J. Kagan, & R. B. Zajonc (Eds.), Emotions, cognition, and behavior (pp. 103–131). Cambridge: Cambridge University Press.
Holroyd, C. B., Dien, J., & Coles, M. G. H. (1998). Error-related scalp potentials elicited by hand and foot movements: Evidence for an output-independent error-processing system in humans. Neuroscience Letters 242, 65–68.Google Scholar
Hutchison, W. D., Davis, K. D., Lozano, A. M., Tasker, R. R., & Dostrovsky, J. O. (1999). Pain-related neurons in the human cingulate cortex. Nature Neuroscience 2, 403–405.Google Scholar
Jones, A. K. P., Qi, L. Y., Fujirawa, T., Luthar, S. K., Asburner, J., & Bloomfield, P. (1991). In vivo distribution of opioid receptors in relation to the cortical projections of the medial and lateral pain systems measured with positron emission tomography. Neuroscience Letters 126, 25–28.Google Scholar
Jones, E. G., & Leavitt, R. Y. (1974). Retrograde axonal transport and the demonstration of non-specific projections to the cerebral cortex and striatum from thalamic intralaminar nuclei in the rat, cat and monkey. Journal of Comparative Neurology 154, 349–378.Google Scholar
Jürgens, U. (1979). Neural control of vocalization in non human primates. In H. D. Steklis & M. J. Raleigh (Eds.), Neurobiology of social communication in primates (pp. 11–44). New York: Academic Press.
Jürgens, U., & Ploog, D. (1970). Cerebral representation of vocalization in the squirrel monkey. Experimental Brain Research 10, 532–554.Google Scholar
Jürgens, U., & Pratt, R. (1979). Role of the periaqueductal grey in vocal expression of emotion. Brain Research 167, 367–378.Google Scholar
Keysers, C., & Perrett, D. I. (2004). Demystifying social cognition: A hebbian perspective. Trends in Cognitive Science 8, 501–507.Google Scholar
Luu, P., Collins, P., & Tucker, D. M. (2000). Mood, personality, and self-monitoring: Negative affect and emotionality in relation to frontal lobe mechanisms of error monitoring. Journal of Experimental Psychology: General 129, 43–60.Google Scholar
Luu, P., & Tucker, D. M. (2003). Self-regulation and the executive functions: Electrophysiological clues. In A. Zani & A. M. Preverbio (Eds.), The cognitive electrophysiology of mind and brain (pp. 199–223). San Diego, CA: Academic Press.
MacLean, P. (1987). The midline frontolimbic cortex and the evolution of crying and laughter. In E. Perecman (Ed.), The frontal lobes revisited. New York: IRBN Press.
McEwen, B. S. (2000). The neurobiology of stress: From serendipity to clinical relevance. Brain Research 886, 172–189.Google Scholar
Moses, L. J., Baldwin, D. A., Rosicky, J. G., & Tidball, G. (2001). Evidence for referential understanding in the emotions domain at twelve and eighteen months. Child Development 72, 718–735.Google Scholar
Pandya, D. N., & Yeterian, E. H. (1990). Prefrontal cortex in relation to other cortical areas in rhesus monkey: Architecture and connections. Progress in Brain Research 85, 63–94.Google Scholar
Panksepp, J. (2003a). At the interface of the affective, behavioral, and cognitive neurosciences: Decoding the emotional feelings of the brain. Brain and Cognition 52, 4–14.Google Scholar
Panksepp, J. (2003b). Neuroscience. Feeling the pain of social loss. Science 302, 237–239.Google Scholar
Papini, M. R. (2002). Pattern and process in the evolution of learning. Psychology Review 109, 186–201.Google Scholar
Papini, M. R. (2003). Comparative psychology of surprising nonreward. Brain, Behavior and Evolution 62, 83–95.Google Scholar
Ploog, D. W. (1992). Neuroethological perspectives on the human brain: From the expression of emotions to intentional signing and speech. In A. Harrington (Ed.), So human a brain: Knowledge and values in the neurosciences (pp. 3–13). Boston: Birkhauser.
Posner, M. I., & Rothbart, M. K. (1991). Attentional mechanisms and conscious experience. In The neuropsychology of consciousness (pp. 91–111): New York: Academic Press.
Rainville, P., Duncan, G. H., Price, D. D., Carrier, B., & Bushnell, C. M. (1997). Pain affect encoded in human anterior cingulate but not somatosensory cortex. Science 277, 968–971.Google Scholar
Rivers, W. H. R., & Head, H. (1908). A human experiment in nerve division. Brain 31, 323–450.Google Scholar
Rizzolatti, G., & Fadiga, L. (1998). Grasping objects and grasping action meanings: The dual role of monkey rostroventral premotor cortex (area f5). Novartis Foundation Symposium 218, 81–95.Google Scholar
Roth, A. S., Ostroff, R. B., & Hoffman, R. E. (1996). Naltrexone as a treatment for repetitive self-injurious behavior: An open-lable trial. Journal of Clinical Psychiatry 57, 233–237.Google Scholar
Schore, A. N. (1994). Affect regulation and the origin of the self: The neurobiology of emotional development. Hillsdale, NJ: Erlbaum.
Stern, D. N. (1985). The interpersonal world of the infant: A view from psychoanalysis and developmental psychology. New York: Basic Books.
Suomi, S. J. (2003). Gene–environment interactions and the neurobiology of social conflict. Annals of the New York Academy of Science 1008, 132–139.Google Scholar
Taylor, M. (1999). Imaginary companions and the children who create them. New York: Oxford University Press.
Trevarthen, C., & Aitken, K. J. (1995). Brain development, infant communication and empathy disorders: Intrinsic factors in child mental health. Development and Psychopathology 6, 597–633.Google Scholar
Tucker, D. M. (2001). Motivated anatomy: A core-and-shell model of corticolimbic architecture. In G. Gainotti (Ed.), Handbook of neuropsychology: Vol. 5. Emotional behavior and its disorders (2nd ed., pp. 125–160). Amsterdam: Elsevier.
van Schie, H. T., Mars, R. B., Coles, M. G. H., & Bekkering, H. (2004). Modulation of activity in the medial frontal and motor cortices during error observation. Nature Neuroscience 7, 549–554.Google Scholar
Vogt, B. A., & Barbas, H. (1986). Structure and connections of the cingulate vocalization region in the rhesus monkey. In J. D. Newman (Ed.), The physiological control of mammalian vocalization (pp. 203–225). New York: Plenum Press.
Vogt, B. A., & Pandya, D. N. (1987). Cingulate cortex of the rhesus monkey: Ii. Cortical afferents. The Journal of Comparative Neurology 262, 271–289.Google Scholar
Vogt, B. A., Sikes, R. W., & Vogt, L. J. (1993). Anterior cingulate cortex and the medial pain system. In B. A. Vogt & M. Gabriel (Eds.), Neurobiology of the cingulate cortex and limbic thalamus (pp. 314–344). Boston: Birkhauser.
Wamsley, J. K., Zarbin, M. A., Young, W. S., & Kuhar, M. J. (1982). Distribution of opiate receptors in the monkey brain: An autoradiographic study. Neuroscience 3, 595–613.Google Scholar
Werner, H. (1957). The comparative psychology of mental development. New York: Harper.