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4 - An Integrative Approach to the Neurophysiology of Emotion Regulation: The Case of Social Withdrawal

Published online by Cambridge University Press:  02 July 2009

Sheryl L. Olson
Affiliation:
University of Michigan, Ann Arbor
Arnold J. Sameroff
Affiliation:
University of Michigan, Ann Arbor
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Summary

The concept of emotion regulation as a psychological construct has become an issue of significant scientific debate during the last decade (see Cole, Martin, & Dennis, 2004). Recent conceptualizations of emotion regulation have ranged from “changes associated with activated emotions” (Cole et al., 2004. p. 320) to emotion regulation as embedded in emotion or as an integrated component of emotional processes, including the generation, manifestation, and termination of the emotional experience (Campos, Frankel, & Camras, 2004). Because of the integrative nature of the physiological processes involved in the perception, processing, and reaction to emotional stimuli,we agree with Campos et al.'s (2004) working definition of emotion regulation. We view emotion regulation as a chain of neurocognitive processes that modulate the activation, intensity, duration, quality, and expression of emotional experience. At their most basic form, these processes are in charge of the processing of emotional stimuli and the subsequent regulation of arousal (Bradley, 2000).

Although theorists have called for a “process” model of emotion regulation (Campos et al., 2004), empirical validation of this model has been limited. One barrier to progress has been the lack of well-articulated processes involved in emotion regulation and of cohesive theoretical formulations that account for the highly interconnected nature of these processes. One example of this process model can be observed in children's reactions to fear-inducing stimuli. In our laboratory, we perform a brief fear-inducing task during which children are exposed to a realistic rubber snake. The reaction to such stimuli varies significantly.

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References

Adolphs, R., Tranel, D., Hamann, S., Young, A. W., Calder, A. J., Phelps, E. A., et al. (1999). Recognition of facial emotion in nine individuals with bilateral amygdala damage. Neuropsychologia, 37(10), 1111–1117.CrossRefGoogle ScholarPubMed
Afifi, A., & Bergman, R. (1998). Functional neuroanatomy. New York: McGraw-Hill.Google Scholar
Aggleton, J. P., & Passingham, R. E. (1981). Syndrome produced by lesions of the amygdala in monkeys (Macaca mulatta). Journal of Comparative & Physiological Psychology, 95(6), 961–977.CrossRefGoogle Scholar
Amaral, D. G. (2002). The primate amygdala and the neurobiology of social behavior: Implications for understanding social anxiety. Biological Psychiatry, 51(1), 11–17.CrossRefGoogle ScholarPubMed
Amaral, D. G. (2003). The amygdala, social behavior, and danger detection. Ann. N.Y. Acad. Sci. 1000, 337–347.CrossRefGoogle ScholarPubMed
Anisman, H., Zaharia, M. D., Meaney, M. J., & Merali, Z. (1998). Do early-life events permanently alter behavioral and hormonal responses to stressors? [Special issue]. International Journal of Developmental Neuroscience, 16(3–4), 149–164.CrossRefGoogle Scholar
Bechara, A., Tranel, D., Damasio, H., & Damasio, A. R. (1996). Failure to respond autonomically to anticipated future outcomes following damage to prefrontal cortex. Cerebral Cortex, 6(2), 215–225.CrossRefGoogle ScholarPubMed
Boucsein, K., Weniger, G., Mursch, K., Steinhoff, B. J., & Irle, E. (2001). Amygdala lesion in temporal lobe epilepsy subjects impairs associative learning of emotional facial expressions. Neuropsychologia, 39(3), 231–236.CrossRefGoogle ScholarPubMed
Bradley, S. J. (2000). Affect regulation and the development of psychopathology. New York: Guilford Press.Google Scholar
Calder, A. J., Young, A. W., Rowland, D., Perrett, D. I., Hodges, J. R., & Etcoff, N. L. (1996). Facial emotion recognition after bilateral amygdala damage: Differentially severe impairment of fear. Cognitive Neuropsychology, 13(5), 699–745.CrossRefGoogle Scholar
Caldji, C., Francis, D., Sharma, S., Plotsky, P. M., & Meaney, M. J. (2000). The effects of early rearing environment on the development of GABA-sub(A) and central benzodiazepine receptor levels and novelty-induced fearfulness in the rat. Neuropsychopharmacology, 22(3), 219–229.CrossRefGoogle Scholar
Campos, J. J., Frankel, C. B., & Camras, L. (2004). On the nature of emotion regulation. Child Development, 75(2), 377–394.CrossRefGoogle ScholarPubMed
Checkley, S. (1996). The neuroendocrinology of depression. International Review of Psychiatry, 8(4), 373–378.CrossRefGoogle Scholar
Cicchetti, D., & Rogosch, F. A. (2001a). Diverse patterns of neuroendocrine activity in maltreated children [Special issue]. Development & Psychopathology, 13(3), 677–693.CrossRefGoogle Scholar
Cicchetti, D., & Rogosch, F. A. (2001b). The impact of child maltreatment and psychopathology on neuroendocrine functioning. Development & Psychopathology, 13(4), 783–804.Google ScholarPubMed
Cole, P. M., Martin, S. E., & Dennis, T. A. (2004). Emotion regulation as a scientific construct: Methodological challenges and directions for child development research. Child Development, 75(2), 317–333.CrossRefGoogle ScholarPubMed
Davidson, R. J. (1993). Cerebral asymmetry and emotion: Conceptual and methodological conundrums. Cognition and Emotion, 7, 115–138.CrossRefGoogle Scholar
Davidson, R. J., & Fox, N. A. (1989). Frontal brain asymmetry predicts infant's response to maternal separation. Journal of Abnormal Psychology, 98, 127–131.CrossRefGoogle Scholar
Davidson, R. J., Ekman, P., Saron, C. D., Senulis, J. A., & Friesen, W. V. (1990). Approach withdrawal and cerebral asymmetry: Emotional expression and brain physiology: I. Journal of Personality & Social Psychology, 58(2), 330–341.CrossRefGoogle Scholar
Davidson, R. J., & Irwin, W. (1999). The functional neuroanatomy of emotion and affective style. Trends in Cognitive Neurosciences, 3, 11–21.CrossRefGoogle ScholarPubMed
Davidson, R. J., Jackson, D. C., & Kalin, N. H. (2000). Emotion, plasticity, context, and regulation: Perspectives from affective neuroscience [Special issue]. Psychological Bulletin, 126(6), 890–909.CrossRefGoogle Scholar
Davis, E. P., Donzella, B., Krueger, W. K., & Gunnar, M. R. (1999). The start of a new school year: Individual differences in salivary cortisol response in relation to child temperament. Developmental Psychobiology, 35(3), 188–196.3.0.CO;2-K>CrossRefGoogle ScholarPubMed
Haan, M., Gunnar, M. R., Tout, K., Hart, J., & Stansbury, K. (1998). Familiar and novel contexts yield different associations between cortisol and behavior among 2-year-old children. Developmental Psychobiology, 33(1), 93–101.3.0.CO;2-N>CrossRefGoogle ScholarPubMed
Kloet, E. R. (1991). Brain corticosteroid receptor balance and homeostatic control. Frontiers in Neuroendocrinology, 12, 95–164.Google Scholar
Dettling, A. C., Gunnar, M. R., & Donzella, B. (1999). Cortisol levels of young children in full-day childcare centers: Relations with age and temperament. Psychoneuroendocrinology, 24, 519–536.CrossRefGoogle ScholarPubMed
Donzella, B. G., Gunnar, M. R., Krueger, W. K., & Alwin, J. (2000). Cortisol and vagal tone responses to competitive challenge in preschoolers: Associations with temperament. Developmental Psychobiology, 37(4), 209–220.3.0.CO;2-S>CrossRefGoogle ScholarPubMed
Feldman, S., Conforti, N., & Siegel, R. A. (1982). Adrenocortical responses following limbic stimulation in rats with hypothalamic deafferentations. Neuroendocrinology, 35, 205–211.CrossRefGoogle ScholarPubMed
Feldman, S., Conforti, N., & Weidenfeld, J. (1995). Limbic pathways and hypothalamic neurotransmitters mediating adrenocortical responses to neural stimuli. Neuroscience & Biobehavioral Reviews, 19(2), 235–240.CrossRefGoogle ScholarPubMed
Fox, N. A. (1994). Dynamic cerebral processes underlying emotion regulation. Monographs of the Society for Research in Child Development, 59(2–3), 250–283.CrossRefGoogle ScholarPubMed
Fox, N. A., Bell, M. A., & Jones, N. A. (1992). Individual differences in response to stress and cerebral asymmetry. Developmental Neuropsychology, 8(2–3), 161–184.CrossRefGoogle Scholar
Fox, N. A., Calkins, S. D., & Bell, M. A. (1994). Neural plasticity and development in the first two years of life: Evidence from cognitive and socioemotional domains of research [Special issue]. Development & Psychopathology, 6(4), 677–696.CrossRefGoogle Scholar
Fox, N. A., Rubin, K. H., Calkins, S. D., Marshall, T. R., Coplan, R. J., Porges, S. W., et al. (1995). Frontal activation asymmetry and social competence at four years of age. Child Development, 66(6), 1770–1784.CrossRefGoogle ScholarPubMed
Fox, N. A., Schmidt, L. A., Calkins, S. D., & Rubin, K.H., et al. (1996). The role of frontal activation in the regulation and dysregulation of social behavior during the preschool years. Development & Psychopathology, 8(1), 89–102.CrossRefGoogle Scholar
Gainotti, G. (1972). Emotional behavior and hemispheric side of the lesion. Cortex, 8(1), 41–55.CrossRefGoogle ScholarPubMed
Gerra, G., Avanzini, P., Zaimovic, A., Sartori, R., Bocchi, C., Timpano, M., et al. (1999). Neurotransmitters, neuroendocrine correlates of sensation-seeking temperament in normal humans. Neuropsychobiology, 39(4), 207–213.CrossRefGoogle ScholarPubMed
Gerra, G., Zaimovic, A., Avanzini, P., Chittolini, B., Guicastro, G., Caccavari, R., et al. (1997). Neurotransmitter-neuroendocrine responses to experimentally induced aggression in humans: Influence of personality variable. Psychiatry Research, 66(1), 33–43.CrossRefGoogle ScholarPubMed
Gerra, G., Zaimovic, A., Timpano, M., Zambelli, U., Delsignore, R., & Brambilla, F. (2000). Neuroendocrine correlates of temperamental traits in humans. Psychoneuroendocrinology, 25(5), 479–496.CrossRefGoogle ScholarPubMed
Gewirtz, J. C., Falls, W. A., & Davis, M. (1997). Normal conditioning inhibition and extinction of freezing and fear-potentiated startle following electrolytic lesions of medial prefrontal cortex in rats. Behavioral Neuroscience, 111(4), 712–726.CrossRefGoogle ScholarPubMed
Gladue, B. A. (1991). Aggressive behavioral characteristics, hormones, and sexual orientation in men and women. Aggressive Behavior, 17(6), 313–326.3.0.CO;2-Z>CrossRefGoogle Scholar
Goldstein, L. E., Rasmusson, A. M., Bunney, B. S., & Roth, R. H. (1996). Role of the amygdala in the coordination of behavioral, neuroendocrine, and prefrontal cortical monoamine responses to psychological stress in the rat. Journal of Neuroscience, 16(15), 4787–4797.CrossRefGoogle ScholarPubMed
Guerra, N. G., Nucci, L., & Huesmann, L. R. (1994). Moral cognition and childhood aggression. In Huesmann, L. R. (Ed.), Aggressive behavior: Current perspectives (pp. 13–33). New York: Plenum Press.CrossRefGoogle Scholar
Gunnar, M. R. (1994). Psychoendocrine studies of temperament and stress in early childhood: Expanding current models. In Bates, J. E. & Wachs, T. D. (Eds.), Temperament (pp. 175-198). Washington, DC: American Psychological Association.Google Scholar
Gunnar, M. R. (2001). The role of glucocorticoids in anxiety disorders: A critical analysis. In Vasey, M. W. & Dadds, M. (Eds.), The developmental psychopathology of anxiety (pp. 143–159). New York: Oxford University Press.CrossRefGoogle Scholar
Gunnar, M. R., Tout, K., Haan, M., Pierce, S., & Stansbury, K. (1997). Temperament, social competence, and adrenocortical activity in preschoolers. Developmental Psychobiology, 31(1), 65–85.3.0.CO;2-S>CrossRefGoogle ScholarPubMed
Hamann, S. B., & Adolphs, R. (1999). Normal recognition of emotional similarity between facial expressions following bilateral amygdala damage. Neuropsychologia, 37(10), 1135–1141.CrossRefGoogle ScholarPubMed
Heim, C., Ehlert, U., & Hellhammer, D. H. (2000). The potential role of hypocortisolism in the pathophysiology of stress-related bodily disorders. Psychoneuroendocrinology, 25(1), 1–35.CrossRefGoogle ScholarPubMed
Heim, C., Newport, D. J., Bonsall, R., Miller, A. H., & Nemeroff, C. B. (2001). Altered pituitary-adrenal axis responses to provocative challenge tests in adult survivors of childhood abuse [Special issue]. American Journal of Psychiatry, 158(4), 575–581.CrossRefGoogle Scholar
Heim, C., Newport, D. J., Heit, S., Graham, Y. P., Wilcox, M., Bonsall, R., et al. (2000). Pituitary-adrenal and autonomic responses to stress in women after sexual and physical abuse in childhood. Journal of the American Medical Association, 284(5), 592–597.CrossRefGoogle ScholarPubMed
Heuser, I., Deuschle, M., Weber, B., Stalla, G. K., & Holsboer, F. (2000). Increased activity of the hypothalamus-pituitary-adrenal system after treatment with mineralocorticoid receptor antagonist spironolactone. Psychoneuroendocrinology, 25(5), 513–518.CrossRefGoogle ScholarPubMed
Huot, R. L., Thrivikraman, K. V., Meaney, M. J., & Plotsky, P. M. (2001). Development of adult ethanol preference and anxiety as a consequence of neonatal maternal separation in Long Evans rats and reversal with antidepressant treatment. Psychopharmacology, 158(4), 366–373.CrossRefGoogle ScholarPubMed
Johnson, E. O., Kamilaris, T. C., Chrousos, G. P., & Gold, P. W. (1992). Mechanisms of stress: A dynamic overview of hormonal and behavioral homeostasis. Neuroscience & Biobehavioral Reviews, 16(2), 115–130.CrossRefGoogle ScholarPubMed
Kabbaj, M., Devine, D. P., Savage, V. R., & Akil, H. (2000). Neurobiological correlates of individual differences in novelty-seeking behavior in the rat: Differential expression of stress-related molecules [Special issue]. Journal of Neuroscience, 20(18), 6983–6988.CrossRefGoogle Scholar
Kabbaj, M., Piazza, P., Moal, M., & Maccari, S. (1996). Individual differences in the noradrenergic regulation of hippocampal corticosteroid receptors. Society for Neuroscience Abstracts, 22, 18.Google Scholar
Kagan, J. (1989). Temperamental contributions to social behavior. American Psychologist, 44(4), 668–674.CrossRefGoogle Scholar
Kagan, J. (1994). On the nature of emotion. Monographs of the Society for Research in Child Development, 59(2–3), 250–283.CrossRefGoogle ScholarPubMed
Kagan, J., Reznick, J. S., & Snidman, N. (1988). The physiology and psychology of behavioral inhibition in children. Annual Progress in Child Psychiatry and Child Development, 8(686), 102–127.Google Scholar
Kagan, J., Reznick, J. S., Snidman, N., & Gibbons, J. (1988). Childhood derivatives of inhibition and lack of inhibition to the unfamiliar. Child Development, 59(6), 1580–1589.CrossRefGoogle ScholarPubMed
Kalin, N. H., Larson, C., Shelton, S. E., & Davidson, R. J. (1998). Asymmetric frontal brain activity, cortisol, and behavior associated with fearful temperament in rhesus monkeys. Behavioral Neuroscience, 112(2), 286–292.CrossRefGoogle ScholarPubMed
Kalin, N. H., Shelton, S. E., Davidson, R. J., & Kelley, A. E. (2001). The primate amygdala mediates acute fear but not the behavioral and physiological components of anxious temperament [Special issue]. Journal of Neuroscience, 21(6), 2067–2074.CrossRefGoogle Scholar
Kolb, B., Gibb, R., & Gorny, G. (2001). Cortical plasticity and the development of behavior after early frontal cortical injury [Special issue]. Developmental Neuropsychology, 18(3), 423–444.CrossRefGoogle Scholar
Maccari, S., Piazza, P. V., Deminiere, J. M., & Angelucci, L. (1991). Hippocampal Type I and Type II corticosteroid receptor affinities are reduced in rats predisposed to develop amphetamine self-administration. Brain Research, 548(1–2), 305–309.CrossRefGoogle ScholarPubMed
McBurnett, K., Lahey, B. B., Frick, P. J., Risch, C., Loeber, R., Hart, E. L., et al. (1991). Anxiety, inhibition, and conduct disorder in children: II. Relation to salivary cortisol. Journal of the American Academy of Child & Adolescent Psychiatry, 30(2), 192–196.CrossRefGoogle ScholarPubMed
Meaney, M. J. (1985a). Early postnatal handling alters glucocorticoid receptor concentrations in selected brain regions. Behavioral Neuroscience, 99(4), 765–770.CrossRefGoogle ScholarPubMed
Meaney, M. J. (1985b). The effects of postnatal handling on the development of the glucocorticoid receptor systems and stress recovery in the rat. Progress in Neuro-Psychopharmacology & Biological Psychiatry, 9(5–6), 731–734.CrossRefGoogle ScholarPubMed
Meaney, M. J., & Stewart, J. (1981). A descriptive study of social development in the rat (Rattus norvegicus). Animal Behaviour, 29(1), 34–45.CrossRefGoogle Scholar
Morgan, M. A., Romanski, L. M., & LeDoux, J. E. (1993). Extinction of emotional learning: Contribution of medial prefrontal cortex. Neuroscience Letters, 163(1), 109–113.CrossRefGoogle ScholarPubMed
Morris, J. S., Frith, C. D., Perrett, D. I., Rowland, D., Young, A. W., Calder, A. J., et al. (1996). A differential neural response in the human amygdala to fearful and happy facial expressions. Nature, 383(6603), 812–815.CrossRefGoogle ScholarPubMed
Morris, P. L. P., Robinson, R. G., Raphael, B., & Hopwood, M. J. (1996). Lesion location and poststroke depression. Journal of Neuropsychiatry & Clinical Neurosciences, 8(4), 399–403.Google ScholarPubMed
Oitzl, M. S., Haarst, A. D., & Kloet, E. R. (1997). Behavioral and neuroendocrine responses controlled by the concerted action of central mineralocorticoid (MRs) and glucocorticoid receptors (GRs) [Special issue]. Psychoneuroendocrinology, 22(1), s87–s93.CrossRefGoogle Scholar
Phillips, M. L., Young, A. W., Senior, C., Brammer, M., Andrews, C., Calder, A. J., et al. (1997). A specific neural substrate for perceiving facial expressions of disgust. Nature, 389(6650), 495–498.CrossRefGoogle ScholarPubMed
Piazza, P. V., Deroche, V., Deminiere, J. M., Maccari, S., Moal, M., & Simon, H. (1993). Cortiscosterone in the range of stress induced levels possess reinforcing properties: Implications for sensation seeking behaviors. Proceedings of the National Academy of Sciences, 90, 11738–11742.CrossRefGoogle Scholar
Rauch, S. L., Kolk, B. A., Fisler, R. E., & Alpert, N. M. (1996). A symptom provocation study of posttraumatic stress disorder using positron emission tomography and script-driven imagery. Archives of General Psychiatry, 53(5), 380–387.CrossRefGoogle ScholarPubMed
Robinson, J. L., Kagan, J., Reznick, J. S., & Corley, R. (1992). The heritability of inhibited and uninhibited behavior: A twin study. Developmental Psychology, 28(6), 1030–1037.CrossRefGoogle Scholar
Rosen, J. B., Hamerman, E., Sitcoske, M., Glowa, J. R., & Schulkin, J. (1996). Hyperexcitability: Exaggerated fear-potentiated startle produced by partial amygdala kindling. Behavioral Neuroscience, 110(1), 43–50.CrossRefGoogle ScholarPubMed
Rubin, K. H., Coplan, R. J., Fox, N. A., & Calkins, S. D. (1995). Emotionality, emotion regulation, and preschoolers' social adaptation [Special issue]. Development & Psychopathology, 7(1), 49–62.CrossRefGoogle Scholar
Schmidt, L. A., Fox, N. A., Rubin, K. H., & Sternberg, E. M. (1997). Behavioral and neuroendocrine responses in shy children. Developmental Psychobiology, 30(2), 127–140.3.0.CO;2-S>CrossRefGoogle ScholarPubMed
Schmidt, L. A., Fox, N. A., Schulkin, J., & Gold, P. W. (1999). Behavioral and psychophysiological correlates of self-presentation in temperamentally shy children. Developmental Psychobiology, 35(2), 119–135.3.0.CO;2-G>CrossRefGoogle ScholarPubMed
Schmidt, L. A., Fox, N. A., Sternberg, E. M., Gold, P. W., Smith, C. C., & Schulkin, J. (1999). Adrenocortical reactivity and social competence in seven-year-olds. Personality & Individual Differences, 26(6), 977–985.CrossRefGoogle Scholar
Scott, S. K., Young, A. W., Calder, A. J., Hellawell, D. J., Agglenton, J. P., & Johnsons, M. (1997). Impaired auditory recognition of fear and anger following bilateral amygdala lesions. Nature, 385, 254–257.CrossRefGoogle ScholarPubMed
Strohle, A., Poettig, M., Barden, N., Holsboer, F., & Montkowski, A. (1998). Age and stimulus-dependent changes in anxiety-related behavior of transgenic mice with GR dysfunction. NeuroReport, 9, 2099–2102.CrossRefGoogle ScholarPubMed
Tennes, K., Downey, K., & Vernadakis, A. (1997). Urinary cortisol excretion rates and anxiety in normal 1-year-old infants. Psychosomatic Medicine, 39(3), 178–187.CrossRefGoogle Scholar
Tobin, J. P. (2001). Posttraumatic stress disorder and the adrenal gland. Irish Journal of Psychological Medicine, 18(1), 27–29.CrossRefGoogle Scholar
Kar, L., Piechowski, R. A., Rittenhouse, P. A., & Gray, T. S. (1991). Amygdaloid lesions: Differential effect on conditioned stress and immobilization-induced increases in corticosterone and renin secretion. Neuroendocrinology, 54, 89–95.Google ScholarPubMed
Vazquez, D. M. (1998). Stress and the developing limbic-hypothalamic-pituitary-adrenal axis. Psychoneuroendocrinology, 23(7), 663–700.CrossRefGoogle ScholarPubMed
ver Ellen, P., & Kammen, D. P. (1990). The biological findings in post-traumatic stress disorder: A review [Special issue]. Journal of Applied Social Psychology, 20(21), 1789–1821.CrossRefGoogle Scholar
Wittling, W. G. S., & Genzel, S. (1995). Brain asymmetries in cerebral regulation of cortisol secretion. Homeostasis in Health & Disease, 36(1), 1–5.Google Scholar

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