Psychoendocrine Responses of Mother and Infant Monkeys to Disturbance and Separation

  • Christopher L. Coe
  • Sandra G. Wiener
  • Seymour Levine


In mammalian and avian species, it is essential that the young maintain at least periodic contact with their mother in order to obtain nurturance and warmth. This contact is ensured through the development of emotional dependency or attachment, as well as by the complementary distress reaction that occurs following sudden or forced separation of mother and infant. During the last several years, our laboratory has investigated this response as a way of evaluating how mother and infant primates cope with stressful situations. This research not only has generated new information on the nature of attachment processes in nonhuman primates but has also provided a unique way of determining how young organisms cope with stress. In addition to demonstrating that social relationships are important in the mediation of stress and coping, we have found that the concepts developed in the stress literature have a surprising degree of applicability to an understanding of the dynamics of mother-infant relationships.


Cortisol Level Rhesus Monkey Home Cage Squirrel Monkey Plasma Cortisol Level 
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  1. Abbott, D. H., & Hearn, J. P. Physical, hormonal and behavioral aspects of sexual development in the marmoset monkey, Callithrix jacchus. Journal of Reproduction and Fertility, 1978, 53, 155–166.CrossRefGoogle Scholar
  2. Anderson, C. O., & Mason, W. A. Early experience and complexity of social organization in groups of young rhesus macaques (Macaca mulatto.). Journal of Comparative Physiology and Psychology, 1974, 87, 681–690.CrossRefGoogle Scholar
  3. Badia, P., Harsh, J., & Abbott, B. Choosing between predictable and unpredictable shock conditions: Data and theory. Psychological Bulletin, 1979, 86, 1107–1131.CrossRefGoogle Scholar
  4. Bowlby, J. Attachment and loss: Attachment. New York: Basic Books, 1969.Google Scholar
  5. Coe, C. L., & Levine, S. Normal responses to mother-infant separation in nonhuman primates. In D. F. Klein & J. Rabkin (Eds.), Anxiety: New research and changing concepts. New York: Raven Press, 1981, pp. 155–177.Google Scholar
  6. Coe, C. L., Mendoza, S. P., Smotherman, W. P., & Levine, S. Mother-infant attachment in the squirrel monkey: Adrenal response to separation. Behavioral Biology, 1978, 22, 256–263.PubMedCrossRefGoogle Scholar
  7. Dixson, A. F., Martin, R. D., Bonney, R. C., & Fleming, D. Reproductive biology of the owl monkey, Aotus frivirgatus griseimembra. In T. C. Anand Kumar (Ed.), Non-human primate models for study of human reproduction. Basel: Karger, 1980, pp. 61–68.Google Scholar
  8. Dolhinow, P. An experimental study of mother loss in the Indian langur monkey (Presbytis entellus). Folia Primatologica, 1980, 33, 77–128.CrossRefGoogle Scholar
  9. Gliner, J. A. Predictable vs. unpredictable shock: Preference behavior and stomach ulceration. Physiology and Behavior, 1912, 9, 693–698.CrossRefGoogle Scholar
  10. Gluck, J. P. The intellectual consequences of early social restriction in rhesus monkeys (Macaca mulatta). In G. C. Ruppenthal & D. T. Reese (Eds.), Nursery care of nonhuman primates. New York: Plenum Press, 1979, pp. 253–268.Google Scholar
  11. Gunnar, M. R., Gonzalez, C. A., Goodlin, B. L., & Levine, S. Behavioral and pituitary-adrenal responses during a prolonged separation period in infant rhesus macaques. Psychoneuroendocrinology, 1981, 6, 65–75.PubMedCrossRefGoogle Scholar
  12. Harlow, H. F. Age-mate or peer affectional systems. Advances in the Study of Behavior, 1969, 2, 333–383.CrossRefGoogle Scholar
  13. Harlow, H. F., & Harlow, M. K. Effects of various mother-infant relationships on rhesus monkey behaviors. In B. M. Foss (Ed.), Determinants of infant behaviour (Vol. 4). London: Methuen, 1969, pp. 15–36.Google Scholar
  14. Harlow, H. F., & Zimmerman, R. R. Affectional responses in the infant monkey. Science, 1959, 130, 421–432.PubMedCrossRefGoogle Scholar
  15. Hennessy, J. W., & Levine, S. Stress, arousal and the pituitary-adrenal system: A psychoneuroendocrine hypothesis. In J. Sprague & A. Epstein (Eds.), Progress in psychobiology and physiological psychology (Vol. 8). New York: Academic Press, 1979, pp. 133–178.Google Scholar
  16. Hennessy, M. B., & Kaplan, J. N. The effects of separation and novelty on the behavior and cortisol levels in surrogate-reared infant squirrel monkeys. Paper presented at the Developmental Psychobiology meetings, November 1981, New Orleans.Google Scholar
  17. Hennessy, M. B., Kaplan, J. N., Mendoza, S. P., Lowe, E. L., & Levine, S. Separation distress and attachment in surrogate-reared squirrel monkeys. Physiology and Behavior, 1979, 23, 1017–1023.PubMedCrossRefGoogle Scholar
  18. Hill, S. D., McCormack, S. A., & Mason, W. A. Effects of artificial mothers and visual experience on adrenal responsiveness of infant monkeys. Developmental Psychobiology, 1973, 6, 421–429.PubMedCrossRefGoogle Scholar
  19. Hinde, R. A., & Spencer-Booth, Y. Effects of brief separation from mother on rhesus monkeys. Science, 1971, 173, 111–118.PubMedCrossRefGoogle Scholar
  20. Hinde, R. A., Leighton-Shapiro, M., & McGinnis, L. Effects of various types of separation experience on rhesus monkeys 5 months later. Journal of Child Psychology and Psychiatry, 1978, 19, 199–211.PubMedCrossRefGoogle Scholar
  21. Hymowitz, N. Suppression of responding during signaled and unsignaled shock. Psychological Bulletin, 1979, 86, 175–190.CrossRefGoogle Scholar
  22. Jordan, T. C., Patterson, J., Coe, C. L., & Levine, S. Predictability and coping with separation in infant squirrel monkeys. Manuscript in preparation, 1983.Google Scholar
  23. Kagan, J. Discrepancy, temperament and infant distress. In M. Lewis & L. A. Rosenblum (Eds.), The origins of fear. New York: Wiley, 1974, pp. 229–248.Google Scholar
  24. Kaplan, J. Growth and development of infant squirrel monkeys during the first six months of life. In G. C. Ruppenthal & D.J. Reese (Eds.), Nursery care of nonhuman primates. New York: Plenum Press, 1979, pp. 153–164.Google Scholar
  25. Kaufman, I. C., & Rosenblum, L. A. The reaction to separation in infant monkeys: Anaclitic depression and conservation withdrawal. Psychosomatic Medicine, 1967, 29, 648–675.PubMedGoogle Scholar
  26. Lazarus, R. S. Psychological stress and the coping process. New York: McGraw-Hill, 1966.Google Scholar
  27. Levine, S., Goe, C. L.: Smotherman, W. P., & Kaplan, J. N. Prolonged cortisol elevation in the infant squirrel monkey after reunion with mother. Physiology and Behavior, 1978, 20, 7–10.PubMedCrossRefGoogle Scholar
  28. Mason, J. W. A review of psychoendocrine research on the pituitary-adrenal cortical system. Psychosomatic Medicine, 1968, 30, 576–607.PubMedGoogle Scholar
  29. Mason, W. A. Motivational factors in psychosocial development. In W. J. Arnold & M. M. Page (Eds.), Nebraska Symposium on Motivation, 1970. Lincoln: University of Nebraska Press, 1971, pp. 35–67.Google Scholar
  30. McGinnis, L. M. Maternal separation studies in children and nonhuman primates. In R. W. Bell & W. P. Smotherman (Eds.), Maternal influences and early behavior. New York: Spectrum, 1980, pp. 311–336.CrossRefGoogle Scholar
  31. Mendoza, S. P., Lowe, E. L., & Levine, S. Social organization and social behavior in two subspecies of squirrel monkeys (Saimiri sciureus). Folia Primatologica, 1978, 30, 126–144.CrossRefGoogle Scholar
  32. Mendoza, S. P., Smotherman, W. P., Miner, M. T., Kaplan, J. & Levine, S. Pituitary-adrenal response to separation in mother and infant squirrel monkeys. Developmental Psychobiology, 1978, 11, 169–175.PubMedCrossRefGoogle Scholar
  33. Mendoza, S. P., Coe, C. L., Smotherman, W. P., Kaplan, J., & Levine, S. Functional consequences of attachment: A comparison of two species. In R. W. Bell & W. P. Smotherman (Eds.), Maternal influences and early behavior, New York: Spectrum, 1980, pp. 235–252.CrossRefGoogle Scholar
  34. Miller, R. E., Caul, W. F., & Mirsky, I. A. Patterns of eating and drinking in socially-isolated rhesus monkeys. Physiology and Behavior, 1971, 7, 127–134.PubMedCrossRefGoogle Scholar
  35. Miller, R. E., Ranelli, C. J., & Levine, J. M. Nonverbal communication as an index of disturbance. In I. Hanin & E. Usdin (Eds.), Animal models in psychiatry and neurology. Oxford: Pergamon, 1977, pp. 171–180.Google Scholar
  36. Mineka, S. Depression and helplessness in primates. In H. Fitzgerald, J. Mullins, & P. Gage (Eds.), Primate behavior and child nurturance (Vol. 3). New York: Plenum Press, 1981.Google Scholar
  37. Mineka, S., & Suomi, S. J. Social separation in monkeys. Psychological Bulletin, 1978, 85, 1376–1400.PubMedCrossRefGoogle Scholar
  38. Mineka, S., Suomi, S. J., & DeLizio, R. Multiple separations in adolescent monkeys: An opponent-process interpretation. Journal of Experimental Psychology, General, 1981, 110, 56–85.CrossRefGoogle Scholar
  39. Nagle, G. A., Denari, J. H., Riarte, A., Quiroga, S., Zárate, R., Germino, N. I., Merlo, A., & Rosner, J. M. Endocrine and morphological aspects of the menstrual cycle in the cebus monkey (Cebus appela). In T. C. Anand Kumar (Ed.), Non-human primate models for study of human reproduction. Basel: Karger, 1980, pp. 69–81.Google Scholar
  40. Napier, J. R., & Napier, P. H. A handbook of living primates. New York: Academic Press, 1967.Google Scholar
  41. Natelson, B. H., Tapp, W. N., Adamus, J. E., Mittler, J. C., & Levin, B. E. Humoral indices of stress in rats. Physiology and Behavior, 1981, 26, 1049–1054.PubMedCrossRefGoogle Scholar
  42. Reite, M., Short, R., Kaufman, I. C., Stynes, A. J., & Pauley, J. D. Heart rate and body temperature in separated monkey infants. Biological Psychiatry, 1978, 13, 91–105.PubMedGoogle Scholar
  43. Reite, M., Short, R., & Seiler, C. Physiological correlates of maternal separation in surrogate-reared infants: A study in altered attachment bonds. Developmental Psychobiology, 1978, 11, 427–435.PubMedCrossRefGoogle Scholar
  44. Robertson, J., & Robertson, J. Young children in brief separation: A fresh look. Psychoanalytic Study of the Child, 1971, 26, 264–315.PubMedGoogle Scholar
  45. Rose, R. M. Endocrine responses to stressful psychological events. Psychiatric Climcs of North America, 1980, 3, 251–275.Google Scholar
  46. Rosenblum, L. A. Infant attachment in monkeys. In R. Schaffer, (Ed.), The origins of human social relations. New York: Academic Press, 1971, pp. 85–113. (a)Google Scholar
  47. Rosenblum, L. A. The ontogeny of mother-infant relations in macaques. In H. Moltz (Ed.), The ontogeny of vertebrate behavior. New York: Academic Press, 1971, pp. 315–367. (b)Google Scholar
  48. Rosenblum, L. A., & Kaufman, I. C. Variations in infant development and response to maternal loss in monkeys. American Journal of Orthopsychiatry, 1968, 38, 418–426.PubMedCrossRefGoogle Scholar
  49. Rosenblum, L. A., & Plimpton, E. H. Adaption to separation: The infant’s effort to cope with an altered environment. In M. Lewis & L. A. Rosenblum (Eds.), The uncommon child: Genesis of behavior (Vol. 3). New York: Plenum Press, 1981.Google Scholar
  50. Rosenblum, L. A., & Youngstein, K. P. Developmental changes in compensatory dyadic response in mother and infant monkeys. In J. Lewis & L. A. Rosenblum (Eds.), The influence of the infant on its caregiver. New York: Wiley, 1974, pp. 141–161.Google Scholar
  51. Ruppenthal, G. C., & Sackett, G. A. Experimental and husbandry procedures: Their impact on development. In G. C. Ruppenthal & G. A. Sackett (Eds.), Nursery care of nonhuman primates. New York: Plenum Press, 1979, pp. 269–287.Google Scholar
  52. Sackett, G. A. Innate mechanisms, rearing conditions and a theory of early experience effects in primates. In M. R. Jones (Ed.), Miami Symposium on the Prediction of Behavior: Early Experience. Miami: Miami University Press, 1970, pp. 11–53.Google Scholar
  53. Seay, B., Hansen, E., & Harlow, H. F. Mother-infant separation in monkeys. Journal of Child Psychology and Psychiatry, 1962, 5, 123–132.CrossRefGoogle Scholar
  54. Seligman, M. E. P. Learned helplessness: On depression, development and death. San Francisco: W. H. Freeman, 1975.Google Scholar
  55. Smotherman, W. P., Hunt, L. E., McGinnis, L. M., & Levine, S. Mother-infant separation in group-living rhesus macaques.: A hormonal analysis. Developmental Psychobiology, 1979, 12, 211–217.PubMedCrossRefGoogle Scholar
  56. Sroufe, L. A., Waters, E., & Matas, L. Contextual determinants of infant affective response. In M. Lewis & L. A. Rosenblum (Eds.), The origins of fear. New York: Wiley, 1974, pp. 49–72.Google Scholar
  57. Suomi, S., Harlow, H., & Domek, C. Effect of repetitive infant-infant separation of young monkeys. Journal of Abnormal Psychology, 1970, 76, 161–172.PubMedCrossRefGoogle Scholar
  58. Vogt, J. L, & Levine, S. Response of mother-infant squirrel monkeys to separation and disturbance. Physiology and Behavior, 1980, 24, 829–832.PubMedCrossRefGoogle Scholar
  59. Vogt, J. L., Coe, C. L. & Levine, S. Behavioral and adrenocorticoid responsiveness of squirrel monkeys to a live snake: Is flight necessarily stressful? Behavioral and Neural Biology, 1981, 32, 391–405.PubMedCrossRefGoogle Scholar
  60. Wallen, K., Bielert, C., & Slimp, J. Foot clasp mounting in the prepubertal rhesus monkey: Social and hormonal influences. In S. Chevalier-Skolnikoff and F. E. Poirier (Eds.), Primate bio-social development. New York: Garland, 1977, pp. 439–462.Google Scholar
  61. Weinberg, J., & Levine, S. Psychobiology of coping in animals: The effects of predictability. In S. Levine & H. Ursin (Eds.), Coping and health. New York: Plenum Press, 1980, pp. 39–59.Google Scholar
  62. Weinraub, M., & Lewis, M. The determinants of children’s responses to separation. Monographs of the Society for Research in Child Development, 1977, 42, Serial No. 172.Google Scholar
  63. Weiss, J. M. Effects of coping responses on stress. Journal of Comparative Physiology and Psychology, 1968, 65, 251–260.CrossRefGoogle Scholar
  64. Weiss, J. M. Somatic effects of predictable and unpredictable shock. Psychosomatic Medicine, 1970, 32, 397–408.PubMedGoogle Scholar

Copyright information

© Plenum Press, New York 1983

Authors and Affiliations

  • Christopher L. Coe
    • 1
  • Sandra G. Wiener
    • 1
  • Seymour Levine
    • 1
  1. 1.Department of Psychiatry and Behavioral SciencesStanford University School of MedicineStanfordUSA

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