Social buffering of the stress response: Diversity, mechanisms, and functions

Protracted or repeated activation of the hypothalamic-pituitary-adrenocortical (HPA) system is associated with a variety of physical and psychological pathologies. Studies dating back to the 1970s have documented many cases in which the presence of a social companion can moderate HPA responses to stressors. However, there also are many cases in which this "social buffering" of the HPA axis is not observed. An examination of the literature indicates that the nature of the relationship between individuals is crucial in determining whether or not social buffering of the HPA response will occur. Other factors that affect social buffering, either directly or by influencing the social relationship, include the social organization of the species, previous experience, gender, integration into a social unit, and the developmental stage at which individuals are examined. Current evidence suggests that social buffering involves mechanisms acting at more than one level of the CNS. It is suggested that, in addition to promoting health, social buffering may have evolved to direct the establishment of social relationships, and to facilitate developmental transitions in social interactions appropriate for different life stages.

[1]  J. Baldwin The ontogeny of social behaviour of squirrel monkeys (Saimiri sciureus) in a seminatural environment. , 1969, Folia primatologica; international journal of primatology.

[2]  D. M. Lyons,et al.  Distinct immediate and prolonged effects of separation on plasma cortisol in adult female squirrel monkeys , 1992, Psychobiology.

[3]  C. Stasi,et al.  Role of the Brain-Gut Axis in the Pathophysiology of Crohn’s Disease , 2008, Digestive Diseases.

[4]  M. Stanton,et al.  Maternal modulation of infant glucocorticoid stress responses: Role of age and maternal deprivation , 1988, Psychobiology.

[5]  E. Hess,et al.  Early behavior: Comparative and developmental approaches , 1975 .

[6]  C. Coe,et al.  Hormonal responses accompanying fear and agitation in the squirrel monkey , 1982, Physiology & Behavior.

[7]  S. Boinski Habitat use by squirrel monkeys (Saimiri oerstedi) in Costa Rica. , 1987, Folia primatologica; international journal of primatology.

[8]  S. Cobb Presidential Address-1976. Social support as a moderator of life stress. , 1976, Psychosomatic medicine.

[9]  C. Kirschbaum,et al.  Social support and oxytocin interact to suppress cortisol and subjective responses to psychosocial stress , 2003, Biological Psychiatry.

[10]  J. W. Rudy,et al.  Changes in the categorization of appetitive and aversive events during postnatal development of the rat. , 1988, Developmental psychobiology.

[11]  J. T. Martin Embryonic Pituitary Adrenal Axis, Behavior Development and Domestication in Birds , 1978 .

[12]  I. Neumann Involvement of the brain oxytocin system in stress coping: interactions with the hypothalamo-pituitary-adrenal axis. , 2002, Progress in brain research.

[13]  M. Hennessy,et al.  Plasma cortisol and vocalization responses of postweaning age guinea pigs to maternal and sibling separation: evidence for filial attachment after weaning. , 1995, Developmental psychobiology.

[14]  I. Eibl-Eibesfeldt Ethology, the biology of behavior , 1970 .

[15]  J. Haller,et al.  Genomic and non-genomic effects of glucocorticoids on aggressive behavior in male rats , 2004, Psychoneuroendocrinology.

[16]  C. Carter,et al.  Social Modulation of Corticosteroid Responses in Male Prairie Voles , 1997, Annals of the New York Academy of Sciences.

[17]  S. Lindell,et al.  Neurobiological characteristics of rhesus macaque abusive mothers and their relation to social and maternal behavior , 2005, Neuroscience & Biobehavioral Reviews.

[18]  M. Hennessy,et al.  Monoamine activity in anterior hypothalamus of guinea pig pups separated from their mothers. , 1994, Behavioral neuroscience.

[19]  N. Sachser,et al.  SOCIAL RELATIONSHIPS AND THE MANAGEMENT OF STRESS , 1998, Psychoneuroendocrinology.

[20]  K. J. Parker,et al.  Development of selective partner preferences in captive male and female meadow voles, Microtus pennsylvanicus , 2001, Animal Behaviour.

[21]  J. Anselmo-Franci,et al.  Stress increases oxytocin release within the hypothalamic paraventricular nucleus , 1998, Brain Research.

[22]  P. Brain,et al.  Effects of adrenalectomy and treatments with ACTH and glucocorticoids on isolation-induced aggressive behavior in male albino mice. , 1974, Progress in brain research.

[23]  N. Pillay,et al.  INTRASPECIFIC VARIATION IN THE SPATIAL AND SOCIAL ORGANIZATION OF THE AFRICAN STRIPED MOUSE , 2005 .

[24]  A. Sapse Cortisol, high cortisol diseases and anti-cortisol therapy , 1997, Psychoneuroendocrinology.

[25]  G. Bath A Natural History of Domesticated Mammals , 2001 .

[26]  H. Engler,et al.  Social stress and T cell maturation in male rats: transient and persistent alterations in thymic function , 2003, Psychoneuroendocrinology.

[27]  B. McEwen Protective and damaging effects of stress mediators: central role of the brain , 2006, Dialogues in clinical neuroscience.

[28]  L. Gavrilović,et al.  Immobilization and cold stress affect sympatho–adrenomedullary system and pituitary–adrenocortical axis of rats exposed to long-term isolation and crowding , 2004, Physiology & Behavior.

[29]  K. Uvnäs‐Moberg,et al.  OXYTOCIN MAY MEDIATE THE BENEFITS OF POSITIVE SOCIAL INTERACTION AND EMOTIONS 1 The purpose of this paper is to describe the neuroendocrine mechanisms of positive social interactions. 1 , 1998, Psychoneuroendocrinology.

[30]  Matthew D. Lieberman,et al.  Does Rejection Hurt? An fMRI Study of Social Exclusion , 2003, Science.

[31]  N. Christenfeld,et al.  Gender, social support, and cardiovascular responses to stress. , 1999, Psychosomatic medicine.

[32]  D. Lott,et al.  Intraspecific Variation in the Social Systems of Wild Vertebrates , 1991 .

[33]  N. Sachser,et al.  Maternal separation in Guinea-pigs: A study in behavioural endocrinology , 2003 .

[34]  M. Gunnar,et al.  The stressfulness of separation among nine-month-old infants: effects of social context variables and infant temperament. , 1992, Child development.

[35]  N. Sachser,et al.  The Behavioral Endocrinology of Domestication: A Comparison between the Domestic Guinea Pig (Cavia apereaf.porcellus) and Its Wild Ancestor, the Cavy (Cavia aperea) , 1999, Hormones and Behavior.

[36]  Todd H. Ahern,et al.  The CRF System Mediates Increased Passive Stress-Coping Behavior Following the Loss of a Bonded Partner in a Monogamous Rodent , 2009, Neuropsychopharmacology.

[37]  M. Hennessy,et al.  Hormonal and behavioral attachment responses in infant guinea pigs. , 1987, Developmental psychobiology.

[38]  S. Moriceau,et al.  Maternal attenuation of hypothalamic paraventricular nucleus norepinephrine switches avoidance learning to preference learning in preweanling rat pups , 2007, Hormones and Behavior.

[39]  S. Levine Influence of psychological variables on the activity of the hypothalamic-pituitary-adrenal axis. , 2000, European journal of pharmacology.

[40]  J. Panksepp,et al.  Oxytocin mediates acquisition of maternally associated odor preferences in preweanling rat pups. , 1996, Behavioral neuroscience.

[41]  B. Uchino Social Support and Health: A Review of Physiological Processes Potentially Underlying Links to Disease Outcomes , 2006, Journal of Behavioral Medicine.

[42]  Thomas R. Insel,et al.  Enhanced social interactions in rats following chronic, centrally infused oxytocin , 1992, Pharmacology Biochemistry and Behavior.

[43]  J. Epplen,et al.  Monogamy in a new species of wild guinea pigs (Galea sp.) , 2002, Naturwissenschaften.

[44]  K. Kotrschal,et al.  Benefits of family reunions: Social support in secondary greylag goose families , 2009, Hormones and Behavior.

[45]  R. Sullivan,et al.  Consolidation and expression of a shock-induced odor preference in rat pups is facilitated by opioids , 2003, Physiology & Behavior.

[46]  J. French,et al.  Close Proximity of the Heterosexual Partner Reduces the Physiological and Behavioral Consequences of Novel-Cage Housing in Black Tufted-Ear Marmosets ( Callithrix kuhli ) , 1998, Hormones and Behavior.

[47]  T. Kral,et al.  The immune-hypothalamic-pituitary-adrenal axis. , 1989, Endocrine reviews.

[48]  James K Rilling,et al.  Neural correlates of maternal separation in rhesus monkeys , 2001, Biological Psychiatry.

[49]  S. Moriceau,et al.  Maternal presence serves as a switch between learning fear and attraction in infancy , 2006, Nature Neuroscience.

[50]  P. Sacerdote,et al.  Individual housing induces altered immuno-endocrine responses to psychological stress in male mice , 2003, Psychoneuroendocrinology.

[51]  J. Herman,et al.  Bed Nucleus of the Stria Terminalis Subregions Differentially Regulate Hypothalamic–Pituitary–Adrenal Axis Activity: Implications for the Integration of Limbic Inputs , 2007, The Journal of Neuroscience.

[52]  J. French,et al.  Vocal buffering of the stress response: exposure to conspecific vocalizations moderates urinary cortisol excretion in isolated marmosets , 2005, Hormones and Behavior.

[53]  J. Epplen,et al.  Body Weight and Rearing Conditions of Males, Female Choice and Paternities in a Small Mammal, Cavia aperea , 2008 .

[54]  Jan Born,et al.  Sniffing neuropeptides: a transnasal approach to the human brain , 2002, Nature Neuroscience.

[55]  D. Amaral,et al.  Some observations on cortical inputs to the macaque monkey amygdala: An anterograde tracing study , 2002, The Journal of comparative neurology.

[56]  S. Mendoza,et al.  Behavior and plasma cortisol following brief peer separation in juvenile squirrel monkeys , 1982, American journal of primatology.

[57]  W. Mason,et al.  Parental division of labour and differentiation of attachments in a monogamous primate (Callicebus moloch) , 1986, Animal Behaviour.

[58]  J. Weinberg,et al.  Adrenocortical activity during conditions of brief social separation in preweaning rats. , 1990, Behavioral and neural biology.

[59]  M. Hennessy,et al.  Social preferences of developing guinea pigs (Cavia porcellus) from the preweaning to the periadolescent periods. , 2003, Journal of comparative psychology.

[60]  N. Sachser,et al.  Social organization predicts nature of infant-adult interactions in two species of wild guinea pigs (Cavia aperea and Galea monasteriensis). , 2006, Journal of comparative psychology.

[61]  K. Kendrick,et al.  Face pictures reduce behavioural, autonomic, endocrine and neural indices of stress and fear in sheep , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[62]  J. Baldwin The Behavior of Squirrel Monkeys (Saimiri) in Natural Environments , 1985 .

[63]  N. Sachser,et al.  Social housing conditions around puberty determine later changes in plasma cortisol levels and behavior , 2007, Physiology & Behavior.

[64]  K. Grossmann,et al.  Biobehavioral organization in securely and insecurely attached infants. , 1993, Child development.

[65]  Dietrich von Holst,et al.  The concept of stress and its relevance for animal behavior , 1998 .

[66]  J. Henry,et al.  Stress, Health, and the Social Environment: A Sociobiologic Approach to Medicine , 1977 .

[67]  H. McClure,et al.  Effect of a preferred companion in modulating stress in adult female rhesus monkeys , 1994, Physiology & Behavior.

[68]  D. Mobbs,et al.  When Your Gain Is My Pain and Your Pain Is My Gain: Neural Correlates of Envy and Schadenfreude , 2009, Science.

[69]  M. Hennessy,et al.  Cortisol and behavioral responses to separation in mother and infant guinea pigs. , 1987, Behavioral and neural biology.

[70]  T. Insel,et al.  Rearing Effects on Cerebrospinal Fluid Oxytocin Concentration and Social Buffering in Rhesus Monkeys , 2003, Neuropsychopharmacology.

[71]  M. Hennessy Both prevention of physical contact and removal of distal cues mediate cortisol and vocalization responses of guinea pig pups to maternal separation in a novel environment , 1988, Physiology & Behavior.

[72]  M. Hennessy Presence of companion moderates arousal of monkeys with restricted social experience , 1984, Physiology & Behavior.

[73]  E. S. E. Hafez,et al.  The behaviour of domestic animals , 1963 .

[74]  J. Kiecolt-Glaser,et al.  The physiology of marriage: pathways to health , 2003, Physiology & Behavior.

[75]  C. Pieper,et al.  Social support in social interaction: a moderator of cardiovascular reactivity. , 1992, Psychosomatic medicine.

[76]  S L Lightman,et al.  Central oxytocin administration reduces stress-induced corticosterone release and anxiety behavior in rats. , 1997, Endocrinology.

[77]  C. Coe,et al.  Handbook of Squirrel Monkey Research , 1985, Springer US.

[78]  F. Goodwin,et al.  Clinical and biochemical manifestations of depression. Relation to the neurobiology of stress (1) , 1988, The New England journal of medicine.

[79]  W. Mason,et al.  Responses of infant titi monkeys, Callicebus moloch, to removal of one or both parents: evidence for paternal attachment. , 1995, Developmental psychobiology.

[80]  M. Boccia,et al.  Oxytocin antagonism alters rat dams' oral grooming and upright posturing over pups , 2003, Physiology & Behavior.

[81]  F. Goodwin,et al.  Clinical and biochemical manifestations of depression. Relation to the neurobiology of stress (2) , 1988, The New England journal of medicine.

[82]  M. Hennessy,et al.  Consequences of the presence of the mother or unfamiliar adult female on cortisol, ACTH, testosterone and behavioral responses of periadolescent guinea pigs during exposure to novelty , 2000, Psychoneuroendocrinology.

[83]  J. Miller,et al.  Behavioral and glucocorticoid responses of adult domestic dogs (Canis familiaris) to companionship and social separation. , 1996, Journal of comparative psychology.

[84]  S. Maier,et al.  Medial prefrontal cortical activation modulates the impact of controllable and uncontrollable stressor exposure on a social exploration test of anxiety in the rat , 2009, Stress.

[85]  M. Palkovits,et al.  Stress-Induced Norepinephrine Release in the Hypothalamic Paraventricular Nucleus and Pituitary-Adrenocortical and Sympathoadrenal Activity: In Vivo Microdialysis Studies , 1995, Frontiers in Neuroendocrinology.

[86]  R. Vertes Differential projections of the infralimbic and prelimbic cortex in the rat , 2004, Synapse.

[87]  W. McShea,et al.  Dynamics of social nesting in overwintering meadow voles (Microtus pennsylvanicus): possible consequences for population cycling , 1984, Behavioral Ecology and Sociobiology.

[88]  N. Sachser Different Forms of Social Organization At High and Low Population Densities in Guinea Pigs , 1986 .

[89]  C. Carter,et al.  The effects of stress on social preferences are sexually dimorphic in prairie voles. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[90]  Miss A.O. Penney (b) , 1974, The New Yale Book of Quotations.

[91]  C. Carter,et al.  Modulation of pair bonding in female prairie voles (Microtus ochrogaster) by corticosterone. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[92]  Carol Carter Porges Neuroendocrine perspectives on social attachment and love , 1998 .

[93]  G. Evans,et al.  Social support lowers cardiovascular reactivity to an acute stressor. , 1993, Psychosomatic medicine.

[94]  T. Wills,et al.  Stress, social support, and the buffering hypothesis. , 1985, Psychological bulletin.

[95]  W. Jacobs,et al.  Male-female associations in the domestic guinea pig , 1976, Animal learning & behavior.

[96]  J. Herman,et al.  Neurocircuitry of stress: central control of the hypothalamo–pituitary–adrenocortical axis , 1997, Trends in Neurosciences.

[97]  F. Trillmich,et al.  Large males dominate: ecology, social organization, and mating system of wild cavies, the ancestors of the guinea pig , 2008, Behavioral Ecology and Sociobiology.

[98]  M. Hennessy,et al.  Social buffering of the cortisol response of adult female guinea pigs , 2008, Physiology & Behavior.

[99]  M. W. Andrews,et al.  Persistent elevations of cerebrospinal fluid concentrations of corticotropin-releasing factor in adult nonhuman primates exposed to early-life stressors: implications for the pathophysiology of mood and anxiety disorders. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[100]  R. Hayward Stress , 2005, The Lancet.

[101]  N. Rowland,et al.  Administration of dexfenfluramine in pregnant rats: Effect on brain serotonin parameters in offspring , 1992, Pharmacology Biochemistry and Behavior.

[102]  M. Hennessy,et al.  Presence of Mother and Unfamiliar Female Alters Levels of Testosterone, Progesterone, Cortisol, Adrenocorticotropin, and Behavior in Maturing Guinea Pigs , 2002, Hormones and Behavior.

[103]  N. Sachser,et al.  Is a wild mammal kept and reared in captivity still a wild animal? , 2003, Hormones and Behavior.

[104]  S. Schwaiger,et al.  Plasma corticosterone fluctuations in an infant-learning paradigm. , 1988, Behavioral neuroscience.

[105]  R. Boice Domestication. , 1973, Psychological bulletin.

[106]  R. Sapolsky,et al.  How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. , 2000, Endocrine reviews.

[107]  D. M. Lyons,et al.  Review Sociophysiology of Squirrel Monkeys , 2022 .

[108]  M. Hennessy,et al.  Development of selective social buffering of the plasma cortisol response in laboratory-reared male guinea pigs (Cavia porcellus). , 2009, Behavioral neuroscience.

[109]  J. Epplen,et al.  Female influences on pair formation, reproduction and male stress responses in a monogamous cavy (Galea monasteriensis) , 2008, Hormones and Behavior.

[110]  W. P. Smotherman,et al.  Mother-infant separation in group-living rhesus macaques: a hormonal analysis. , 1979, Developmental psychobiology.

[111]  M. Hennessy,et al.  Factors influencing cortisol and behavioral responses to maternal separation in guinea pigs. , 1989, Behavioral neuroscience.

[112]  Jesse L. Hawke,et al.  Social influences on cortisol and behavioral responses of preweaning, periadolescent, and adult guinea pigs , 2002, Physiology & Behavior.

[113]  M. Hennessy Effects of social partners on pituitary-adrenal activity during novelty exposure in adult female squirrel monkeys , 1986, Physiology & Behavior.

[114]  N. Sachser,et al.  Sex-specific difference in social support—a study in female guinea pigs , 2003, Physiology & Behavior.

[115]  M. Lamb,et al.  Attachment and bonding: a new synthesis , 2005 .

[116]  M. Stanton,et al.  Social influences on conditioned cortisol secretion in the squirrel monkey , 1985, Psychoneuroendocrinology.

[117]  S. Lightman,et al.  Oxytocin Attenuates Stress-Induced c-fos mRNA Expression in Specific Forebrain Regions Associated with Modulation of Hypothalamo–Pituitary–Adrenal Activity , 2004, The Journal of Neuroscience.

[118]  N. Sachser,et al.  Cortisol responses and social buffering: A study throughout the life span , 2006, Hormones and Behavior.

[119]  Clemens Kirschbaum,et al.  Sex-Specific Effects of Social Support on Cortisol and Subjective Responses to Acute Psychological Stress , 1995, Psychosomatic medicine.

[120]  W. P. Smotherman,et al.  Pituitary-adrenal response to separation in mother and infant squirrel monkeys. , 1978, Developmental psychobiology.

[121]  T. Kamarck,et al.  Social support reduces cardiovascular reactivity to psychological challenge: a laboratory model. , 1990, Psychosomatic medicine.

[122]  R. Parritz,et al.  Behavioral inhibition and stress reactivity: the moderating role of attachment security. , 1996, Child development.

[123]  D. M. Lyons,et al.  Social grouping tendencies and separation-induced distress in juvenile sheep and goats. , 1993, Developmental psychobiology.

[124]  W. Mason,et al.  Endocrine sensitivity to novelty in squirrel monkeys and titi monkeys: Species differences in characteristic modes of responding to the environment , 1995, Physiology & Behavior.

[125]  C. Ferris,et al.  Cortisol Exerts Site‐, Context‐ and Dose‐Dependent Effects on Agonistic Responding in Hamsters , 1991, Journal of neuroendocrinology.

[126]  J. Winslow,et al.  Social buffering: relief from stress and anxiety , 2006, Philosophical Transactions of the Royal Society B: Biological Sciences.

[127]  Matthew D. Lieberman,et al.  Neural pathways link social support to attenuated neuroendocrine stress responses , 2007, NeuroImage.

[128]  M. Hennessy,et al.  Comparison of the effects of the mother and an unfamiliar adult female on cortisol and behavioral responses of pre- and postweaning guinea pigs. , 2000, Developmental psychobiology.

[129]  L. Remage-Healey,et al.  Behavioral and adrenocortical responses to mate separation and reunion in the zebra finch , 2003, Hormones and Behavior.

[130]  M. Gunnar,et al.  The role of peers in modifying behavioral distress and pituitary-adrenal response to a novel environment in year-old rhesus monkeys , 1980, Physiology & Behavior.

[131]  J W Mason,et al.  A historical view of the stress field. , 1975, Journal of human stress.

[132]  Norbert Sachser,et al.  SOCIAL SYSTEM AND SPATIAL ORGANIZATION OF WILD GUINEA PIGS (CAVIA APEREA) IN A NATURAL POPULATION , 2004 .

[133]  J. House,et al.  Social relationships and health. , 1988, Science.

[134]  A. Armario,et al.  Corticoadrenal and behavioral response to open field in pairs of male rats either familiar or non-familiar to each other , 1983, Experientia.

[135]  J. Herman,et al.  Role of GABA and Glutamate Circuitry in Hypothalamo‐Pituitary‐Adrenocortical Stress Integration , 2004, Annals of the New York Academy of Sciences.

[136]  Ulrike Ehlert,et al.  Effects of different kinds of couple interaction on cortisol and heart rate responses to stress in women , 2007, Psychoneuroendocrinology.

[137]  E. Price Behavioral Aspects of Animal Domestication , 1984, The Quarterly Review of Biology.

[138]  Zuoxin Wang,et al.  Nucleus accumbens oxytocin and dopamine interact to regulate pair bond formation in female prairie voles , 2003, Neuroscience.

[139]  M. Gunnar,et al.  The effects of morning naps, car trips, and maternal separation on adrenocortical activity in human infants. , 1991, Child development.

[140]  K. Kotrschal,et al.  Active and passive social support in families of greylag geese (Anser anser). , 2005, Behaviour.

[141]  Deanne F. Johnson,et al.  Influence of postnatal rearing conditions on the response of squirrel monkey infants to brief perturbations in mother-infant relationships , 1987, Physiology & Behavior.

[142]  Bruce S. McEwen,et al.  Allostasis, amygdala, and anticipatory angst , 1994, Neuroscience & Biobehavioral Reviews.

[143]  R. Rose,et al.  Plasma cortisol and growth hormone responses to intravenous characterization. , 1975, Journal of human stress.

[144]  T. Insel,et al.  Cellular Mechanisms of Social Attachment , 2001, Hormones and Behavior.