Neuroscience
Frontiers in Evolutionary Neuroscience ·
Volume 2 - 2011 | https://doi.org/10.3389/fnevo.2010.00111
Social Allostasis: Anticipatory Regulation of the Internal Milieu
- Jay Schulkin1,2*corresponding author
- 11 Department of Neuroscience, Georgetown University Washington, DC, USA
- 22 National Institute of Mental Health Bethesda, MD, USA
Abstract
Social regulation of the internal milieu is a fundamental behavioral adaptation. Cephalic capability is reflected by anticipatory behaviors to serve systemic physiological regulation. Homeostatic regulation, a dominant perspective, reflects reactive responses; allostatic regulation, the physiology of change, emphasizes longer-term anticipatory, and feedforward systems. Steroids, such as cortisol, and peptides such as corticotrophin releasing hormone are but one example of such anticipatory regulatory systems. The concept of “allostasis” is in part to take account of anticipatory control amidst diverse forms of adaptation underlying this regulatory adaptation that supports social contact and the internal milieu.
Keywords
References
- Abbott D. H., Keverne E. B., Bercovitch F. B., Shively C. A., Mendoza S. P., Saltzman W., Snowdon C. T., Ziegler T. E., Banjevic M., Garland T., Sapolsky R. M. (2003). Are subordinates always stressed? A comparative analysis of rank differences in cortisol levels among primates. Horm. Behav. 43, 67 – 82.
- Adkins-Regan E. (2005). Hormones and animal social behavior. Princeton, NJ: Princeton University Press.
- Ahnert L., Gunnar M. R., Lamb M. E., Barthel M. (2004). Transition to childcare: associations with infant–mother attachment, infant negative emotion, and cortisol elevations. Child Dev. 75, 639 – 650. doi:10.1111/j.1467-8624.2004.00698.x
- Arnold A. P., Breedloev S. M. (1985). Organizational and activational effects of sex steroids on brain and behavior: a reanalysis. Horm. Behav. 19, 469 – 498.
- Barger N., Stefanacci L., Semendeferi K. (2007). A comparative volumetric analysis of the amygdaloid complex and basolateral division in the human and ape brain. Am. J. Phys. Anthropol. 134, 392 – 403.
- Barton R. A. (2006). Primate brain evolution: integrating comparative neurophysiological and ethological data. Evol. Anthropol. 15, 224 – 236.
- Barton R. A., Aggleton J. P., Greyner R. (2003). Evolutionary coherence of the mammalian amygdala. Proc. R. Soc. Lond. B Biol. Sci. 270, 539 – 543.
- Bauman D. E. (2000). “Regulation of nutrient partitioning during lactation: homeostasis and homeorhesis revisited,” in Ruminant Physiology, ed. Cronje P. J. (New York: CAB Publishing), 311 – 328.
- Bernard C. (1859). Lecons sur les Proprietes Physiologiques et les Alterations Pathologiques de l'Organisme. Paris: Balliers.
- Berridge K. C. (2004). Motivation concepts in behavioral neuroscience. Physiol. Behav. 81, 179 – 209.
- Berridge K. C. (2007). The debate over dopamine's role in reward: the case for incentive salience. Physiol. Behav. 191, 391 – 431.
- Buttemer W. A., Astheimer L. B., Wingfield J. C. (1991). The effect of corticosterone on standard metabolic rates of small passerine birds. J. Comp. Physiol. 161, 427 – 431.
- Cacioppo J. T., Bernston G. G. (2007). “The brain, homeostasis and health: balancing demands of the internal and external milieu,” in Oxford Handbook of Health Psychology, eds Fiedman H. S., Cohen-Silver R. (Oxford: Oxford University Press), 73 – 91.
- Cacioppo J. T., Hawkley L., Ernst J. M., Burleson M., Berntson G. G., Nouriani B., Spiegel D. (2006). Loneliness within a nomological net: an evolutionary perspective. J. Res. Pers. 40, 1054 – 1085.
- Cannon W. B. (1929). Bodily Changes in Pain, Hunger, Fear and Rage. New York: Appleton and Co.
- Cameron N. M., Shahrokh D., Del Corpo A., Dhir S. K., Szyf M., Champagne F. A., Meaney M. J. (2008). Epigenetic programming of phenotypic variations in reproductive strategies in the rat through maternal care. J. Neuroendocrinol. 20, 795 – 801. doi:10.1111/j.1365-2826.2008.01725.x
- Cannon W. B. (1963). The Wisdom of the Body. New York: W. W. Norton.
- Carlson E. D., Chamberlain R. M. (2005). Allostatic load and health disparities: a theoretical orientation. Res. Nurs. Health 28, 306 – 315.
- Carpenter R. H. S. (2004). Homeostasis: a plea for a unified approach. Adv. Physiol. Educ. 28, 180 – 187.
- Carter C. S., Lederhendler I. L., Kirkpatrick B. (1999). The Integrative Neurobiology of Affiliation. Cambridge: MIT Press.
- Cavigelli S. A., Dubovick T., Levash W., Jolly A., Pitts A. (2003). Female dominance status and fecal corticoids in a cooperative breeder with low reproductive skew: ring-tailed lemurs. Horm. Behav. 43, 166 – 179.
- Champagne F. A. (2003). Variations in maternal care in the rat as a mediating influence for the effects of environment on development. Physiol. Behav. 79, 359 – 371.
- Cheney D. L., Seyfarth R. M. (1990). How Monkeys See the World. Chicago: University of Chicago Press.
- Cheney D. L., Seyfarth R. M. (2007). Baboon Metaphysics. Chicago, IL: University of Chicago Press.
- Choleris E., Devidze N., Kavaliers M., Pfaff D. W. (2008). “Steroidal/neuropeptides interactions in hypothalamus and amygdala related to social anxiety,” in Progress in Brain Research, Vol. 170, eds Neumann I. D., Landgraf R. (Oxford, UK), 291 – 303.
- Chrousos G. P. (1996). The hypothalamic-pituitary-adrenal axis and immunomediated inflammation. N. Eng. J. Med. 332, 1351 – 1362.
- Chrousos G. P., Gold P. W. (1992). The concepts of stress and stress system disorders: overview of physical and behavioral homeostasis. J. Am. Med. Assoc. 267, 1244 – 1252. doi:10.1001/jama.267.9.1244
- Cook C. J. (2002). Glucocorticoid feedback increases the sensitivity of the limbic system to stress. Physiol. Behav. 75, 455 – 464.
- Coplan J. D., Andrews M. W., Rosenblum L. A., Owens M. J., Friedman S., Gorman J. M., Nemeroff C. B. (1996). 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. Proc. Natl. Acad. Sci. U.S.A. 93, 1619 – 1623.
- Creel S. (2001). Social dominance and stress hormones. Trends Ecol. Evol. 16, 491 – 497.
- Crews D. (2008). Epigenetics and its implications for behavioral neuroendocrinology. Front. Neuroendocrinol. 29, 344 – 357. doi:10.1016/j.yfrne.2008.01.003
- Crimmins E. M., Johnston M., Hayward M., Seeman T. (2003). Age differences in allostatic load: an index of physiological dysregulation. Exp. Gerontol. 38, 731 – 734.
- Dallman M. F. (2003). Stress by any other name? Horm. Behav. 43, 18 – 20.
- Dallman M. F., Pecoraro N., Akana S. F., La Fleur S. E., Gomez F., Houshyar H., Bell M. E., Bhatnagar S., Laugero K. D., Manalo S. (2003). Chronic stress and obesity: a new view of “comfort food”. Proc. Natl. Acad. Sci. U.S.A. 100, 11696 – 11701.
- Dallman M. F., Akana S. F., Cascio C. S., Darlington D. N., Jacobson L., Levin N. (1987). Regulation of ACTH secretion: variations on a theme of B. Recent Prog. Horm. Res. 43, 113 – 173.
- Dallman M. F., Akana S. F., Levin N., Walker C. D., Bradbury M. J., Suemaru S., Scribner K. S. (1994). Corticosteroids and the control of function in the hypothalamo-pituitary–adrenal (HPA) axis. Ann. N. Y. Acad. Sci. 747, 22 – 31; discussion 31–32, 64–67.
- Darwin C. (1874). The Descent of Man and Selection in Relation to Sex. Chicago: Rand, McNally and Co.
- Darwin C. (1958). The Origin of Species. New York: Mentor Book.
- Darwin C. (1998). The Expression of the Emotions in Man and Animals. Oxford: Oxford University Press.
- Day T. A. (2005). Defining stress as a prelude to mapping its neurocircuitry: no help from allostasis. Prog. Neuropsychopharmacol. Biol. Psychiatry 29, 1195 – 1200.
- Di Chiara G. (1999). Drug addiction as dopamine-dependent associative learning. Eur. J. Pharmacol. 375, 13 – 30.
- Dixson A. F., George L. (1982). Prolactin and parental behaviour in a male New World primate. Nature 299, 551 – 553. doi:10.1038/299551a0
- Donley M. P., Schulkin J., Rosen J. B. (2005). Glucocorticoid receptor antagonism in the basolateral amygdala and ventral hippocampus interferes with long-term memory of contextual fear. Behav. Brain Res. 164, 197 – 205.
- Dunbar R. I. M. (1998). The social brain hypothesis. Evol. Anthropol. 6, 178 – 190.
- Dunbar R. I. M., Shultz S. (2007). Evolution in the social brain. Science 317, 1344 – 1347. doi:10.1126/science.1145463
- Eberhart J. A., Keverne E. B., Meller R. E. (1980). Social influences on plasma testosterone levels in male talapoin monkeys. Horm. Behav. 14, 247 – 266.
- Ellison T. T., Gray P. B. (2009). Endocrinology of Social Relationships. Cambridge: Harvard University Press.
- Engh A. L., Beehner J. C., Bergman T. J., Whitten P. L., Hoffmeier R. R., Seyfarth R. M., Cheney D. L. (2006a). Female hierarchy instability, male immigration and infanticide increase glucocorticoid levels in female chacma baboons. Anim. Behav. 71, 1227 – 1337. doi:10.1016/j.anbehav.2005.11.009
- Engh A. L., Beehner J. C., Bergman T. J., Whitten P. L., Hoffmeier R. R., Seyfarth R. M., Cheney D. L. (2006b). Behavioral and hormonal responses to predation in female chacma baboons (Papio hamadryas ursinus). Proc. Biol. Sci. 273, 707 – 712. doi:10.1098/rspb.2005.3378
- Erickson K., Gabry K. E., Lindell S., Champoux M., Schulkin J., Gold P., Suomi S. J., Higley J. D. (2005). Social withdrawal behaviors in nonhuman primates and changes in neuroendocrine and monoamine concentrations during a separation paradigm. Dev. Psychobiol. 46, 331 – 339. doi:10.1002/dev.20061
- Falk D. (1983). Cereberal cortices of east African early hominids. Science 221, 1072 – 1074. doi:10.1126/science.221.4615.1072
- Fink G. (1997). “Mechanisms of negative and positive feedback of steroids in the HPA system,” in Principles of Medical Biology, Vol. 10, eds Bittar E. E., Bittar N. (New York: JAI Press) 29 – 30.
- Fitzsimons J. T. (1999). Angiotensin, thirst and sodium appetite. Physiol. Rev. 76, 583 – 686.
- Fleming A. S., Ruble D., Krieger H., Wong P. Y. (1997). Hormonal and experiential correlates of maternal responsiveness during pregnancy and the puerperium in human mothers. Horm. Behav. 31, 145 – 158.
- Fleming A. S., Steiner M., Corter C. (1997). Hormones, hedonics and maternal responsiveness in human mothers. Horm. Behav. 32, 85 – 98.
- Fluharty S. J., Epstein A. N. (1983). Sodium appetite elicited by intracerebroventricular infusion of angiotensin II in the rat: II. Synergistic interaction with systemic mineralocorticoids. Behav. Neurosci. 97, 746 – 758.
- Foley R. (1996). An evolutionary and chronological framework for human social behaviour. Proc. Br. Acad. 88, 95 – 117.
- Francis D. D., Diorio J., Liu D., Meaney M. J. (1999). Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science 286, 1155 – 1158. doi:10.1126/science.286.5442.1155
- Francis D. D., Young L. J., Meaney M. J., Insel T. R. (2002). Naturally occurring differences in maternal care are associated with the expression of oxytocin and vasopressin (V1a) receptors: gender differences. J. Neuroendocrinol. 14, 349 – 353. doi:10.1046/j.0007-1331.2002.00776.x
- Freud S. (1959). Inhibitions, Symptoms and Anxiety. (Strachey A. Trans.). Revised and newly edited by James Strachey. New York: W.W. Norton.
- Fromm E. (1947). Man for himself. New York: Rinehart & Company.
- Ganzel B. L., Morris P. A., Wethington E. (2010). Allostasis and the human brain: integrating models of stress from the social and life sciences. Psychol. Rev. 1, 134 – 174.
- Gluckman P. D., Hanson M. A., Spencer H. G. (2005). Predictive adaptive responses and human evolution. Trends Ecol. Evol. 20, 527 – 533.
- Goldstein D. S. (1995). Stress, catecholamines, and cardiovascular disease. New York: Oxford University Press.
- Goodson J. L. (2005). The vertebrate social behavioral network: evolutionary themes and variations. Horm. Behav. 48, 11 – 22.
- Goy R. W., McEwen B. S. (1980). Sexual differentiation of the brain. Cambridge, MA: MIT Press.
- Goymann W., Wingfield J. C. (2004). Allostatic load, social status and stress hormones: the costs of social status matter. Anim. Behav. 67, 591 – 602. doi:10.1016/j.anbehav.2003.08.007
- Grippo A. J., Gerena D., Huang J., Kumar N., Shah M., Ughreja R., Carter C. S. (2007). Social isolation induces behavioral and neuroendocrine disturbances relevant to depression in female and male prairie voles. Psychoneuroendocrinology 32, 966 – 980. doi:10.1016/j.psyneuen.2007.07.004
- Gunnar M. R. (1998). Quality of early care and buffering or neuroendocrine stress reactions: potential effects on the developing human brain. Prev. Med. 27, 208 – 211.
- Gunnar M. R., Davis E. P. (2005). “Stress and emotion in early childhood,” in Comprehensive handbook of psychology, Vol. 6, Developmental psychology, eds Lerner R. M., Easterbrooks M. A., Mistry J. (New York: Wiley), 113 – 134.
- Gunnar M. R., Mangelsdorf S., Larson M., Hertsgaard L. (1989). Attachment, temperament, and adrenocortical activity in infancy: a study of psychoendocrine regulation. Dev. Psychol. 25, 355 – 363.
- Habib K. E., Weld K. P., Rice K. C., Pushkas J., Champoux M., Listwak S., Webster E. L., Atkinson A. J., Shulkin J., Contoreggi C., Chrousos G. P., McCann S. M., Suomi S. J., Higley J. D., Gold P. W. (2000). Oral administration of a corticotropin-releasing hormone receptor antagonist significantly attenuates behavioral, neuroendocrine, and autonomic responses to stress in primates. Proc. Natl. Acad. Sci. U.S.A. 97, 6079 – 6084.
- Harlow J. F., Soumi S. J. (1971). Social recovery by isolation reared monkeys. Proc. Natl. Acad. Sci. U.S.A. 68, 1534 – 1538.
- Hellhammer J., Schlotz W., Stone A. A., Pirke K. M., Hellhammer D. (2004). Allostatic load, perceived stress, and health: a prospective study in two age groups. Ann. N. Y. Acad. Sci. 1032, 8 – 13.
- Herbert J. (1993). Peptides in the limbic system: neurochemical codes for co-ordinated adaptive responses to behavioral and physiological demand. Prog. Neurobiol. 41, 723 – 791.
- Herbert J., Schulkin J. (2002). “Neurochemical coding of adaptive responses in the limbic system,” in Hormones, Brain and Behavior, ed. Pfaff D. (New York: Elsevier Press), 659 – 690.
- Holliday R. (2002). Epigenetics comes of age in the twenty-first century. J. Genet. 81, 1 – 4. doi:10.1007/BF02715863
- Holliday R., Ho T. (1998). Evidence for gene silencing by endogenous DNA methylation. Proc. Natl. Acad. Sci.U.S.A. 95, 8727 – 8732.
- Huppert F. A., Baylis N., Keverne B. (2005). The Science of Well-Being. Oxford: Oxford University Press.
- Ikemoto S., Panksepp J. (1999). The role of nucleus accumbens dopamine in motivated behavior: a unifying interpretation with special reference to reward-seeking. Brain Res. Rev. 31, 6 – 41.
- Imaki T., Nahan J. L., Rivier C., Vale W. (1991). Differential regulation of corticotropin releasing hormone mRNA in rat brain regions by glucocorticoids and stress. J. Neurosci. 11, 585 – 598.
- Insel T. R., Fernald R. D. (2004). How the brain processes social information. Annu. Rev. Neurosci. 27, 697 – 722.
- James W. (1952). The Principles of Psychology. New York: Dover Press.
- Jaspers K. (1997). General Psychopathology, Vol. I and II. (Hoenig J., Hamilton M. W. Trans.) Baltimore: The Johns Hopkins University Press.
- Johnston-Brooks C. H., Lewis M. A., Evans G. W., Whalen C. K. (1998). Chronic stress and illness in children: the role of allostatic load. Psychosom. Med. 60, 597 – 603.
- Kagan J. (1984). The Nature of the Child. New York: Basic Books.
- Kalin N. H. (1985). Biological effects of corticotropin releasing hormone administered to rhesus monkeys. Fed. Proc. 44, 249 – 253.
- 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. Behav. Neurosci. 112, 286 – 292.
- Kalin N. H., Shelton S. E., Barksdale C. M. (1989). Behavioral and physiologic effects of CRH administered to infant primates undergoing maternal separation. Neuropsychopharmacology 2, 97 – 104. doi:10.1016/0893-133X(89)90012-2
- Kalin N. H., Shelton S. E., Davidson R. J. (2000). Cerebrospinal fluid corticotropin-releasing hormone levels are elevated in monkeys with patterns of brain activity associated with fearful temperament. Biol. Psychiatry 47, 579 – 585.
- Kalya S. P. (1993). Mandatory neuropeptide-steroid signaling for the preovulatory luteinizing hormone-releasing hormone discharge. Endocr. Rev. 14, 507 – 538.
- Karlamangla A. S., Singer B. H., McEwen B. S., Rowe J. W., Seeman T. E. (2002). Allostatic load as a predictor of functional decline. MacArthur studies of successful aging. J. Clin. Epidemiol. 55, 696 – 710.
- Keverne E. B. (2004a). Brain evolution, chemosensory processing, and behavior. Nutr. Rev. 62, S218 – S223; discussion S224–S241. doi:10.1111/j.1753-4887.2004.tb00102.x
- Keverne E. B. (2004b). Understanding well-being in the evolutionary context of brain development. Philos. Trans. R. Soc. Lond. B Biol. Sci. 359, 1349 – 1358. doi:10.1098/rstb.2004.1517
- Keverne E. B., Curley J. P. (2004). Vasopressin, oxytocin and social behavior. Curr. Opin. Neurobiol. 14, 777 – 783.
- Keverne E. B., Curley J. P. (2008). Epigenetics, brain evolution and behavior. Front. Neuroendocrinol. 29, 398 – 412. doi:10.1016/j.yfrne.2008.03.001
- Kolber B. J., Roberts M. S., Howell M. P., Wozniak D. F., Sands M. S., Muglia L. J. (2008). Central amygdala glucocorticoid receptor action promotes fear-associated CRH activation and conditioning. Proc. Natl. Acad. Sci. U.S.A. 105, 12004 – 12009.
- Koob G. F., LeMoal M. (2001). Drug addiction, dysregulation of reward, and allostasis. Neuropsychopharmacology 24, 94 – 129. doi:10.1016/S0893-133X(00)00195-0
- Koob G. F., LeMoal M. (2005). Neurobiology of Addiction. New York: Elsevier.
- Korte S. M., Koolhaas J. M., Wingfield J. C., McEwen B. S. (2004). The Darwinian concept of stress: benefits of allostasis and costs of allostatic load and the trade-offs in health and disease. Neurosci. Biobehav. Rev. 29, 3 – 38.
- Kubzansky L. D., Kawachi I., Sparrow D. (1999). Socioeconomic status, hostility, and risk factor clustering in the Normative Aging Study: any help from the concept of allostatic load? Ann. Behav. Med. 21, 330 – 338.
- Kukolja J., Schlapfer T. E., Keysers C., Klingmüller D., Maier W., Fink G. R., Hurlemann R. (2008). Modeling a negative response in the human amygdala by noradrenergic-glucocorticoid interactions. J. Neurosci. 28, 12868 – 12876. doi:10.1523/JNEUROSCI.3592-08.2008
- Landys M. M., Ramenofsky M., Wingfield J. C. (2006). Actions of glucocorticoids at a seasonal baseline as compared to stress-related levels in the regulation of periodic life processes. Gen. Comp. Endocrinol. 148, 132 – 149. doi:10.1016/j.ygcen.2006.02.013
- Levine S. (1975). “Psychosocial factors in growth and development,” in Society, Stress, and Disease, ed. Levi L. (London: Oxford University Press), 43 – 50.
- Liu D., Diorio J., Tannenbaum B., Caldji C., Francis D., Freedman A., Sharma S., Pearson D., Plotsky P. M., Meaney M. J. (1997). Maternal care, hippocampal glucocorticoid receptors, and hypothalamic–pituitary–adrenal responses to stress. Science 277, 1659 – 1662. doi:10.1126/science.277.5332.1659
- Lorenz K. (1965). Evolution and Modification of Behavior. Chicago: University of Chicago Press.
- Lorenz K. (1981). The Foundations of Ethology. New York: Springer.
- Lupien S. J., King S., Meaney M. J., McEwen B. S. (2000). Child's stress hormone levels correlate with mother's socioeconomic status and depressive state. Biol. Psychiatry 48, 976 – 980.
- Lupien S. J., Maheu F., Tu M., Fiocco A., Schramek T. E. (2007). The effects of stress and stress hormones on human cognition: implications for the field of brain and cognition. Brain Cogn. 65, 209 – 237. doi:10.1016/j.bandc.2007.02.007
- Makino S., Gold P. W., Schulkin J. (1994a). Corticosterone effects on corticotropin-releasing hormone mRNA in the central nucleus of the amygdala and the parvocellular region of the paraventricular nucleus of the hypothalamus. Brain Res. 640, 105 – 112. doi:10.1016/0006-8993(94)91862-7
- Makino S., Gold P. W., Schulkin J. (1994b). Effects of corticosterone on CRH mRNA and content in the bed nucleus of the amygdala and the paraventricular nucleus of the hypothalamus. Brain Res. 657, 141 – 149. doi:10.1016/0006-8993(94)90961-X
- Makino S., Schulkin J., Smith M. A., Pacak K., Palkorits M., Gold P. W. (1995). Regulation of corticotropin-releasing hormone receptor messenger ribonucleic acid in the rat brain and pituitary by glucocorticoids and stress. Endocrinology 136, 4517 – 4525. doi:10.1210/en.136.10.4517
- McCarthy M. M. (2008). Estradiol and the developing brain. Physiol. Rev. 88, 91 – 134.
- McEwen B. S. (1995). Steroid actions on neuronal signalling. Ernst Schering Res. Found. Lect. Ser. 27, 1 – 45.
- McEwen B. S. (1998). Protective and damaging effects of stress mediators. N. Engl. J. Med. 338, 171 – 179.
- McEwen B. S. (2007). Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol. Rev. 87, 873 – 904.
- McEwen B. S., Stellar E. (1993). Stress and the individual: mechanisms leading to disease. Arch. Int. Med. 153, 2093 – 3101.
- McEwen B. S., Wingfield J. C. (2003). The concept of allostasis in biology and medicine. Horm. Behav. 41, 2 – 15.
- McEwen B. S., Wingfield J. C. (2010). What's in a name? Integrating homeostasis, allostasis and stress. Horm. Behav. 57, 105 – 111.
- McGaugh J. L. (2000). Memory – A century of consolidation. Science 287, 248 – 251. doi:10.1126/science.287.5451.248
- McGaugh J. L. (2003). Memory and emotion. New York: Columbia University Press.
- Meaney M. J. (2001). Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu. Rev. Neurosci. 24, 1161 – 1192.
- Meaney M. J., Diorio J., Francis D., Widdowson J., LaPlante P., Caldji C., Sharma S., Seckly J. R., Plotsky P. M. (1996). Early environmental regulation of forebrain glucocorticoid receptor gene expression: implications for adrenocortical responses to stress. Dev. Neurosci. 18, 49 – 72.
- Merali Z., Anisman H., James J. S., Kent P., Schulkin J. (2008). Effects of corticosterone on CRH and gastrin-releasing peptide release in response to an aversive stimulus in two regions of the forebrain. Eur. J. Neurosci. 28, 165 – 172.
- Merali Z., McIntosch J., Anisman H. (2004). Anticipatory cues differentially provoke in vivo peptidergic and monomaninertic release at the medial prefrontal cortex. Neuropharmacology 29, 1417 – 1418.
- Merali Z., McIntosh J., Kent P., Michaud D., Anisman H. (1998). Aversive and appetitive events evoke the release of corticotropin-releasing hormone and bombesin-like peptides at the central nucleus of the amygdala. J. Neurosci. 18, 4758 – 4766.
- Miller N. E. (1957). Experiments of motivation. Studies combining psychological, physiological, and pharmacological techniques. Science 126, 1271 – 1278. doi:10.1126/science.126.3286.1271
- Miller N. E. (1959). “Liberalization of basicc S-R concepts: extensions to conflict behaviour, motivation and social learning,” in Psychology: A Study of a Science, ed. Koch S. Vol. 2 (New York: McGraw-Hill), 196 – 292.
- Moore-Ede M. C. (1986). Physiology of the circadian timing system: predictive versus reactive homeostasis. Am. J. Physiol. 250, R737 – R752.
- Moore-Ede M. C., Sulzman F. M., Fuller C. A. (1992). The clocks that time us. Cambridge, UK: Harvard University Press.
- Nachmias M., Gunnar M., Mangelsdorf S., Hornik Parritz R., Buss K. (1996). Behavioral inhibition and stress reactivity: the moderating role of attachment security. Child Dev. 67, 508 – 522. doi:10.2307/1131829
- Ostwald M. (1962). Aristotle's Nicomachean ethics. New York: Macmillan.
- Mrosovsky N. (1990). Rheostasis, The physiology of Change. New York: Oxford University Press.
- Palombit R. A., Seyfarth R. M., Cheney D. L. (1997). The adaptive value of “friendships” to female baboons: experimental and observational evidence. Anim. Behav. 54, 599 – 614. doi:10.1006/anbe.1996.0457
- Peciña S., Schulkin J., Berridge K. C. (2006). Nucleus accumbens corticotropin-releasing factor increases cue-triggered motivation for sucrose reward: paradoxical positive incentive effects in stress? BMC Biol. 4, 8. doi:10.1186/1741-7007-4-8
- Pfaff D. W. (1980). Estrogens and brain function. New York: Springer-Verlag.
- Pfaff D. W. (1999). Drive. Cambridge: MIT Press.
- Power M. L. (2004). “Viability as opposed to stability: an evolutionary perspective on physiological regulation,” in Allostasis, Homeostasis and the Costs of Adaptation, ed. Schulkin J. (Cambridge: Cambridge University Press), 343 – 364.
- Power M. L., Schulkin J. (2009). Evolution of Obesity. Baltimore: Johns Hopkins University Press.
- Richter C. P. (1943). Total self-regulatory functions in animals and human beings. Harvey Lect. 38, 367 – 371.
- Ricklefs R. E., Wikelski M. (2002). The physiology/life history nexus. Trends Ecol. Evol. 17, 462 – 466.
- Robinson T. E., Berridge K. C. (1993). The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Res. Rev. 18, 247 – 291.
- Robson S., Wood B. (2008). Hominin life history: reconstruction and evolution. J. Anat. 212, 394 – 425. doi:10.1111/j.1469-7580.2008.00867.x
- Romero L. M., Dickens M. J., Cyr N. E. (2009). The reactive scope model – a new model integrating homeostasis, allostasis, and stress. Horm. Behav. 55, 375 – 389.
- Roozendaal B. (2000). Glucocorticoids and the regulation of memory consolidation. Psychoneuroendocrinology 25, 213 – 238. doi:10.1016/S0306-4530(99)00058-X
- Roozendaal B., Brunson K. L., Holloway B. L., McGaugh J. L., Baram T. Z. (2002). Involvement of stress-released corticotropin-releasing hormone in the basolateral amygdala in regulating memory consolidation. Proc. Natl. Acad. Sci. U.S.A. 99, 13908 – 13913.
- Roozendaal B., Carmi O., McGaugh J. L. (1996). Adrenocortical suppression blocks the memory-enhancing effects of amphetamine and epinephrine. Proc. Natl. Acad. Sci. U.S.A. 93, 1429 – 1433.
- Roozendaal B., de Quervain D. J. F., Ferry B., Setlow B., McGaugh J. L. (2001). Basolateral amygdala-nucleus accumbens interactions in mediating glucocorticoid enhancement of memory consolidation. J. Neurosci. 21, 2518 – 2525.
- Ruscio M. G., Sweeny T., Hazelton J., Suppatkul P., Carter C. S. (2007). Social environment regulates corticotropin releasing factor, corticosterone and vasopressin in juvenile prairie voles. Horm. Behav. 51, 54 – 61.
- Ryff C. D., Singer B. H., Dienberg Love G. (2004). Positive health: connecting well-being with biology. Philos. R. Soc. Lond. B Biol. Sci. 359, 1386 – 1394.
- Saltzman W., Schultz-Darken N. J., Scheffler G., Wegner F. H., Abbott D. H. (1994). Social and cooperative influences on plasma cortisol in female marmoset monkeys. Physiol. Behav. 56, 801 – 819.
- Saltzman W., Schultz-Darken N. J., Wegner F. H., Wittwer D. J., Abbott D. H. (1998). Suppression of cortisol levels in subordinate female marmosets: reproductive and social contributions. Horm. Behav. 33, 58 – 74.
- Sapolsky R. M. (1990). Adrenocortical function, social rank, and personality among wild baboons. Biol. Psychiatry 28, 862 – 878.
- Sapolsky R. M. (1992). Stress: The Aging Brain and the Mechanisms of Neuron Death. Cambridge: MIT Press.
- Sapolsky R. M. (1995). Social subordinance as a marker of hypercortisolism. Some unexpected subtleties. Ann. N. Y. Acad. Sci. 771, 626 – 639.
- Sapolsky R. J., Romero M., Munck A. U. (2000). How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr. Rev. 21, 55 – 89.
- Schnorpfeil P., Noll A., Schulze R., Ehlert U., Frey K., Fischer J. W. (2003). Allostatic load and work conditions. Soc. Sci. Med. 57, 647 – 656.
- Schulkin J. (1999). The Neuroendocrine Regulation of Behavior. Cambridge: Cambridge University Press.
- Schulkin J. (2003). Rethinking Homeostasis. Cambridge: MIT Press.
- Schulkin J., Gold P. W., McEwen B. S. (1998). Induction of corticotropin-releasing hormone gene expression by glucocorticoids. Psychoneuronedocrinology 23, 219 – 243. doi:10.1016/S0306-4530(97)00099-1
- Seeman T. E., McEwen B. S., Rowe J. W., Singer B. H. (2001). Allostatic load as a marker of cumulative biological risk: MacArthur studies of successful aging. Proc. Natl. Acad. Sci.U.S.A. 98, 470 – 475.
- Selye H. (1956). The Stress of Life. New York: McGraw-Hill.
- Shepard J. D., Barron K. W., Myers D. A. (2000). Corticosterone delivery to the amygdala increases corticotropin-releasing hormone mRNA in the central nucleus of the amygdala and anxiety-like behavior. Brain Res. 851, 288 – 295. doi:10.1016/S0006-8993(00)02019-9
- Singer B., Ryff C. D. (1999). Hierarchies of life histories and associated health risks. Ann. N. Y. Acad. Sci. 896, 96 – 115.
- Steptoe A., Feldman P. J., Kunz S., Owen N., Willemsen G., Marmot M. (2002). Stress responsivity and socioeconomic status: a mechanism for increased cardiovascular disease risk? Eur. Heart J. 23, 1757 – 1763. doi:10.1053/euhj.2001.3233
- Steptoe A., Owen N., Kunz-Ebrecht S. R., Brydon L. (2004). Loneliness and neuroendocrine, cardiovascular, and inflammatory stress responses in middle-aged men and women. Psychoneuroendocrinology 29, 593 – 611. doi:10.1016/S0306-4530(03)00086-6
- Sterling P. (2004). “Principles of allostasis: optimal design, predictive regulation, psychopathology and rational therapeutics,” in Allostasis, Homeostasis and the Costs of Physiological Adaptation, ed. Schulkin J. (Cambridge: Cambridge University Press), 17 – 64.
- Sterling P., Eyer J. (1988). “Allostasis: a new paradigm to explain arousal pathology,” in Handbook of Life Stress, Cognition, and Health, eds Fisher S., Reason J. (New York: John Wiley and Sons), 629 – 649.
- Strand F. L. (1999). Neuropeptides: Regulators of Physiological Processes. Cambridge, MA: MIT Press.
- Stringer C. B., Andrews P. (1988). Genetic and fossil evidence for the origin of modern humans. Science 239, 1263 – 1268. doi:10.1126/science.3125610
- Swanson L. W. (2000). The cerebral hemisphere regulation of motivated behavior. Brain Res. 836, 113 – 164. doi:10.1016/S0006-8993(00)02905-X
- Swanson L. W., Simmons D. M. (1989). Differential steroid hormone and neural influences on peptide mRNA levels in CRH cells of the paraventricular nucleus: a hybridization histochemical study in the rat. J. Comp. Neurol. 285, 413 – 435.
- Szanton S. L., Gill J. M., Allen J. K. (2005). Allostatic load: a mechanism of socioeconomic health disparities. Biol. Res. Nurs. 7, 7 – 15.
- Tannenbaum B., Tannenbaum G. S., Sudom K., Anisman H. (2002). Neurochemical and behavioral alterations elicited by a chronic intermittent stressor regimen: implications for allostatic load. Brain Res. 953, 82 – 92. doi:10.1016/S0006-8993(02)03273-0
- Taylor S. E., Klein L. T., Lewis B. P., Gruenwald T. L., Gurung R. A., Updegraff J. A. (2000). Biobehavioral responses to stress in females: tend and befriend, not fight or flight. Psychol. Rev. 107, 411 – 429.
- Thompson B. L., Erickson K., Schulkin J., Rosen J. B. (2004). Corticosterone facilitates retention of contextual fear conditioning and increases CRH mRNA expression in the amygdala. Behav. Brain Res. 149, 209 – 215.
- Toates F. (1986). Motivational Systems. Cambridge: Cambridge University Press.
- Tomasello M. (1999). The Cultural Origins of Human Cognition. Cambridge, MA: Harvard University Press.
- Tomasello M., Kruger A. C., Ratner H. H. (1993). Cultural learning. Behav. Brain Sci. 16, 495 – 552. doi:10.1017/S0140525X0003123X
- Valentino R. J., Foote S. L., Page M. E. (1993). The locus coeruleus as a site for integrating corticotropin-releasing factor and noradrenergic mediation of stress responses. Ann. N. Y. Acad. Sci. 697, 173 – 188.
- Van Cauter E., Spiegel K. (1999). Sleep as a mediator of the relationship between socioeconomic status and health: a hypothesis. Ann. N.Y. Acad. Sci. 896, 254 – 261.
- von Kanel R., Dimsdale J. E., Patterson T. L., Grant I. (2003). Acute procoagulant stress response as a dynamic measure of allostatic load in Alzheimer caregivers. Ann. Behav. Med. 26, 42 – 48.
- Watts A. G., Sanchez-Watts G. (1995). Region-specific regulation of neuropeptide mRNAs in rat limbic forebrain neurons by aldosterone and corticosterone. J. Physiol. (Lond.) 484, 721 – 736.
- Weaver I. C., Cervoni N., Champagne F. A., D'Alessio A. C., Sharma S., Seckl J. R., Dymov S., Szyf M., Meaney M. J. (2004). Epigenetic programming by maternal behavior. Nat. Neurosci. 7, 847 – 854.
- Weinstein M., Goldman N., Hedley A., Yu-Hsuan L., Seeman T. (2003). Social linkages to biological markers of health among the elderly. J. Biosoc. Sci. 35, 433 – 453.
- Weiss J. M. (1970). Somatic effects of predictable and unpredictable shock. Psychosom. Med. 32, 397 – 408.
- Wingfield J. C. (2004). “Allostatic load and life cycles: implication for neuroendocrine control mechanisms,” in Allostasis, Homeostasis and the Costs of Physiological Adaptation, ed. Schulkin J. (Cambridge: Cambridge University Press), 302 – 342.
- Wingfield J. C., Jacobs J. D., Soma K., Maney D. L., Hunt K., Wisti-Peterson D., Meddle S., Ramenofsky M., Sullivan K. (1999). “Testosterone, aggression and communication: ecological bases of endocrine phenomenona,” in The design of animal communication, eds Hauser M. D., Konishi M. (Cambridge: Cambridge University Press), 196 – 209.
- Wingfield J. C., Romero L. M. (2001). “Adrenocortical responses to stress and their modulation in free-living vertebrates,” in Coping with the Environment: Neural and Endocrine Mechanisms, ed. McEwen B. S. (Oxford: Oxford University Press), 211 – 234.
- Wood B. (1992). Origin and evolution of the genus homo. Nature 355, 783 – 790. doi:10.1038/355783a0
- Yao M., Schulkin J., Denver R. J. (2008). Evolutionary conserved glucocorticoid regulation of CRH. Endorcinology 149, 2352 – 2360. doi:10.1210/en.2007-1551
Citation
Schulkin, J. (2011). Social Allostasis: Anticipatory Regulation of the Internal Milieu. Frontiers in Evolutionary Neuroscience, Volume 2. https://doi.org/
- Received
- Accepted
- Published
- Volume
- 2 - 2011
Copyright
Copyright © 2011 Schulkin.
License: http://www.frontiersin.org/licenseagreement
*Correspondence: Jay Schulkin
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