Not all stressors are equal: Early social enrichment favors resilience to social but not physical stress in male mice

Hormones and Behavior

Volumn 63, Issue 3, 2013, Pages 503-509

  Branchi, Igor ^a   Santarelli, Sara ^a   D'Andrea, Ivana ^b   Alleva, Enrico ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^b IRCCS NEUROMED   (Italy)

Author keywords

Behavior; Communal nesting; Corticosterone; Early experiences; Match mismatch hypothesis; Physical; Social; Stress; Stress quality

Indexed keywords

CORTICOSTERONE;

ANHEDONIA; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; COPING BEHAVIOR; CORTICOSTERONE BLOOD LEVEL; EARLY LIFE STRESS; ENVIRONMENTAL ENRICHMENT; EXPERIENCE; FEMALE; FORCED SWIMMING TEST; MALE; MOUSE; NONHUMAN; PHYSICAL STRESS; PRIORITY JOURNAL; QUALITATIVE ANALYSIS; REARING; SOCIAL ENVIRONMENT; SOCIAL STRESS; WEANING;

ANHEDONIA; ANIMALS; ANIMALS, NEWBORN; CORTICOSTERONE; FEMALE; MALE; MATERNAL BEHAVIOR; MICE; MICE, INBRED C57BL; NESTING BEHAVIOR; NEUROPSYCHOLOGICAL TESTS; SOCIAL BEHAVIOR; SOCIAL ENVIRONMENT; STRESS, PSYCHOLOGICAL;

EID: 84875052176     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2013.01.003     Document Type: Article

References (62)

1. Bateson P., et al. Developmental plasticity and human health. Nature 2004, 430:419-421.
2. Benus R.F., Henkelmann C. Litter composition influences the development of aggression and behavioural strategy in male Mus domesticus. Behaviour 1998, 135:1229-1249.
3. Berman C.M., et al. Group size, infant development and social networks in free-ranging rhesus monkeys. Anim. Behav. 1997, 53:405-421.
4. Branchi I. The mouse communal nest: investigating the epigenetic influences of the early social environment on brain and behavior development. Neurosci. Biobehav. Rev. 2009, 33:551-559.
5. Branchi I., et al. Early social enrichment shapes social behavior and nerve growth factor and brain-derived neurotrophic factor levels in the adult mouse brain. Biol. Psychiatry 2006, 60:690-696.
6. Branchi I., et al. Shaping brain development: mouse communal nesting blunts adult neuroendocrine and behavioral response to social stress and modifies chronic antidepressant treatment outcome. Psychoneuroendocrinology 2010, 35:743-751.
7. Branchi, I., et al., in press. Early interactions with mother and peers independently build adult social skills and shape BDNF and oxytocin receptor brain levels. Psychoneuroendocrinology. http://dx.doi.org/10.1016/j.psyneuen.2012.07.010.
8. Caldji C., et al. Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:5335-5340.
9. Champagne F.A., Curley J.P. How social experiences influence the brain. Curr. Opin. Neurobiol. 2005, 15:704-709.
10. Champagne F.A., Meaney M.J. Stress during gestation alters postpartum maternal care and the development of the offspring in a rodent model. Biol. Psychiatry 2006, 59:1227-1235.
11. Cirulli F., et al. Early disruption of the mother-infant relationship: effects on brain plasticity and implications for psychopathology. Neurosci. Biobehav. Rev. 2003, 27:73-82.
12. Cirulli F., et al. Changes in plasma levels of BDNF and NGF reveal a gender-selective vulnerability to early adversity in rhesus macaques. Psychoneuroendocrinology 2009, 34:172-180.
13. Cirulli F., et al. Early life influences on emotional reactivity: evidence that social enrichment has greater effects than handling on anxiety-like behaviors, neuroendocrine responses to stress and central BDNF levels. Neurosci. Biobehav. Rev. 2010, 34:808-820.
14. Cohen J. A power primer. Psychol. Bull. 1992, 112:155-159.
15. Cohen S., et al. Psychological stress and disease. JAMA 2007, 298:1685-1687.
16. D'Andrea I., et al. Communal nesting, an early social enrichment, affects social competences but not learning and memory abilities at adulthood. Behav. Brain Res. 2007, 183:60-66.
17. de Kloet E.R., et al. Stress, genes and the mechanism of programming the brain for later life. Neurosci. Biobehav. Rev. 2005, 29:271-281.
18. Denenberg V.H. Critical periods, stimulus input, and emotional reactivity: a theory of infantile stimulation. Psychol. Rev. 1964, 71:335-351.
19. Giachino C., et al. Maternal deprivation and early handling affect density of calcium binding protein-containing neurons in selected brain regions and emotional behavior in periadolescent rats. Neuroscience 2007, 145:568-578.
20. Gluckman P.D., Hanson M.A. Living with the past: evolution, development, and patterns of disease. Science 2004, 305:1733-1736.
21. Gluckman P.D., et al. Environmental influences during development and their later consequences for health and disease: implications for the interpretation of empirical studies. Proc. Biol. Sci. 2005, 272:671-677.
22. Godfrey K.M., Barker D.J. Fetal programming and adult health. Public Health Nutr. 2001, 4:611-624.
23. Godfrey K.M., et al. Epigenetic mechanisms and the mismatch concept of the developmental origins of health and disease. Pediatr. Res. 2007, 61:5R-10R.
24. Greenough W.T., et al. Experience and brain development. Child Dev. 1987, 58:539-559.
25. Hall F.S., et al. Effects of isolation-rearing on voluntary consumption of ethanol, sucrose and saccharin solutions in Fawn Hooded and Wistar rats. Psychopharmacology (Berl) 1998, 139:210-216.
26. Harlow H.F. Agemate or peer affectional system. Advances in the Study of Behavior 1969, Academic Press, New York. D.S. Lehrman (Ed.).
27. Harlow H.F., Suomi S.J. Social recovery by isolation-reared monkeys. Proc. Natl. Acad. Sci. U. S. A. 1971, 68:1534-1538.
28. Heim C., Nemeroff C.B. The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies. Biol. Psychiatry 2001, 49:1023-1039.
29. Heim C., et al. Effect of childhood trauma on adult depression and neuroendocrine function: sex-specific moderation by CRH receptor 1 gene. Front. Behav. Neurosci. 2009, 3:41.
30. Holsboer F. The corticosteroid receptor hypothesis of depression. Neuropsychopharmacology 2000, 23:477-501.
31. Hudson R. The contribution of sibling relations to the emergence of individual behavioural phenotypes. International Conference of Ethology, Budapest 2005, 6.
32. Ising M., Holsboer F. Genetics of stress response and stress-related disorders. Dialogues Clin. Neurosci. 2006, 8:433-444.
33. Ising M., et al. Combined dexamethasone/corticotropin releasing hormone test predicts treatment response in major depression - a potential biomarker?. Biol. Psychiatry 2007, 62:47-54.
34. Kendler K.S., et al. Stressful life events, genetic liability, and onset of an episode of major depression in women. Am. J. Psychiatry 1995, 152:833-842.
35. Kertes D.A., et al. Inhibited temperament and parent emotional availability differentially predict young children's cortisol responses to novel social and nonsocial events. Dev. Psychobiol. 2009, 51:521-532.
36. Knapska E., et al. Differential involvement of the central amygdala in appetitive versus aversive learning. Learn. Mem. 2006, 13:192-200.
37. Laviola G., Alleva E. Sibling effects on the behavior of infant mouse litters (Mus domesticus). J. Comp. Psychol. 1995, 109:68-75.
38. Levine S. Infantile experience and resistance to physiological stress. Science 1957, 126:405.
39. Levine S. Developmental determinants of sensitivity and resistance to stress. Psychoneuroendocrinology 2005, 30:939-946.
40. Liu D., et al. Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 1997, 277:1659-1662.
41. Lupien S.J., et al. Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat. Rev. Neurosci. 2009, 10:434-445.
42. Macrì S., Wurbel H. Developmental plasticity of HPA and fear responses in rats: a critical review of the maternal mediation hypothesis. Horm. Behav. 2006, 50:667-680.
43. Macrì S., et al. Dissociation in the effects of neonatal maternal separations on maternal care and the offspring's HPA and fear responses in rats. Eur. J. Neurosci. 2004, 20:1017-1024.
44. Macrì S., et al. Abnormal behavioral and neurotrophic development in the younger sibling receiving less maternal care in a communal nursing paradigm in rats. Psychoneuroendocrinology 2010, 35:392-402.
45. Meaney M.J. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu. Rev. Neurosci. 2001, 24:1161-1192.
46. Mechan A.O., et al. A comparison of learning and memory characteristics of young and middle-aged wild-type mice in the IntelliCage. J. Neurosci. Methods. 2009, 180:43-51.
47. Nemeroff C.B., et al. Elevated concentrations of CSF corticotropin-releasing factor-like immunoreactivity in depressed patients. Science 1984, 226:1342-1344.
48. Oitzl M.S., et al. Brain development under stress: hypotheses of glucocorticoid actions revisited. Neurosci. Biobehav. Rev. 2010, 34:853-866.
49. Pryce C.R., et al. Long-term effects of early-life environmental manipulations in rodents and primates: potential animal models in depression research. Neurosci. Biobehav. Rev. 2005, 29:649-674.
50. Repetti R., et al. Risky families: family social environments and the mental and physical health of offspring. Psychol. Bull. 2002, 128:330-366.
51. Rijsdijk F.V., et al. Genetic and environmental influences on psychological distress in the population: General Health Questionnaire analyses in UK twins. Psychol. Med. 2003, 33:793-801.
52. Rochefort C., et al. Enriched odor exposure increases the number of newborn neurons in the adult olfactory bulb and improves odor memory. J. Neurosci. 2002, 22:2679-2689.
53. Schmidt M.V. Animal models for depression and the mismatch hypothesis of disease. Psychoneuroendocrinology 2011, 36:330-338.
54. Southwick S.M., Charney D.S. The science of resilience: implications for the prevention and treatment of depression. Science 2012, 338:79-82.
55. Suomi S.J. Peers, play and primary prevention in primates. Primary Prevention of Psychopathology: Social Competence In Children 1979, 127-149. Press of New England, Hanover, NH. M. Kent, J. Rolf (Eds.).
56. Suomi S.J. Mother-infant attachment, peer relationships, and the development of social networks in rhesus monkeys. Hum. Dev. 2005, 48:67-79.
57. Taylor S.E., et al. Early environment, emotions, responses to stress, and health. J. Pers. 2004, 72:1365-1393.
58. Terranova M.L., Laviola G. Individual differences in mouse behavioural development: effects of precocious weaning and ongoing sexual segregation. Anim. Behav. 1995, 50:1261-1271.
59. Van den Berg C.L., et al. Morphine attenuates the effects of juvenile isolation in rats. Neuropharmacology 2000, 39:969-976.
60. von Senden M. Space and Sight: The Perception of Space and Shape in the Congenitally Blind Before and After Operation 1960, Free Press, Glencoe, IL.
61. Weinberg J., et al. Early handling effects on neophobia and conditioned taste aversion. Physiol. Behav. 1978, 20:589-596.
62. Yang M., et al. Social peers rescue autism-relevant sociability deficits in adolescent mice. Autism Res. 2011, 4:17-27.