Evaluating the behavioural consequences of early maternal separation in adult C57BL/6 mice; the importance of time

Behavioural Brain Research

Volumn 207, Issue 2, 2010, Pages 332-342

  van Heerden, Johan H ^a   Russell, Vivienne ^a   Korff, Ane ^a   Stein, Dan J ^a   Illing, Nicola ^a  

^a UNIVERSITY OF CAPE TOWN   (South Africa)

Author keywords

Behaviour; Corticosterone; Elevated plus maze; Maternal separation; Mice; Open field; Stress; Time dependence

Indexed keywords

CORTICOSTERONE;

ADAPTIVE BEHAVIOR; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; BEHAVIORAL SCIENCE; BEHAVIORAL STRESS; C57BL 6 MOUSE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; EXPLORATORY BEHAVIOR; FEMALE; HORMONE RESPONSE; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMMOBILIZATION STRESS; MALE; MATERNAL DEPRIVATION; MAZE TEST; MOUSE; NONHUMAN; OPEN FIELD TEST; PRIORITY JOURNAL; RISK ASSESSMENT; TIME;

AGING; ANIMALS; BEHAVIOR, ANIMAL; CORTICOSTERONE; EXPLORATORY BEHAVIOR; FEMALE; MALE; MATERNAL DEPRIVATION; MAZE LEARNING; MICE; MICE, INBRED C57BL; NEUROPSYCHOLOGICAL TESTS; RANDOM ALLOCATION; RESTRAINT, PHYSICAL; RISK-TAKING; STRESS, PSYCHOLOGICAL; TIME FACTORS;

EID: 74449085689     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2009.10.015     Document Type: Article

References (44)

1. Abel T., and Lattal K.M. Molecular mechanisms of memory acquisition, consolidation and retrieval. Curr Opin Neurobiol 11 (2001) 180-187
2. Aisa B., Tordera R., Lasheras B., Del Rio J., and Ramirez M.J. Cognitive impairment associated to HPA axis hyperactivity after maternal separation in rats. Psychoneuroendocrinology 32 (2007) 256-266
3. Alexopoulos T., and Ric F. The evaluation-behavior link: direct and beyond valence. J Exp Soc Psychol 43 (2007) 1010-1016
4. Bakshi V.P., and Kalin N. Animal models and endophenotypes of anxiety and stress disorders. In: Davis K.L., Charney D., Coyle J.T., and Nemeroff C. (Eds). Neuropsychopharmacology: the fifth generation of progress (2002), Lippincott, Williams and Wilkins, Philadelphia 445-456
5. Bertoglio L.J., and Carobrez A.P. Behavioral profile of rats submitted to session 1-session 2 in the elevated plus-maze during diurnal/nocturnal phases and under different illumination conditions. Behav Brain Res 132 (2002) 135-143
6. Buckley T.C., Blanchard E.B., and Neill W.T. Information processing and PTSD: a review of the empirical literature. Clin Psychol Rev 20 (2000) 1041-1065
7. Caldji C., Francis D., Sharma S., Plotsky P.M., and Meaney M.J. The effects of early rearing environment on the development of GABAA and central benzodiazepine receptor levels and novelty-induced fearfulness in the rat. Neuropsychopharmacology 22 (2000) 219-229
8. Carobrez A.P., and Bertoglio L.J. Ethological and temporal analyses of anxiety-like behavior: the elevated plus-maze model 20 years on. Neurosci Biobehav Rev 29 (2005) 1193-1205
9. Carola V., D'Olimpio F., Brunamonti E., Mangia F., and Renzi P. Evaluation of the elevated plus-maze and open-field tests for the assessment of anxiety-related behaviour in inbred mice. Behav Brain Res 134 (2002) 49-57
10. Choleris E., Thomas A.W., Kavaliers M., and Prato F.S. A detailed ethological analysis of the mouse open field test: effects of diazepam, chlordiazepoxide and an extremely low frequency pulsed magnetic field. Neurosci Biobehav Rev 25 (2001) 235-260
11. Crabbe J.C., Wahlsten D., and Dudek B.C. Genetics of mouse behavior: interactions with laboratory environment. Science 284 (1999) 1670-1672
12. Cryan J.F., and Holmes A. The ascent of mouse: advances in modelling human depression and anxiety. Nat Rev Drug Discov 4 (2005) 775-790
13. Dalm S., Enthoven L., Meijer O.C., et al. Age-related changes in hypothalamic-pituitary-adrenal axis activity of male C57BL/6J mice. Neuroendocrinology 81 (2005) 372-380
14. Daniels W.M., Pietersen C.Y., Carstens M.E., and Stein D.J. Maternal separation in rats leads to anxiety-like behavior and a blunted ACTH response and altered neurotransmitter levels in response to a subsequent stressor. Metab Brain Dis 19 (2004) 3-14
15. Fabricius K., Wortwein G., and Pakkenberg B. The impact of maternal separation on adult mouse behaviour and on the total neuron number in the mouse hippocampus. Brain Struct Funct 212 (2008) 403-416
16. Fernandez Espejo E. Structure of the mouse behaviour on the elevated plus-maze test of anxiety. Behav Brain Res 86 (1997) 105-112
17. Gutman D.A., and Nemeroff C.B. Persistent central nervous system effects of an adverse early environment: clinical and preclinical studies. Physiol Behav 79 (2003) 471-478
18. Heim C., and Nemeroff C.B. The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies. Biol Psychiatry 49 (2001) 1023-1039
19. Kalueff A.V., and Tuohimaa P. Mouse grooming microstructure is a reliable anxiety marker bidirectionally sensitive to GABAergic drugs. Eur J Pharmacol 508 (2005) 147-153
20. Korte S.M., and De Boer S.F. A robust animal model of state anxiety: fear-potentiated behaviour in the elevated plus-maze. Eur J Pharmacol 463 (2003) 163-175
21. Kuhn C., and Schanberg S. Responses to maternal separation: mechanisms and mediators. Int J Dev Neurosci 16 (1998) 10
22. LaBar K.S., and Cabeza R. Cognitive neuroscience of emotional memory. Nat Rev Neurosci 7 (2006) 54-64
23. Mardia K.V., Kent J.T., and Bibby J.M. Multivariate analysis (1979), Academic Press, London
24. Mauchly J.W. Significance test for sphericity of a normal n-variate distribution. Ann Math Stat 11 (1940) 204-209
25. McGowan P.O., Sasaki A., D'Alessio A.C., et al. Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat Neurosci 12 (2009) 342-348
26. Meaney M.J. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu Rev Neurosci 24 (2001) 1161-1192
27. Meaney M.J., and Szyf M. Maternal care as a model for experience-dependent chromatin plasticity?. Trends Neurosci 28 (2005) 456-463
28. Millstein R.A., and Holmes A. Effects of repeated maternal separation on anxiety- and depression-related phenotypes in different mouse strains. Neurosci Biobehav Rev 31 (2007) 3-17
29. Parfitt D.B., Levin J.K., Saltstein K.P., Klayman A.S., Greer L.M., and Helmreich D.L. Differential early rearing environments can accentuate or attenuate the responses to stress in male C57BL/6 mice. Brain Res 1016 (2004) 111-118
30. Parfitt D.B., Walton J.R., Corriveau E.A., and Helmreich D.L. Early life stress effects on adult stress-induced corticosterone secretion and anxiety-like behavior in the C57BL/6 mouse are not as robust as initially thought. Horm Behav 52 (2007) 417-426
31. Pickering C., Gustafsson L., Cebere A., Nylander I., and Liljequist S. Repeated maternal separation of male Wistar rats alters glutamate receptor expression in the hippocampus but not the prefrontal cortex. Brain Res 1099 (2006) 101-108
32. Ramos A. Animal models of anxiety: do I need multiple tests?. Trends Pharmacol Sci 29 (2008) 493-498
33. Rice C.J., Sandman C.A., Lenjavi M.R., and Baram T.Z. A novel mouse model for acute and long-lasting consequences of early life stress. Endrocrinology 149 (2008) 4892-4900
34. Rodgers R., Cao B., Dalvi A., and Holmes A. Animal models of anxiety: an ethological perspective. Braz J Med Biol Res 30 (1997) 16
35. Rodgers R.J., and Dalvi A. Anxiety, defence and the elevated plus-maze. Neurosci Biobehav Rev 21 (1997) 801-810
36. Rodgers R.J., and Johnson N.J.T. Factor analysis of spatiotemporal and ethological measures in the murine elevated plus-maze test of anxiety. Pharmacol Biochem Behav 52 (1995) 297-303
37. Rodgers R.J., Johnson N.J.T., Cole J.C., Dewar C.V., Kidd G.R., and Kimpson P.H. Plus-maze retest profile in mice: importance of initial stages of trial 1 and response to post-trial cholinergic receptor blockade. Pharmacol Biochem Behav 54 (1996) 41-50
38. Romeo R., Mueller A., Sisti H., Ogawa S., McEwen B., and Brake W. Anxiety and fear behavior in adult male and female C57BL/6 mice are modulated by maternal separation. Horm Behav 43 (2003) 7
39. Sanchez M.M., Ladd C.O., and Plotsky P.M. Early adverse experience as a developmental risk factor for later psychopathology: evidence from rodent and primate models. Dev Psychopathol 13 (2001) 419-449
40. Schmidt M., Oitzl M.S., Levine S., and de Kloet E.R. The HPA system during the postnatal development of CD1 mice and the effects of maternal deprivation. Dev Brain Res 139 (2002) 39-49
41. Stern C.A.J., Carobrez A.P., and Bertoglio L.J. Aversive learning as a mechanism for lack of repeated anxiolytic-like effect in the elevated plus-maze. Pharmacol Biochem Behav 90 (2008) 545-550
42. van Heerden J., Conesa A., Stein D., Montaner D., Russell V., and Illing N. Parallel changes in gene expression in peripheral blood mononuclear cells and the brain after maternal separation in the mouse. BMC Res Notes 2 (2009) 195
43. Veenema A.H., Bredewold R., and Neumann I.D. Opposite effects of maternal separation on intermale and maternal aggression in C57BL/6 mice: link to hypothalamic vasopressin and oxytocin immunoreactivity. Psychoneuroendocrinology 32 (2007) 437-450
44. Ziegler D.R., and Herman J.P. Neurocircuitry of stress integration: anatomical pathways regulating the hypothalamo-pituitary-adrenocortical axis of the rat. Integr Comp Biol 42 (2002) 541-551