Variations in the postnatal maternal environment in mice: Effects on maternal behaviour and behavioural and endocrine responses in the adult offspring

Physiology and Behavior

Volumn 93, Issue 1-2, 2008, Pages 395-407

  Coutellier, Laurence ^a   Friedrich, Anne Christin ^a   Failing, Klaus ^a   Würbel, Hanno ^a  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

C57BL 6; Fearfulness; HPA axis; Maternal care; Mice; Postnatal manipulations; Rodents; Social behaviour; Stress reactivity

Indexed keywords

CORTICOSTERONE;

ADAPTATION; ADAPTIVE BEHAVIOR; ANIMAL; ARTICLE; BLOOD; C57BL MOUSE; COMPARATIVE STUDY; ENVIRONMENT; EXPLORATORY BEHAVIOR; FEMALE; MATERNAL BEHAVIOR; MENTAL STRESS; MOUSE; NONPARAMETRIC TEST; PHYSIOLOGY; PSYCHOLOGICAL ASPECT; SEX DIFFERENCE; SOCIAL BEHAVIOR; SOCIAL ENVIRONMENT;

ADAPTATION, PHYSIOLOGICAL; ADAPTATION, PSYCHOLOGICAL; ANIMALS; CORTICOSTERONE; ENVIRONMENT; EXPLORATORY BEHAVIOR; FEMALE; MATERNAL BEHAVIOR; MICE; MICE, INBRED C57BL; SEX FACTORS; SOCIAL BEHAVIOR; SOCIAL ENVIRONMENT; STATISTICS, NONPARAMETRIC; STRESS, PSYCHOLOGICAL;

EID: 42449148868     PISSN: 00319384     EISSN: 1873507X     Source Type: Journal    
DOI: 10.1016/j.physbeh.2007.09.008     Document Type: Article

References (52)

1. Levine S, Alpert M, Lewis GW. Infantile experience and the maturation of the pituitary adrenal axis. Science 1957;126:1347.
2. Laviola G, Terranova ML. The developmental psychobiology of behavioural plasticity in mice: the role of social experiences in the family unit. Neurosci Biobehav Rev 1998;23:197-213.
3. Holmes A, le Guisquet AM, Vogel E, Millstein RA, Leman S, Belzung C. Early life genetic, epigenetic and environmental factors shaping emotionality in rodents. Neurosci Biobehav Rev 2005;29:1335-46.
4. Mintz M, Rüedi-Bettschen D, Feldon J, Pryce CR. Early social and physical deprivation leads to reduced social motivation in adulthood in Wistar rats. Behav Brain Res 2005;156:311-20.
5. Branchi I, D'Andrea I, Fiore M, Di Fausto V, Aloe L, Alleva E. Early social enrichment shapes social behavior and nerve growth factor and brain-derived neurotrophic factor levels in the adult mouse brain. Biol Psychiatry 2006;60:690-6.
6. Caldji C, Tannenbaum B, Sharma S, Francis D, Plotsky PM, Meaney MJ. Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat. Proc Natl Acad Sci 1998;95:5335-40.
7. Meaney MJ. Maternal care, gene expression and the transmission of individual differences in stress across generations. Annu Rev Neurosci 2001;24:1161-92.
8. Cirulli F, Berry A, Alleva E. Early disruption of the mother-infant relationship: effects on brain plasticity and implications for psychopathology. Neurosci Biobehav Rev 2003;27:73-82.
9. Parfitt DB, Levin JK, Salstein KP, Klayman AS, Gree LM, Helmreich DL. Differential early rearing environments can accentuate or attenuate the responses to stress in male C57BL/6mice. Brain Res 2004;1016: 111-1118.
10. Macri S, Mason GJ, Würbel H. 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;20:1017-24.
11. Denenberg VH, Ottinger DR, Stephens MW. Effects of maternal factors upon growth and behavior of the rat. Child Dev 1962;33:65-71.
12. Liu D, Diorio J, Tannenbaum B, Caldji C, Francis D, Freedman A, et al. Maternal care, hippocampal glucocorticoid receptors and hypothalamic- pituitary-adrenal responses to stress. Science 1997;277:1659-61.
13. Macri S, Laviola G. Single episode of maternal deprivation and adult depressive profile in mice: interaction with cannabinoid exposure during adolescence. Behav Brain Res 2004;154:231-8.
14. McLeod J, Sinal CJ, Perrot-Sinal TS. Evidence for non-genomic transmission of ecological information via maternal behavior in female rats. Genes Brain Behav 2007;6:19-29.
15. Léonhardt M, Matthews SG, Meaney MJ, Walker CD. Psychological stressors as a model of maternal adversity: diurnal modulation of corticosterone responses and changes in maternal behaviour. Horm Behav 2007;51:77-88.
16. Macri S, Würbel H. Effects of variation in postnatal maternal environment on maternal behaviour and fear and stress responses in rats. Anim Behav 2007;73(1):171-84.
17. Francis DD, Meaney MJ. Maternal care and the development of stress response. Curr Opin Neurobiol 1999;9:128-34.
18. Pryce CR, Feldon J. Long-term neurobehavioural impact of the postnatal environment in rats: manipulations, effects and mediating mechanisms. Neurosci Biobehav Rev 2003;27:57-71.
19. Schmidt M, Oitzl MS, Levine S, de Kloet ER. The HPA system during the postnatal development of CD1 mice and the effects of maternal deprivation. Dev Brain Res 2002;139:39-49.
20. Romeo RD, Mueller A, Sisti HM, Ogawa S, McEwen BS, Brake WG. Anxiety and fear in adult male and female C57BL/6 mice are modulated by maternal separation. Horm Behav 2003;43:561-7.
21. Moles A, Rizzi R, D'Amato FR. Postnatal stress in mice: does "stressing" the mother have the same effect as "stressing" the pups. Dev Psychobiol 2004;44:230-7.
22. Zaharia MD, Kulczycki J, Shanks N, Meaney MJ, Anisman H. The effects of early postnatal stimulation on Morris water-maze acquisition in adult mice: genetic and maternal factors. Psychopharmacologia 1996;128: 227-39.
23. Gariépy JL, Rodriguiz RM, Jones BC. Handling, genetic and housing effects on the mouse stress system, dopamine function, and behaviour. Pharmacol Biochem Behav 2002;73:7-17.
24. Millstein RA, Holmes A. Effects of repeated maternal separation on anxiety- and depression-related phenotypes in different mouse strains. Neurosci Biobehav Rev 2007;31:3-17.
25. Macri S, Würbel H. Developmental plasticity of HPA and fear responses in rats: a critical review of the maternal mediation hypothesis. Horm Behav 2006;50(5):667-80.
26. Shoji H, Kato K. Maternal behavior of primiparous females in inbred strains of mice: a detailed descriptive analysis. Physiol Behav 2006;89:320-8.
27. Champagne FA, Francis DD, Mar A, Meaney MJ. Variations in maternal care in the rat as a mediating influence for the effects of environment on development. Physiol Behav 2003;79:359-71.
28. Dürschlag M, Würbel H, Stauffacher M, Von Holst D. Repeated blood collection in the laboratory mouse by tail incision-modification of an old technique. Physiol Behav 1996;60:1565-8.
29. Marashi V, Barnekow A, Ossendorf E, Sachser N. Effects of different forms of environmental enrichment on behavioral, endocrinological, and immunological parameters in male mice. Horm Behav 2003;43:281-92.
30. Madini R, Wolfer DP. Elevated null-maze. EMBO/FENS Course Mouse Transgenics and Behaviour. Protocols for demonstrationZurich; 2001. p. 25.1.
31. Pellow S, Chopin P, File SE, Briley M. Validation of open:close arm entries in an elevated plus-maze as a measure of anxiety in the rat. J Neurosci Methods 1985;14:149-67.
32. Sheperd JK, Grewal SS, Fletcher A, Bill DJ, Dourish CT. Behavioural and pharmacological characterisation of the elevated "zero-maze" as an animal model of anxiety. Psychopharmacologia 1994;116:56-64.
33. HallCS. Emotional behavior in the rat. I.Defaecation and urination asmeasures of individual differences in emotionality. J Comp Psychol 1934;18:385-403.
34. Hall CS. Emotional behavior in the rat. III. The relationship between emotionality and ambulatory behaviour. J Comp Psychol 1936;22:345-52.
35. Choleris E, Thomas AW, Kavaliers M, Prato FS. 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 2001;25:253-60.
36. Hughes RN. Behaviour of male and female rats with a free choice of two environments differing in novelty. Anim Behav 1968;16:92-6.
37. Misslin R, Ropartz P. Effects of metamphetamine on novelty-seeking behaviour by mice. Psychopharmacologia 1981;75:39-43.
38. Dixon WJ. BMDP Statistical Software Manual, Volume 1 and 2. Berkeley, Los Angeles: University of California Press; 1993. p. 1311-52.
39. Denenberg VH. Commentary: is maternal stimulation the mediator of the handling effect in infancy?. Dev Psychobiol 1998;34:1-3.
40. Pryce CR, Bettschen D, Feldon J. Comparison of the effects of early handling and early deprivation on maternal care in the rat. Dev Psychobiol 2001;38:239-51.
41. File SE. Factors controlling measures of anxiety and responses to novelty in the mouse. Behav Brain Res 2001;125:151-7.
42. Catalani A, Casolini P, Scaccianoce S, Patacchioli FR, Spinozzi P, Angelucci L. Maternal corticosterone during the lactation paremanently affects brain corticosteroid receptors, stress response and behaviour in rat progeny. Neuroscience 2002;100(2):319-25.
43. Touma C, Palme R, Sachser N. Analyzing corticosterone metabolites in fecal samples of mice: a noninvasive technique to monitor stress hormones. Horm Behav 2004;45(1):10-22.
44. Barnett SA. The rat: a study in behavior. Chicago: University of Chicago Press; 1975.
45. Schradin C, Pillay N. The Striped Mouse (Rhabdomys pumilio) from the Succulent Karoo, South Africa: a territorial group-living solitary forager with communal breeding and helpers at the nest. J Comp Psychol 2004;118:37-47.
46. Moriceau S, Sullivan RM. Maternal presence serves as a switch between learning fear and attraction in infancy. Nature Neurosci 2006;9:1004-6.
47. Cirulli F, Capone F, Bonsignore LT, Aloe L, Alleva E. Early behavioural enrichment in the form of handling renders mouse pups unresponsive to anxiolytic drugs and increases NGF levels in the hippocampus. Behav Brain Res 2007;178:208-15.
48. Calatayud F, Coubard S, Belzung C. Emotional reactivity in mice may not be inherited but influenced by parents. Physiol Behav 2004;80:465-74.
49. Priebe K, Brake WG, Romeo RD, Sisti HM, Mueller A, McEwen BS, et al. Maternal influences on adult stress and anxiety-like behavior in C57BL/6J and BALB/CJ Mice: a cross-fostering study. Dev Psychobiol 2005;47: 398-407.
50. Chapillon P, Manneché C, Belzung C, Caston J. Rearing environmental enrichment in two inbred strains of mice: 1. Effects on emotional reactivity. Behav Genet 1999;29(1):41-6.
51. Plotsky PM, Thrivikraman KV, Nemeroff CB, Caldji C, Sharma S, Meaney MJ. Long-term consequences of neonatal rearing on central corticotropinreleasing factor systems in adult male rat offspring. Neuropsychopharmacology 2005;30:2192-204.
52. Priestnall R. Effects of litter size on the behaviour of lactating female mice (Mus musculus). Anim Behav 1972;20:386-94.