Developmental shifts in the behavioral phenotypes of inbred mice: The role of postnatal and juvenile social experiences

Behavior Genetics

Volumn 40, Issue 2, 2010, Pages 220-232

  Curley, J P ^a   Rock, V ^b,c   Moynihan, A M ^d   Bateson, P ^b   Keverne, E B ^b   Champagne, F A ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF LINCOLN   (United Kingdom)

^d UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Cross fostering; Cross housing; Juvenile; Maternal; Social behavior; Strain differences

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL HOUSING; ANXIETY; ARTICLE; BEHAVIOR GENETICS; BODY WEIGHT; CONTROLLED STUDY; CUB; DEVELOPMENTAL STAGE; FEEDING BEHAVIOR; FEMALE; FOSTER CARE; GENE INTERACTION; INBRED STRAIN; JUVENILE; MALE; MATERNAL CARE; MOUSE; NONHUMAN; PERINATAL PERIOD; PHENOTYPE; REARING; SEX DIFFERENCE; SOCIAL BEHAVIOR; STRAIN DIFFERENCE; WEANING;

ANIMALS; BEHAVIOR, ANIMAL; ENVIRONMENT; FEMALE; GENE EXPRESSION REGULATION; MALE; MATERNAL BEHAVIOR; MICE; MICE, INBRED C57BL; PHENOTYPE; SEX FACTORS; SOCIAL BEHAVIOR; SOCIAL ENVIRONMENT; SPECIES SPECIFICITY;

MUS;

EID: 77949265467     PISSN: 00018244     EISSN: 15733297     Source Type: Journal    
DOI: 10.1007/s10519-010-9334-4     Document Type: Article

References (42)

1. U Abramov T Puussaar S Raud K Kurrikoff E Vasar 2008 Behavioural differences between C57BL/6 and 129S6/SvEv strains are reinforced by environmental enrichment Neurosci Lett 443 223 227 10.1016/j.neulet.2008.07.075 18687379
2. E Alleva A Caprioli G Laviola 1989 Litter gender composition affects maternal behavior of the primiparous mouse dam (Mus musculus) J Comp Psychol 103 83 87 10.1037/0735-7036.103.1.83 2924532
3. A Bartolomucci L Gioiosa A Chirieleison G Ceresini S Parmigiani P Palanza 2004 Cross fostering in mice: behavioral and physiological carry-over effects in adulthood Genes, Brain, Behav 3 115 122 10.1111/j.1601-183X.2003.00059.x (Pubitemid 38405257)
4. JA Beck S Lloyd M Hafezparast M Lennon-Pierce JT Eppig MF Festing EM Fisher 2000 Genealogies of mouse inbred strains Nat Genet 24 23 25 10.1038/71641 10615122 (Pubitemid 30041415)
5. RF Benus M Rondigs 1996 Patterns of maternal effort in mouse lines bidirectionally selected for aggression Anim Behav 51 67 75 10.1006/anbe.1996. 0006 (Pubitemid 3017079)
6. P Bhansali J Dunning SE Singer L David C Schmauss 2007 Early life stress alters adult serotonin 2C receptor pre-mRNA editing and expression of the alpha subunit of the heterotrimeric G-protein G q J Neurosci 27 1467 1473 10.1523/JNEUROSCI.4632-06.2007 17287521 (Pubitemid 46255445)
7. ES Brodkin 2007 BALB/c mice: low sociability and other phenotypes that may be relevant to autism Behav Brain Res 176 53 65 10.1016/j.bbr.2006.06.025 16890300 (Pubitemid 44879621)
8. C Caldji J Diorio H Anisman MJ Meaney 2004 Maternal behavior regulates benzodiazepine/GABAA receptor subunit expression in brain regions associated with fear in BALB/c and C57BL/6 mice Neuropsychopharmacology 29 1344 1352 10.1038/sj.npp.1300436 15085086 (Pubitemid 38780657)
9. FA Champagne JP Curley 2005 How social experiences influence the brain Curr Opin Neurobiol 15 704 709 10.1016/j.conb.2005.10.001 16260130 (Pubitemid 41682312)
10. FA Champagne MJ Meaney 2007 Transgenerational effects of social environment on variations in maternal care and behavioral response to novelty Behav Neurosci 121 1353 1363 10.1037/0735-7044.121.6.1353 18085888
11. FA Champagne DD Francis A Mar MJ Meaney 2003 Variations in maternal care in the rat as a mediating influence for the effects of environment on development Physiol Behav 79 359 371 10.1016/S0031-9384(03)00149-5 12954431 (Pubitemid 37098279)
12. FA Champagne JP Curley EB Keverne PP Bateson 2007 Natural variations in postpartum maternal care in inbred and outbred mice Physiol Behav 91 325 334 10.1016/j.physbeh.2007.03.014 17477940 (Pubitemid 46795437)
13. DA Clayton 1978 Social facilitation of behavior Q Rev Biol 53 373 10.1086/410789
14. JC Crabbe D Wahlsten BC Dudek 1999 Genetics of mouse behavior: interactions with laboratory environment Science 284 1670 1672 10.1126/science.284.5420.1670 10356397 (Pubitemid 29291377)
15. JP Curley ER Jordan WT Swaney A Izraelit S Kammel FA Champagne 2009 The meaning of weaning: influence of the weaning period on behavioral development in mice Dev Neurosci 31 318 331 10.1159/000216543 19546569
16. DD Francis K Szegda G Campbell WD Martin TR Insel 2003 Epigenetic sources of behavioral differences in mice Nat Neurosci 6 445 446 12665797
17. A Holmes AM le Guisquet E Vogel RA Millstein S Leman C Belzung 2005 Early life genetic, epigenetic and environmental factors shaping emotionality in rodents Neurosci Biobehav Rev 29 1335 1346 10.1016/j.neubiorev.2005.04.012 16095695 (Pubitemid 41446904)
18. AL Hughes 1989 Interaction between strains in the social relations of inbred mice Behav Genet 19 685 700 10.1007/BF01066031 2803188
19. AV Kalueff P Tuohimaa 2004 Contrasting grooming phenotypes in C57Bl/6 and 129S1/SvImJ mice Brain Res 1028 75 82 10.1016/j.brainres.2004.09.001 15518644 (Pubitemid 39424181)
20. G Laviola ML Terranova 1998 The developmental psychobiology of behavioural plasticity in mice: the role of social experiences in the family unit Neurosci Biobehav Rev 23 197 213 10.1016/S0149-7634(98)00021-9 9884113 (Pubitemid 29011622)
21. D Liu J Diorio B Tannenbaum C Caldji D Francis A Freedman S Sharma D Pearson PM Plotsky MJ Meaney 1997 Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress Science 277 1659 1662 10.1126/science.277.5332.1659 9287218 (Pubitemid 27446227)
22. MJ Meaney 2001 Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations Annu Rev Neurosci 24 1161 1192 10.1146/annurev.neuro.24.1.1161 11520931 (Pubitemid 32695257)
23. LR Meek PL Dittel MC Sheehan JY Chan SR Kjolhaug 2001 Effects of stress during pregnancy on maternal behavior in mice Physiol Behav 72 473 479 10.1016/S0031-9384(00)00431-5 11282130 (Pubitemid 32244409)
24. A Moles A Bartolomucci L Garbugino R Conti A Caprioli R Coccurello R Rizzi B Ciani FR D'Amato 2006 Psychosocial stress affects energy balance in mice: modulation by social status Psychoneuroendocrinology 31 623 633 10.1016/j.psyneuen.2006.01.004 16616814
25. NP Murphy HA Lam NT Maidment 2001 A comparison of morphine-induced locomotor activity and mesolimbic dopamine release in C57BL6, 129 Sv and DBA2 mice J Neurochem 79 626 635 10.1046/j.1471-4159.2001.00599.x 11701766 (Pubitemid 33029936)
26. JB Panksepp GP Lahvis 2007 Social reward among juvenile mice Genes, Brain, Behav 6 661 671 10.1111/j.1601-183X.2006.00295.x (Pubitemid 47476188)
27. MP Paulus SC Dulawa RJ Ralph AG Mark 1999 Behavioral organization is independent of locomotor activity in 129 and C57 mouse strains Brain Res 835 27 36 10.1016/S0006-8993(99)01137-3 10448193 (Pubitemid 29336547)
28. P Prakash Z Merali M Kolajova BM Tannenbaum H Anisman 2006 Maternal factors and monoamine changes in stress-resilient and susceptible mice: cross-fostering effects Brain Res 1111 122 133 10.1016/j.brainres.2006.06.089 16876768 (Pubitemid 44331185)
29. K Priebe RD Romeo DD Francis HM Sisti A Mueller BS McEwen WG Brake 2005 Maternal influences on adult stress and anxiety-like behavior in C57BL/6 J and BALB/cJ mice: a cross-fostering study Dev Psychobiol 47 398 407 10.1002/dev.20098 16284964 (Pubitemid 43081900)
30. L Prut C Belzung 2003 The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review Eur J Pharmacol 463 3 33 10.1016/S0014-2999(03)01272-X 12600700 (Pubitemid 36205070)
31. CL Randall D Lester 1975 Social modification of alcohol consumption in inbred mice Science 189 149 151 10.1126/science.1138373 1138373
32. RH Ressler 1962 Parental handling in two strains of mice reared by foster parents Science 137 129 130 10.1126/science.137.3524.129 14491572
33. L Ricceri A Moles J Crawley 2007 Behavioral phenotyping of mouse models of neurodevelopmental disorders: Relevant social behavior patterns across the life span Behav Brain Res 176 40 52 10.1016/j.bbr.2006.08.024 16996147 (Pubitemid 44879627)
34. MG Ruscio T Sweeny J Hazelton P Suppatkul CS Carter 2007 Social environment regulates corticotropin releasing factor, corticosterone and vasopressin in juvenile prairie voles Horm Behav 51 54 61 10.1016/j.yhbeh.2006. 08.004 17007856 (Pubitemid 44838631)
35. H Shoji K Kato 2006 Maternal behavior of primiparous females in inbred strains of mice: a detailed descriptive analysis Physiol Behav 89 320 328 10.1016/j.physbeh.2006.06.012 16842828 (Pubitemid 44436311)
36. PB Smith DR Pederson 1988 Maternal sensitivity and patterns of infant-mother attachment Child Dev 59 1097 1101 10.2307/1130276 3168617
37. MB Solomon MT Foster TJ Bartness KL Huhman 2007 Social defeat and footshock increase body mass and adiposity in male Syrian hamsters Am J Physiol Regul Integr Comp Physiol 292 R283 R290 16946084
38. R van der Veen DN Abrous ER de Kloet PV Piazza M Koehl 2008 Impact of intra- and interstrain cross-fostering on mouse maternal care Genes, Brain, Behav 7 184 192 10.1111/j.1601-183X.2007.00337.x (Pubitemid 351342194)
39. V Voikar S Koks E Vasar H Rauvala 2001 Strain and gender differences in the behavior of mouse lines commonly used in transgenic studies Physiol Behav 72 271 281 10.1016/S0031-9384(00)00405-4 11240006 (Pubitemid 32184818)
40. D Wahlsten P Metten TJ Phillips SL Boehm 2nd S Burkhart-Kasch J Dorow S Doerksen C Downing J Fogarty K Rodd-Henricks R Hen CS McKinnon CM Merrill C Nolte M Schalomon JP Schlumbohm JR Sibert CD Wenger BC Dudek JC Crabbe 2003 Different data from different labs: lessons from studies of gene-environment interaction J Neurobiol 54 283 311 10.1002/neu.10173 12486710 (Pubitemid 36050068)
41. IC Weaver N Cervoni FA Champagne AC D'Alessio S Sharma JR Seckl S Dymov M Szyf MJ Meaney 2004 Epigenetic programming by maternal behavior Nat Neurosci 7 847 854 10.1038/nn1276 15220929 (Pubitemid 38989508)
42. M Yang ML Scattoni V Zhodzishsky T Chen H Caldwell WS Young HG McFarlane JN Crawley 2007 Social approach behaviors are similar on conventional versus reverse lighting cycles, and in replications across cohorts, in BTBR T+ tf/J, C57BL/6 J, and vasopressin receptor 1B mutant mice Front Behav Neurosci 1 1 10.3389/neuro.08.001.2007 18958184