Evaluation of social and physical enrichment in modulation of behavioural phenotype in C57BL/6J female mice

PLoS ONE

Volumn 6, Issue 9, 2011, Pages

  Kulesskaya, Natalia ^a   Rauvala, Heikki ^a   Voikar, Vootele ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL WELFARE; ANXIETY; ARTICLE; BEHAVIOR CHANGE; CONTROLLED STUDY; ENVIRONMENTAL ENRICHMENT; FEMALE; FORCED SWIMMING TEST; LOCOMOTION; MAZE TEST; MOUSE; NESTING; NOCICEPTION; NONHUMAN; PHENOTYPE; PHYSICAL ACTIVITY; REARING; SOCIAL BEHAVIOR; SOCIAL INTERACTION; SOCIAL ISOLATION; TASK PERFORMANCE; WEANING; ANIMAL; ANIMAL HOUSING; C57BL MOUSE; EXPLORATORY BEHAVIOR; MOTOR ACTIVITY; PHYSIOLOGY;

ANIMALIA; MUS;

ANIMALS; ANXIETY; BEHAVIOR, ANIMAL; EXPLORATORY BEHAVIOR; FEMALE; HOUSING, ANIMAL; MAZE LEARNING; MICE; MICE, INBRED C57BL; MOTOR ACTIVITY;

EID: 80052531716     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0024755     Document Type: Article

References (99)

1. Auwerx J, Avner P, Baldock R, Ballabio A, Balling R, et al. (2004) The European dimension for the mouse genome mutagenesis program. Nat Genet 36: 925-927.
2. Austin CP, Battey JF, Bradley A, Bucan M, Capecchi M, et al. (2004) The knockout mouse project. Nat Genet 36: 921-924.
3. Gerlai R, (2002) Phenomics: fiction or the future? Trends Neurosci 25: 506-509.
4. Bailey KR, Rustay NR, Crawley JN, (2006) Behavioral phenotyping of transgenic and knockout mice: practical concerns and potential pitfalls. ILAR J 47: 124-131.
5. Crawley JN, Paylor R, (1997) A proposed test battery and constellations of specific behavioral paradigms to investigate the behavioral phenotypes of transgenic and knockout mice. Horm Behav 31: 197-211.
6. Paylor R, Spencer CM, Yuva-Paylor LA, Pieke-Dahl S, (2006) The use of behavioral test batteries, II: Effect of test interval. Physiol Behav 87: 95-102.
7. McIlwain KL, Merriweather MY, Yuva-Paylor LA, Paylor R, (2001) The use of behavioral test batteries: Effects of training history. Physiol Behav 73: 705-717.
8. Voikar V, Vasar E, Rauvala H, (2004) Behavioral alterations induced by repeated testing in C57BL/6J and 129S2/Sv mice: implications for phenotyping screens. Genes Brain Behav 3: 27-38.
9. Wahlsten D, Metten P, Phillips TJ, Boehm SL, Burkhart-Kasch S, et al. (2003) Different data from different labs: lessons from studies of gene-environment interaction. J Neurobiol 54: 283-311.
10. Wahlsten D, Rustay NR, Metten P, Crabbe JC, (2003) In search of a better mouse test. Trends Neurosci 26: 132-136.
11. Crabbe JC, Wahlsten D, Dudek BC, (1999) Genetics of mouse behavior: interactions with laboratory environment. Science 284: 1670-1672.
12. Wurbel H, (2002) Behavioral phenotyping enhanced- beyond (environmental) standardization. Genes Brain Behav 1: 3-8.
13. Wurbel H, (2000) Behaviour and the standardization fallacy. Nat Genet 26: 263.
14. Van der Staay FJ, Steckler T, (2002) The fallacy of behavioral phenotyping without standardisation. Genes Brain Behav 1: 9-13.
15. Green EC, Gkoutos GV, Lad HV, Blake A, Weekes J, et al. (2005) EMPReSS: European mouse phenotyping resource for standardized screens. Bioinformatics 21: 2930-2931.
16. Schneider I, Tirsch WS, Faus-Kessler T, Becker L, Kling E, et al. (2006) Systematic, standardized and comprehensive neurological phenotyping of inbred mice strains in the German Mouse Clinic. J Neurosci Methods 157: 82-90.
17. Mandillo S, Tucci V, Holter SM, Meziane H, Banchaabouchi MA, et al. (2008) Reliability, robustness, and reproducibility in mouse behavioral phenotyping: a cross-laboratory study. Physiol Genomics 34: 243-255.
18. Tucci V, Lad HV, Parker A, Polley S, Brown SD, et al. (2006) Gene-environment interactions differentially affect mouse strain behavioral parameters. Mamm Genome 17: 1113-1120.
19. Richter SH, Garner JP, Wurbel H, (2009) Environmental standardization: cure or cause of poor reproducibility in animal experiments? Nat Methods 6: 257-261.
20. Beckers J, Wurst W, de Angelis MH, (2009) Towards better mouse models: enhanced genotypes, systemic phenotyping and envirotype modelling. Nat Rev Genet 10: 371-380.
21. Richter SH, Garner JP, Zipser B, Lewejohann L, Sachser N, et al. (2011) Effect of population heterogenization on the reproducibility of mouse behavior: a multi-laboratory study. PLoS ONE 6: e16461.
22. Baumans V, (2005) Environmental enrichment for laboratory rodents and rabbits: requirements of rodents, rabbits, and research. Ilar J 46: 162-170.
23. Willner P, Mitchell PJ, (2002) The validity of animal models of predisposition to depression. Behav Pharmacol 13: 169-188.
24. Millstein RA, Holmes A, (2007) Effects of repeated maternal separation on anxiety- and depression-related phenotypes in different mouse strains. Neurosci Biobehav Rev 31: 3-17.
25. Millstein RA, Ralph RJ, Yang RJ, Holmes A, (2006) Effects of repeated maternal separation on prepulse inhibition of startle across inbred mouse strains. Genes, Brain and Behavior 5: 346-354.
26. Koolhaas JM, Bartolomucci A, Buwalda B, de Boer SF, Flugge G, et al. (2011) Stress revisited: a critical evaluation of the stress concept. Neurosci Biobehav Rev 35: 1291-1301.
27. Krohn TC, Sorenson DB, Otteson JL, Hansen AK, (2006) The effects of individual housing on mice and rats: a review. Anim Welf 15: 343-352.
28. Brain P, (1975) What does individual housing mean to a mouse? Life Sci 16: 187-200.
29. Voikar V, Polus A, Vasar E, Rauvala H, (2005) Long-term individual housing in C57BL/6J and DBA/2 mice: assessment of behavioral consequences. Genes Brain Behav 4: 240-252.
30. Abramov U, Raud S, Koks S, Innos J, Kurrikoff K, et al. (2004) Targeted mutation of CCK(2) receptor gene antagonises behavioural changes induced by social isolation in female, but not in male mice. Behav Brain Res 155: 1-11.
31. Palanza P, (2001) Animal models of anxiety and depression: how are females different? Neurosci Biobehav Rev 25: 219-233.
32. Palanza P, Gioiosa L, Parmigiani S, (2001) Social stress in mice: gender differences and effects of estrous cycle and social dominance. Physiol Behav 73: 411-420.
33. Martin AL, Brown RE, (2010) The lonely mouse: Verification of a separation-induced model of depression in female mice. Behav Brain Res 207: 196-207.
34. Fox C, Merali Z, Harrison C, (2006) Therapeutic and protective effect of environmental enrichment against psychogenic and neurogenic stress. Behav Brain Res 175: 1-8.
35. Mohammed AH, Zhu SW, Darmopil S, Hjerling-Leffler J, Ernfors P, et al. (2002) Environmental enrichment and the brain. Prog Brain Res 138: 109-133.
36. van Praag H, Kempermann G, Gage FH, (2000) Neural consequences of environmental enrichment. Nat Rev Neurosci 1: 191-198.
37. Olsson IA, Dahlborn K, (2002) Improving housing conditions for laboratory mice: a review of "environmental enrichment". Lab Anim 36: 243-270.
38. Baumans V, Augustsson H, Perretta G, (2011) Animal Needs and Environmental Refinement. In: Howard B, Nevalainen T, Perretta G, editors. The COST Manual of Laboratory Animal Care and Use: Refinement, Reduction, and Research CRC Press pp. 75-100.
39. Voikar V, Koks S, Vasar E, Rauvala H, (2001) Strain and gender differences in the behavior of mouse lines commonly used in transgenic studies. Physiol Behav 72: 271-281.
40. Lister RG, (1987) The use of a plus-maze to measure anxiety in the mouse. Psychopharmacology (Berl) 92: 180-185.
41. Porsolt RD, Bertin A, Jalfre M, (1977) Behavioral despair in mice: a primary screening test for antidepressants. Arch Int Pharmacodyn Ther 229: 327-336.
42. Olsson IA, Hansen AK, Sandoe P, (2007) Ethics and refinement in animal research. Science 317: 1680.
43. Varga O, Hansen AK, Sandoe P, Olsson IA, (2010) Improving transparency and ethical accountability in animal studies: three ways to link ethical approvals to publications. EMBO Rep 11: 500-503.
44. Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG, (2010) Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol 8: e1000412.
45. Wurbel H, (2007) Publications should include an animal-welfare section. Nature 446: 257.
46. Nuffield_Council (2005) The ethics of research involving animals London Nuffield Council on Bioethics website Available: http://www.nuffieldbioethics.org/animal-research. Accessed 2010 Aug 22.
47. Jordan EG, Mogil JS, (2006) Mice, pain, and empathy. Science 314: 253; author reply 253.
48. Miller G, (2006) Animal behavior. Signs of empathy seen in mice. Science 312: 1860-1861.
49. Marris E, (2009) More pain studies needed. Nature 458: 394-395.
50. Hurst JL, West RS, (2010) Taming anxiety in laboratory mice. Nat Methods 7: 825-826.
51. King LA, (2003) Behavioral evaluation of the psychological welfare and environmental requirements of agricultural research animals: theory, measurement, ethics, and practical implications. Ilar J 44: 211-221.
52. Smith AL, Corrow DJ, (2005) Modifications to husbandry and housing conditions of laboratory rodents for improved well-being. Ilar J 46: 140-147.
53. Poole T, (1997) Happy animals make good science. Lab Anim 31: 116-124.
54. Cryan JF, Holmes A, (2005) The ascent of mouse: advances in modelling human depression and anxiety. Nat Rev Drug Discov 4: 775-790.
55. Holmes A, Le Guisquet AM, Vogel E, Millstein RA, Leman S, et al. (2005) Early life genetic, epigenetic and environmental factors shaping emotionality in rodents. Neurosci Biobehav Rev 29: 1335-1346.
56. Schmidt MV, (2010) Molecular mechanisms of early life stress-lessons from mouse models. Neurosci Biobehav Rev 34: 845-852.
57. Schmidt MV, Wang XD, Meijer OC, (2011) Early life stress paradigms in rodents: potential animal models of depression? Psychopharmacology (Berl) 214: 131-140.
58. Bartolomucci A, (2007) Social stress, immune functions and disease in rodents. Front Neuroendocrinol 28: 28-49.
59. House JS, (2001) Social isolation kills, but how and why? Psychosom Med 63: 273-274.
60. Arndt SS, Laarakker MC, van Lith HA, van der Staay FJ, Gieling E, et al. (2009) Individual housing of mice-impact on behaviour and stress responses. Physiol Behav 97: 385-393.
61. Kim JW, Kirkpatrick B, (1996) Social isolation in animal models of relevance to neuropsychiatric disorders. Biol Psychiatry 40: 918-922.
62. Rodgers RJ, Cole JC, (1993) Influence of social isolation, gender, strain, and prior novelty on plus-maze behaviour in mice. Physiol Behav 54: 729-736.
63. Hilakivi LA, Ota M, Lister RG, (1989) Effect of isolation on brain monoamines and the behavior of mice in tests of exploration, locomotion, anxiety and behavioral 'despair'. Pharmacol Biochem Behav 33: 371-374.
64. Blanchard RJ, McKittrick CR, Blanchard DC, (2001) Animal models of social stress: effects on behavior and brain neurochemical systems. Physiol Behav 73: 261-271.
65. Fone KC, Porkess MV, (2008) Behavioural and neurochemical effects of post-weaning social isolation in rodents-relevance to developmental neuropsychiatric disorders. Neurosci Biobehav Rev 32: 1087-1102.
66. Valzelli L, (1973) The "isolation syndrome" in mice. Psychopharmacologia 31: 305-320.
67. Bernberg E, Andersson IJ, Gan LM, Naylor AS, Johansson ME, et al. (2008) Effects of social isolation and environmental enrichment on atherosclerosis in ApoE-/- mice. Stress 11: 381-389.
68. Palermo-Neto J, Fonseca ES, Quinteiro-Filho WM, Correia CS, Sakai M, (2008) Effects of individual housing on behavior and resistance to Ehrlich tumor growth in mice. Physiol Behav 95: 435-440.
69. van Bogaert MJV, Groenink L, Oosting RS, Westphal KGC, van der Gugten J, et al. (2006) Mouse strain differences in autonomic responses to stress. Genes Brain Behav 5: 139-149.
70. Bowers SL, Bilbo SD, Dhabhar FS, Nelson RJ, (2008) Stressor-specific alterations in corticosterone and immune responses in mice. Brain Behav Immun 22: 105-113.
71. Brown KJ, Grunberg NE, (1995) Effects of housing on male and female rats: crowding stresses male but calm females. Physiol Behav 58: 1085-1089.
72. Beery AK, Zucker I, (2011) Sex bias in neuroscience and biomedical research. Neurosci Biobehav Rev 35: 565-572.
73. Burrows EL, McOmish CE, Hannan AJ, (2011) Gene-environment interactions and construct validity in preclinical models of psychiatric disorders. Prog Neuropsychopharmacol Biol Psychiatry in press: doi:10.1016/j.pnpbp.2010.1012.1011.
74. Parker G, Brotchie H, (2010) Gender differences in depression. Int Rev Psychiatry 22: 429-436.
75. McLean CP, Anderson ER, (2009) Brave men and timid women? A review of the gender differences in fear and anxiety. Clin Psychol Rev 29: 496-505.
76. Wolfer DP, Crusio WE, Lipp HP, (2002) Knockout mice: simple solutions to the problems of genetic background and flanking genes. Trends Neurosci 25: 336-340.
77. Nithianantharajah J, Hannan AJ, (2006) Enriched environments, experience-dependent plasticity and disorders of the nervous system. Nat Rev Neurosci 7: 697-709.
78. Rampon C, Tang YP, Goodhouse J, Shimizu E, Kyin M, et al. (2000) Enrichment induces structural changes and recovery from nonspatial memory deficits in CA1 NMDAR1-knockout mice. Nat Neurosci 3: 238-244.
79. Laviola G, Hannan AJ, Macri S, Solinas M, Jaber M, (2008) Effects of enriched environment on animal models of neurodegenerative diseases and psychiatric disorders. Neurobiol Dis 31: 159-168.
80. van Dellen A, Blakemore C, Deacon R, York D, Hannan AJ, (2000) Delaying the onset of Huntington's in mice. Nature 404: 721-722.
81. Lambert TJ, Fernandez SM, Frick KM, (2005) Different types of environmental enrichment have discrepant effects on spatial memory and synaptophysin levels in female mice. Neurobiol Learn Mem 83: 206-216.
82. Wurbel H, (2001) Ideal homes? Housing effects on rodent brain and behaviour. Trends Neurosci 24: 207-211.
83. Bartolomucci A, Palanza P, Sacerdote P, Ceresini G, Chirieleison A, et al. (2003) Individual housing induces altered immuno-endocrine responses to psychological stress in male mice. Psychoneuroendocrinology 28: 540-558.
84. Lister RG, (1990) Ethologically-based animal models of anxiety disorders. Pharmacol Ther 46: 321-340.
85. Pietropaolo S, Singer P, Feldon J, Yee BK, (2008) The postweaning social isolation in C57BL/6 mice: preferential vulnerability in the male sex. Psychopharmacology (Berl) 197: 613-628.
86. Koike H, Ibi D, Mizoguchi H, Nagai T, Nitta A, et al. (2009) Behavioral abnormality and pharmacologic response in social isolation-reared mice. Behav Brain Res 202: 114-121.
87. Karolewicz B, Paul IA, (2001) Group housing of mice increases immobility and antidepressant sensitivity in the forced swim and tail suspension tests. Eur J Pharmacol 415: 197-201.
88. Geyer MA, (1999) Assessing prepulse inhibition of startle in wild-type and knockout mice. Psychopharmacology (Berl) 147: 11-13.
89. Swerdlow NR, Geyer MA, (1998) Using an animal model of deficient sensorimotor gating to study the pathophysiology and new treatments of schizophrenia. Schizophr Bull 24: 285-301.
90. Varty GB, Powell SB, Lehmann-Masten V, Buell MR, Geyer MA, (2006) Isolation rearing of mice induces deficits in prepulse inhibition of the startle response. Behav Brain Res 169: 162-167.
91. Weiss IC, Feldon J, (2001) Environmental animal models for sensorimotor gating deficiencies in schizophrenia: a review. Psychopharmacology (Berl) 156: 305-326.
92. Ponder CA, Kliethermes CL, Drew MR, Muller J, Das K, et al. (2007) Selection for contextual fear conditioning affects anxiety-like behaviors and gene expression. Genes Brain Behav 6: 736-749.
93. Marques JM, Alonso I, Santos C, Silveira I, Olsson IA, (2009) The spatial learning phenotype of heterozygous leaner mice is robust to systematic variation of the housing environment. Comp Med 59: 129-138.
94. Van Loo PL, de Groot AC, Van Zutphen BF, Baumans V, (2001) Do Male Mice Prefer or Avoid Each Other's Company? Influence Of Hierarchy, Kinship, and Familiarity J Appl Anim Welf Sci 4: 91-103.
95. Van de Weerd HA, Van Loo PLP, Van Zutphen LFM, Koolhaas JM, Baumans V, (1998) Preferences for nest boxes as environmental enrichment for laboratory mice. Animal Welfare 7: 11-25.
96. Van de Weerd HA, Van Loo PLP, Van Zutphen LFM, Koolhaas JM, Baumans V, (1998) Strength of preference for nesting material as environmental enrichment for laboratory mice. Applied Animal Behaviour Science 55: 369-382.
97. Van de Weerd HA, Van Loo PL, Van Zutphen LF, Koolhaas JM, Baumans V, (1997) Preferences for nesting material as environmental enrichment for laboratory mice. Lab Anim 31: 133-143.
98. Van de Weerd HA, Van Loo PL, Van Zutphen LF, Koolhaas JM, Baumans V, (1997) Nesting material as environmental enrichment has no adverse effects on behavior and physiology of laboratory mice. Physiol Behav 62: 1019-1028.
99. Kilkenny C, Parsons N, Kadyszewski E, Festing MF, Cuthill IC, et al. (2009) Survey of the quality of experimental design, statistical analysis and reporting of research using animals. PLoS ONE 4: e7824.