Environmental enrichment during rearing alters corticosterone levels, thymocyte numbers, and aggression in female BALB/c mice

Journal of the American Association for Laboratory Animal Science

Volumn 51, Issue 1, 2012, Pages 18-24

  Hutchinson, Eric K ^a   Avery, Anne C ^b   VandeWoude, Sue ^b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CORTICOSTERONE; CREATININE;

AGGRESSION; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BODY WEIGHT; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; CREATININE URINE LEVEL; ENVIRONMENTAL ENRICHMENT; FEMALE; HAIR LOSS; HYDRATION; MOTOR DYSFUNCTION; MOUSE; NESTING; NONHUMAN; THYMOCYTE; THYMUS ATROPHY; URINE LEVEL; URINE VOLUME; WEANING;

AGGRESSION; ANALYSIS OF VARIANCE; ANIMAL HUSBANDRY; ANIMAL WELFARE; ANIMALS; BODY WEIGHT; CORTICOSTERONE; ENVIRONMENT; FEMALE; MICE; MICE, INBRED BALB C; STEREOTYPED BEHAVIOR; THYMOCYTES;

ANIMALIA; MUS;

EID: 84856933454     PISSN: 15596109     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (53)

1. Abramov U, Puussaar T, Raud S, Kurrikoff K, Vasar E. 2008. Behavioural differences between C57BL/6 and 129S6/SvEv strains are reinforced by environmental enrichment. Neurosci Lett 443:223-227.
2. Amaral OB, Vargas RS, Hansel G, Izquierdo I, Souza DO. 2008. Duration of environmental enrichment influences the magnitude and persistence of its behavioral effects on mice. Physiol Behav 93:388-394.
3. Animal Welfare Act as Amended. 2007. 7 USC §2131-2159.
4. Black PH, Garbutt LD. 2002. Stress, inflammation, and cardiovascular disease. J Psychosom Res 52:1-23.
5. Bond TL, Neumann PE, Mathieson WB, Brown RE. 2002. Nest building in nulligravid, primigravid, and primiparous C57BL/6J and DBA/2J mice (Mus musculus). Physiol Behav 75:551-555. (Pubitemid 34327962)
6. Catlow BJ, Rowe AR, Clearwater CR, Mamcarz M, Arendash GW, Sanchez-Ramos J. 2009. Effects of environmental enrichment and physical activity on neurogenesis in transgenic PS1/APP mice. Brain Res 1256:173-179.
7. Chapillon P, Manneche C, Belzung C, Caston J. 1999. Rearing environmental enrichment in 2 inbred strains of mice: effects on emotional reactivity. Behav Genet 29:41-46. (Pubitemid 29265765)
8. Coutellier L, Wurbel H. 2009. Early environmental cues affect object recognition memory in adult female but not male C57BL/6 mice. Behav Brain Res 203:312-315.
9. Eriksson H. 1971. Absorption and enterohepatic circulation of neutral steroids in the rat. Eur J Biochem 19:416-423.
10. Eriksson H. 1971. Steroids in germfree and conventional rats. Metabolites of (4-14C)pregnenolone and (4-14C)corticosterone in urine and faeces from male rats. Eur J Biochem 18:86-93.
11. Espey MG, Basile AS. 1999. Glutamate augments retrovirus-induced immunodeficiency through chronic stimulation of the hypothalamic-pituitary- adrenal axis. J Immunol 162:4998-5002. (Pubitemid 29314908)
12. Fernandez-Teruel A, Gimenez-Llort L, Escorihuela RM, Gil L, Aguilar R, Steimer T, Tobena A. 2002. Early-life handling stimulation and environmental enrichment: are some of their effects mediated by similar neural mechanisms? Pharmacol Biochem Behav 73:233-245. (Pubitemid 34667035)
13. Fitchett AE, Collins SA, Mason H, Barnard CJ, Cassaday HJ. 2005. Urinary corticosterone measures: effects of strain and social rank in BKW and CD-1 mice. Behav Processes 70:168-176. (Pubitemid 41208071)
14. Gartner K, Buttner D, Dohler K, Friedel R, Lindena J, Trautschold I. 1980. Stress response of rats to handling and experimental procedures. Lab Anim 14:267-274. (Pubitemid 11244923)
15. Gresack JE, Kerr KM, Frick KM. 2007. Short-term environmental enrichment decreases the mnemonic response to estrogen in young, but not aged, female mice. Brain Res 1160:91-101. (Pubitemid 47058040)
16. Harburger LL, Lambert TJ, Frick KM. 2007. Age-dependent effects of environmental enrichment on spatial reference memory in male mice. Behav Brain Res 185:43-48. (Pubitemid 47552574)
17. Harlow HF. 1958. The nature of love. Am Psychol 13:673-685.
18. Herring A, Ambree O, Tomm M, Habermann H, Sachser N, Paulus W, Keyvani K. 2009. Environmental enrichment enhances cellular plasticity in transgenic mice with Alzheimer-like pathology. Exp Neurol 216:184-192.
19. Hess SERS, Dufour BD, Gaskill BN, Pajor EA, Garner JP. 2008. Home improvement: C57BL/6J mice given more naturalistic nesting materials build better nests. J Am Assoc Lab Anim Sci 47:25-31.
20. Hutchinson E, Avery A, Vandewoude S. 2005. Environmental enrichment for laboratory rodents. ILAR J 46:148-161. (Pubitemid 40514523)
21. Institute for Laboratory Animal Research. 2011. Guide for the care and use of laboratory animals, 8th ed. Washington (DC): National Academies Press.
22. Jankowsky JL, Xu G, Fromholt D, Gonzales V, Borchelt DR. 2003. Environmental enrichment exacerbates amyloid plaque formation in a transgenic mouse model of Alzheimer disease. J Neuropathol Exp Neurol 62:1220-1227. (Pubitemid 37494191)
23. Latham N, Mason G. 2010. Frustration and perseveration in stereotypic captive animals: is a taste of enrichment worse than none at all? Behav Brain Res 211:96-104.
24. Leal-Galicia P, Castaneda-Bueno M, Quiroz-Baez R, Arias C. 2008. Long-term exposure to environmental enrichment since youth prevents recognition memory decline and increases synaptic plasticity markers in aging. Neurobiol Learn Mem 90:511-518.
25. Li L, Tang BL. 2005. Environmental enrichment and neurodegenerative diseases. Biochem Biophys Res Commun 334:293-297. (Pubitemid 40982368)
26. Lin EJ, Choi E, Liu X, Martin A, During MJ. 2011. Environmental enrichment exerts sex-specific effects on emotionality in C57BL/6J mice. Behav Brain Res 216:349-357.
27. Lonetti G, Angelucci A, Morando L, Boggio EM, Giustetto M, Pizzorusso T. 2010. Early environmental enrichment moderates the behavioral and synaptic phenotype of MeCP2-null mice. Biol Psychiatry 67:657-665.
28. Mainardi M, Scabia G, Vottari T, Santini F, Pinchera A, Maffei L, Pizzorusso T, Maffei M. 2010. A sensitive period for environmental regulation of eating behavior and leptin sensitivity. Proc Natl Acad Sci USA 107:16673-16678.
29. Meijer MK, Lemmens AG, Van Zutphen BF, Baumans V. 2005. Urinary corticosterone levels in mice in response to intraperitoneal injections with saline. J Appl Anim Welf Sci 8:279-283.
30. Moles A, Sarli C, Bartolomucci A, D'Amato FR. 2008. Interaction with stressed mothers affects corticosterone levels in pups after reunion and impairs the response to dexamethasone in adult mice. Psychoneuroendocrinology 33:462-470. (Pubitemid 351503687)
31. Nevison CM, Hurst JL, Barnard CJ. 1999. Strain-specific effects of cage enrichment in male laboratory mice (Mus musculus). Anim Welf 8:361-379. (Pubitemid 129619720)
32. Newberry RC. 1995. Environmental enrichment: increasing the biological relevance of captive environments. Appl Anim Behav Sci 44:229-243.
33. Olsson IA, Dahlborn K. 2002. Improving housing conditions for laboratory mice: a review of "environmental enrichment". Lab Anim 36:243-270. (Pubitemid 34785762)
34. Robertson KL, Rowland NE. 2005. Effect of two types of environmental enrichment for singly housed mice on food intake and weight gain. Lab Anim (NY) 34:29-32. (Pubitemid 44662090)
35. Rosenbaum MD, VandeWoude S, Johnson TE. 2009. Effects of cage-change frequency and bedding volume on mice and their microenvironment. J Am Assoc Lab Anim Sci 48:763-773.
36. Schridde U, van Luijtelaar G. 2004. The influence of strain and housing on 2 types of spike-wave discharges in rats. Genes Brain Behav 3:1-7. (Pubitemid 38160236)
37. Shackleton CH, Hughes BA, Lavery GG, Walker EA, Stewart PM. 2008. The corticosteroid metabolic profile of the mouse. Steroids 73:1066-1076.
38. Simonetti T, Lee H, Bourke M, Leamey CA, Sawatari A. 2009. Enrichment from birth accelerates the functional and cellular development of a motor control area in the mouse. PLoS ONE 4:e6780.
39. Solinas M, Thiriet N, El Rawas R, Lardeux V, Jaber M. 2009. Environmental enrichment during early stages of life reduces the behavioral, neurochemical, and molecular effects of cocaine. Neuropsychopharmacology 34:1102-1111.
40. Thiriet N, Amar L, Toussay X, Lardeux V, Ladenheim B, Becker KG, Cadet JL, Solinas M, Jaber M. 2008. Environmental enrichment during adolescence regulates gene expression in the striatum of mice. Brain Res 1222:31-41.
41. Tischkau SA, Mukai M. 2009. Activation of aryl hydrocarbon receptor signaling by cotton balls used for environmental enrichment. J Am Assoc Lab Anim Sci 48:357-362.
42. Touma C, Sachser N, Mostl E, Palme R. 2003. Effects of sex and time of day on metabolism and excretion of corticosterone in urine and feces of mice. Gen Comp Endocrinol 130:267-278. (Pubitemid 36207609)
43. Tsai PP, Pachowsky U, Stelzer HD, Hackbarth H. 2002. Impact of environmental enrichment in mice. 1: effect of housing conditions on body weight, organ weights and haematology in different strains. Lab Anim 36:411-419. (Pubitemid 35192156)
44. Vachon P, Moreau JP. 2001. Serum corticosterone and blood glucose in rats after 2 jugular vein blood sampling methods: comparison of the stress response. Contemp Top Lab Anim Sci 40:22-24. (Pubitemid 33674824)
45. Van Loo PLP, Van De Weerd HA, Baumans V. 1996. Short and long term influence of an easy applicable enrichment device on the behaviour of the laboratory mouse. Scand J Lab Anim Sci 23:113-118.
46. van Praag H, Kempermann G, Gage FH. 2000. Neural consequences of environmental enrichment. Nat Rev Neurosci 1:191-198.
47. Vande Woude S, Rollin M, Avery A. 2002. The effects of environmental enrichment on murine immune responses. Contemp Top Lab Anim Sci 41:69.
48. Viola GG, Botton PH, Moreira JD, Ardais AP, Oses JP, Souza DO. 2010. Influence of environmental enrichment on an object recognition task in CF1 mice. Physiol Behav 99:17-21.
49. Webster JI, Tonelli L, Sternberg EM. 2002. Neuroendocrine regulation of immunity. Annu Rev Immunol 20:125-163. (Pubitemid 34295785)
50. Winter J, Bokkenheuser VD, Ponticorvo L. 1979. Bacterial metabolism of corticoids with particular reference to the 21-dehydroxylation. J Biol Chem 254:2626-2629. (Pubitemid 9196096)
51. Wood NI, Carta V, Milde S, Skillings EA, McAllister CJ, Ang YL, Duguid A, Wijesuriya N, Afzal SM, Fernandes JX, Leong TW, Morton AJ. 2010. Responses to environmental enrichment differ with sex and genotype in a transgenic mouse model of Huntington's disease. PLoS ONE 5:e9077.
52. Wurbel H, Stauffacher M. 1996. Prevention of stereotypy in laboratory mice: effects on stress physiology and behaviour. Physiol Behav 59:1163-1170. (Pubitemid 26198196)
53. Würbel H, Stauffacher M, Von Holst D. 1996. Stereotypies in laboratory mice. Quantitative and qualitative description of the ontogeny of 'wire-gnawing' and 'jumping' in Zur:ICR and Zur:ICR-nu. Ethology 102:371-385. (Pubitemid 26263042)