Variation in stress reactivity affects cage-induced stereotypies in female CD-1 (ICR) mice

Applied Animal Behaviour Science

Volumn 133, Issue 1-2, 2011, Pages 101-108

  Engel, Anna Katarina J ^a   Gross, Alexandra N ^a,b   Richter, S Helene ^c   Rommen, Jonas ^a   Touma, Chadi ^d   Würbel, Hanno ^a  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

^b UNIVERSITY OF MÜNSTER   (Germany)

^c CENTRAL INSTITUTE OF MENTAL HEALTH   (Germany)

^d MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

Author keywords

Behaviour; CD 1; Corticosterone; HPA response; Mouse; Stereotypy; Stress; Welfare

Indexed keywords

ANIMAL WELFARE; BEHAVIORAL RESPONSE; CAPTIVE POPULATION; DRUG; ENVIRONMENTAL CONDITIONS; ENVIRONMENTAL STRESS; FEMALE BEHAVIOR; HORMONE; RODENT; SELECTIVE BREEDING; STEREOTYPIC BEHAVIOR; STEROID;

ANIMALIA; MUS;

EID: 79959516436     PISSN: 01681591     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.applanim.2011.04.017     Document Type: Article

References (52)

1. Bhatnagar S., Shanks N., Meaney M.J. Plaque-forming cell responses and antibody titers following injection of sheep-red blood cells in nonstressed, acute and/or chronically stressed handled and nonhandled animals. Dev. Psychobiol. 1996, 29:171-181.
2. Buijs R.M., Kalsbeek A. Hypothalamic integration of central and peripheral clocks. Nat. Rev. Neurosci. 2001, 2:521-526.
3. Cabib S. The neurobiology of stereotypy II: the role of stress. Stereotypic Animal Behaviour: Fundamentals and Applications to Welfare 2006, 227-255. CABI, Wallingford. G. Mason, J. Rushen (Eds.).
4. Coutellier L., Friedrich A.-C., Failing K., Marashi V., Würbel H. Effects of rat odour and shelter on maternal behaviour in C57BL/6 dams and on fear and stress responses in their adult offspring. Physiol. Behav. 2008, 94:393-404.
5. Darnaudéry M., Maccari S. Epigenetic programming of the stress response in male and female rats by prenatal restraint stress. Brain Res. Rev. 2008, 57:571-585.
6. Dallman M.F., Engeland W.C., Rose J.C., Wilkinson C.W., Shinsako J., Siedenburg F. Nycthemeral rhythm in adrenal responsiveness to ACTH. Am. J. Physiol. 1978, 235:R210-R218.
7. Dallman M.F., Akana S.F., Scribner K.A., Bradbury M.J., Walker C.D. Stress, feedback and facilitation in the hypothalamo-pituitary adrenal axis. J. Neuroendocrinol. 1992, 4:517-526.
8. De Kloet E.R., Vregdenhil E., Oitzl M.S., Joels M. Brain corticosteroid receptor balance in health and disease. Endocrinol. Rev. 1998, 19:269-301.
9. 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, 60:1565-1568.
10. Engeland W.C., Arnhold M.M. Neural circuitry in the regulation of adrenal corticosterone rhythmicity. Endocrine 2005, 325-331.
11. Francis D.D., Diorio J., Plotsky P.M., Meaney M.J. Environmental enrichment reverses the effects of maternal separation on stress reactivity. J. Neurosci. 2002, 22:7840-7843.
12. Garner J.P. Perseveration and stereotypy - systems-level insights from clinical psychology. Stereotypic Animal Behaviour: Fundamentals and Applications to Welfare 2006, 121-152. CABI, Wallingford. G. Mason, J. Rushen (Eds.).
13. Garner J.P., Mason G.J. Evidence for a relationship between cage stereotypies and behavioural disinhibition in laboratory rodents. Behav. Brain Res. 2002, 136:83-92.
14. Halberg F., Albrecht P.G., Bittner J.J. Corticosterone rhythm of mouse adrenal in relation to serum corticosterone and sampling. Am. J. Physiol. 1959, 197:1083-1085.
15. Heinzmann J.M., Thoeringer C.K., Knapman A., Palme R., Holsboer F., Uhr M., Landgraf R., Touma C. Intrahippocampal corticosterone dynamics in mice selectively bred for extremes in stress reactivity: a microdialysis study. J. Neuroendocrinol. 2010, 22:1187-1197.
16. Jacobson L., Sapolsky R. The role of the hippocampus in feedback regulation of the hypothalamic-pituitary-adrenocortical axis. Endocr. Rev. 1991, 12:118-134.
17. Kalsbeek A., van Heerikhuize J.J., Wortel J., Buijs R.M. A diurnal rhythm of stimulatory input to the hypothalamo-pituitary-adrenal system as revealed by timed intrahypothalamic administration of the vasopressin V1 antagonist. J. Neurosci. 1996, 16:5555-5565.
18. Laban O., Dimitrijevic M., Hoersten S., von, Markovic B.M., Jankovic B.D. Experimental allergic encephalomyelitis in the rat. Brain Behav. Immun. 1995, 9:9-19.
19. Ladd C.O., Huot R.L., Thrivikraman K.V., Nemeroff C.B., Plotsky P.M. Long-term adaptations in glucocorticoid receptor and mineralocorticoid receptor mRNA and negative feedback on the hypothalamo-pituitary-adrenal axis following neonatal maternal separation. Biol. Psychiatry 2004, 55:367-375.
20. Latham N., Mason G. Frustration and perseveration in stereotypic captive animals: is a taste of enrichment worse than none at all?. Behav. Brain Res. 2010, 211:96-104.
21. Lee J.W., Ryoo Z.Y., Lee E.J., Hong S.H., Chung W.H., Lee H.T., Chung K.S., Kim T.Y., Oh Y.S., Suh J.G. Circling mouse, a spontaneous mutant in the inner ear. Exp. Anim. 2002, 51:167-171.
22. Lewis R.S., Hurst J.L. The assessment of bar-chewing as an escape behaviour in laboratory mice. Anim. Welfare 2004, 13:19-25.
23. Macrì S., Würbel H. Developmental plasticity of HPA and fear responses in rats: a critical review of the maternal mediation hypothesis. Horm. Behav. 2006, 50:667-680.
24. Macrì S., Chiarotti F., Würbel H. Maternal separation and maternal care act independently on the development of HPA responses in male rats. Behav. Brain Res. 2008, 191:227-234.
25. Mason G.J. Stereotypies: a critical review. Anim. Behav. 1991, 41:1015-1037.
26. McBride S.D., Hemmings A. Altered mesoaccumbens and nigro-striatal dopamine physiology is associated with stereotypy development in a non-rodent species. Behav. Brain Res. 2005, 159:113-118.
27. Meaney M.J., Aitken D.H., Bhatnagar S., Van Berkel C.H., Sapolsky R.M. Postnatal handling attenuates neuroendocrine, anatomical, and cognitive impairments related to the aged hippocampus. Science 1988, 238:766-768.
28. Meaney M.J. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Ann. Rev. Neurosci. 2001, 24:1161-1192.
29. Nevison C.M., Hurst J.L., Barnard C.J. Why do male ICR(CD-1) mice perform bar-related (stereotypic) behaviour?. Behav. Process. 1999, 47:95-111.
30. Ödberg F.O. Abnormal behaviours: Stereotypies. Proc. 1st World Congr. Ethol. Appl. Zootechnics. Industrias Graficas Espana. Madrid. 1978, 475-480.
31. Ödberg F.O. The jumping stereotypy in the bank vole (Clethrionomys glareolus). Biol. Behav. 1986, 11:130-143.
32. Plotsky P.M. Pathways to the secretion of adrenocorticotropin: a view from the portal. J. Neuroendocrinol. 1991, 3:1-9.
33. Redbo I., Nordblad A. Stereotypies in heifers are affected by feeding regime. Appl. Anim. Behav. Sci. 1997, 53:193-202.
34. Rice W.R. Analyzing table of statistical tests. Evolution 1989, 43:223-225.
35. Romano M.C., Rodas A.Z., Valdez R.A., Hernández S.E., Galindo F., Canales D., Brousset D.M. Stress in wildlife species: noninvasive monitoring of glucocorticoids. Neuroimmunomodulation 2010, 17:209-212.
36. Schmidt M.V., Scharf S.H., Liebl C., Harbich D., Mayer B., Holsboer F., Müller M.B. A novel chronic social stress paradigm in female mice. Horm. Behav. 2010, 57:415-420.
37. Schmidt M.V., Sterlemann V., Ganea K., Liebl C., Alam S., Harbich D., Greetfeld M., Uhr M., Holsboer F., Müller M.B. Persistent neuroendocrine and behavioral effects of a novel, etiologically relevant mouse paradigm for chronic social stress during adolescence. Psychoneuroendocrinology 2007, 32:417-429.
38. Schönecker B., Heller K.E. Indication of a genetic basis of stereotypies in laboratory-bred bank voles (Clethrionomys glareolus). Appl. Anim. Behav. Sci. 2000, 68:339-347.
39. Schwaibold U., Pillay N. Stereotypic behaviour is genetically transmitted in the African striped mouse, Rhabdomys pumilio. Appl. Anim. Behav. Sci. 2001, 74:273-280.
40. Siegel S., Castellan N.J. Nonparametric Statistics for the Behavioral Sciences 1988, McGraw-Hill, London. 2nd ed.
41. Touma C., Bunck M., Glasl L., Nussbaumer M., Palme R., Stein H., Wolferstätter M., Zeh R., Zimbelmann M., Holsboer F., Landgraf R. Mice selected for high versus low stress reactivity: a new animal model for affective disorders. Psychoneuroendocrinology 2008, 33:839-862.
42. Touma C., Fenzl T., Ruschel J., Palme R., Holsboer F., Kimura M., Landgraf R. Rhythmicity in mice selected for extremes in stress reactivity: behavioural, endocrine and sleep changes resembling endophenotypes of major depression. PLoS ONE 2009, 4(1):e4325.
43. Turner M. Towards an executive dysfunction account of repetitive behaviour in autism. Autism as An Executive Disorder 1997, 57-100. Oxford University Press, New York. J. Russell, A. et (Eds.).
44. Vanderschuren L.J.M.J., Kalivas P.W. Alterations in dopaminergic and glutamatergic transmission in the induction and expression of behavioral sensitization: a critical review of preclinical studies. Psychopharmacology 2000, 151:99-120.
45. Weaver I.C., Cervoni N., Champagne F.A., D'Alessio A.C., Sharma S., Seckl J.R., Dymov S., Szyf M., Meaney M.J. Epigenetic programming by maternal behavior. Nat. Neurosci. 2004, 7:847-854.
46. Willner P. Chronic mild stress (CMS) revisited: consistency and behavioural-neurobiological concordance in the effects of CMS. Neuropsychobiology 2005, 52:90-110.
47. Würbel H., Stauffacher M., von Holst D. Stereotypies in laboratory mice - quantitative and qualitative description of the ontogeny of 'wire-gnawing' and 'jumping' in ICR and ICR nu - mice. Ethology 1996, 102:371-385.
48. Würbel H., Stauffacher M. Age and weight at weaning affect corticosterone level and development of stereotypies in ICR-mice. Anim. Behav. 1997, 53:891-900.
49. Würbel H., Stauffacher M. Physical condition at weaning affects exploratory behaviour and stereotypy development in laboratory mice. Behav. Process. 1998, 43:61-69.
50. Würbel H., Chapman R., Rutland C. Effect of feed and environmental enrichment on development of stereotypic wire-gnawing in laboratory mice. Appl. Anim. Behav. Sci. 1998, 60:69-81.
51. Würbel H. The motivational basis of caged rodents' stereotypies. Stereotypic Animal Behaviour - Fundamentals and Applications to Welfare 2006, 86-120. CABI, Wallingford. G.J. Mason, J. Rushen (Eds.).
52. Zanella A.J., Broom D.M., Hunter J.C., Mendl M.T. Brain opioid receptors in relation to stereotypies, inactivity, and housing in sows. Physiol. Behav. 1996, 59:769-775.