Middle-aged mice with enrichment-resistant stereotypic behaviour show reduced motivation for enrichment

Animal Behaviour

Volumn 80, Issue 3, 2010, Pages 363-373

  Tilly, Sarah Lee C ^a   Dallaire, Jamie ^b   Mason, Georgia J ^b  

^a UTRECHT UNIVERSITY   (Netherlands)

^b UNIVERSITY OF GUELPH   (Canada)

Author keywords

Age; Animal welfare; Enrichment; Establishment; Laboratory mice; Motivation; Mus musculus; Reward value; Stereotypic behaviour

Indexed keywords

AGE STRUCTURE; ANIMAL WELFARE; CAPTIVE POPULATION; ENRICHMENT; HYPOTHESIS TESTING; LABORATORY METHOD; RODENT; STEREOTYPIC BEHAVIOR;

ANIMALIA; MUS; MUS MUSCULUS;

EID: 77955568317     PISSN: 00033472     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.anbehav.2010.06.008     Document Type: Article

References (79)

1. Ames A. The Welfare and Management of Bears in Zoological Gardens 1994, Universities Federation for Animal Welfare, Potters Bar.
2. Augustsson H., Van de Weerd H.A., Kruitwagen C.L.J.J., Baumans V. Effect of enrichment on variation and results in the light/dark test. Laboratory Animals 2003, 37:328-340.
3. Baker K.C. Advanced age influences chimpanzee behavior in small social groups. Zoo Biology 2000, 19:111-119.
4. Benus R.F., den Daas S., Koolhaas J.M., van Oortmerssen G.A. Routine-formation and flexibility in social and nonsocial behaviour of aggressive and non-aggressive male mice. Behaviour 1990, 112:176-193.
5. Bondi C.O., Rodriguez G., Gould G.G., Frazer A., Morilak D.A. Chronic unpredictable stress induces a cognitive deficit and anxiety-like behavior in rats that is prevented by chronic antidepressant drug treatment. Neuropsychopharmacology 2008, 33:320-331.
6. Burghardt G. The Genesis of Animal Play: Testing the Limits 2005, MIT Press, Cambridge, Massachusetts.
7. Clubb, R. 2001. Factors affecting the development of abnormal, stereotyped behaviour in zoo-housed carnivores. Ph.D. thesis, University of Oxford.
8. Cooper, J. J. 1992. Behavioural analysis of stereotypic behaviour in rodents. Ph.D. thesis, University of Bristol.
9. Cooper J.J., Nicol C.J. Stereotypic behaviour affects environmental preference in bank voles (Clethrionomys glareolus). Animal Behaviour 1991, 41:971-977.
10. Cooper J.J., Ödberg F. The emancipation of stereotypies with age. Proceedings of the International Congress of the Society for Veterinary Ethology 1991, 142. Universities Federation for Animal Welfare, Edinburgh. M.C. Appleby, R.I. Horrell, J.C. Petherick, S.M. Rutter (Eds.).
11. Cooper J.J., Ödberg F., Nicol C.J. Limitations on the effectiveness of environmental improvement in reducing stereotypic behaviour in bank voles (Clethrionomys glareolus). Applied Animal Behaviour Science 1996, 48:237-248.
12. Cronin, G. M. 1985. The development and significance of abnormal stereotyped behaviours in tethered sows. Ph.D. thesis, Wageningen University.
13. Crawley J.N. What's Wrong With My Mouse? Behavioral Phenotyping of Transgenic and Knockout Mice 2007, Wiley-Liss, Wilmington. 2nd edn.
14. Darlington R.B., Smulders T.V. Problems with residual analysis. Animal Behaviour 2001, 62:599-602.
15. Di Giovanni M., Valente M. Trial and error: attempting to change the lives of socially and environmentally deprived primates. Proceedings of the 4th International Conference on Environmental Enrichment 2001, 358-363. The Shape of Enrichment, San Diego. V.J. Hare, K.E. Worley, K. Myers (Eds.).
16. Dodman N.H., Karlsson E.K., Moon-Fanelli A., Galdzicka M., Perloski M., Shuster L., Lindblad-Toh K., Ginns E.I. A canine chromosome 7 locus confers compulsive disorder susceptibility. Molecular Psychiatry 2010, 15:8-10.
17. Eaton G.G., Kelley S.T., Axthelm M.K., Iliff-Sizemore S.A., Shiigi S.M. Psychological well-being in paired adult female rhesus (Macaca mulatta). American Journal of Primatology 1994, 33:89-99.
18. Fentress J.C. Dynamic boundaries of patterned behaviour: interaction and self-organisation. Perspectives in Ethology. Vol. I 1976, 155-224. Plenum, New York. P.P.G. Bateson, R.A. Hinde (Eds.).
19. Fentress J.C. The tonic hypothesis and the patterning of behavior. Annals of the New York Academy of Sciences 1977, 290:370-395.
20. Flurkey K., Currer J.M., Harrison D.E. The mouse in aging research. The Mouse in Biomedical Research. Vol. III. Normative Biology, Husbandry, and Models 2007, 637-672. Academic Press, Burlington. 2nd edn. J.G. Fox, S.W. Barthold, M.T. Davisson, C.E. Newcomer, F.W. Quimby, A.L. Smith (Eds.).
21. García-Berthou E. On the misuse of residuals in ecology: testing regression residuals vs. the analysis of covariance. Journal of Animal Ecology 2001, 70:708-711.
22. Garner, J. P. 1999. The aetiology of stereotypy in caged animals. Ph.D. thesis, University of Oxford.
23. 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. 2nd edn. G. Mason, J. Rushen (Eds.).
24. Garner J.P., Meehan C.L., Mench J.A. Stereotypies in caged parrots, schizophrenia and autism: evidence for a common mechanism. Behavioural Brain Research 2003, 145:125-134.
25. Golani I., Kafkafi N., Drai D. Phenotyping stereotypic behaviour: collective variables, range of variation and predictability. Applied Animal Behaviour Science 1999, 65:191-220.
26. Grafen A., Hails R. Modern Statistics for the Life Sciences 2002, Oxford University Press, Oxford.
27. Hadley C., Hadley B., Ephraim S., Yang M., Lewis M.H. Spontaneous stereotypy and environmental enrichment in deer mice (Peromyscus maniculatus): reversibility of experience. Applied Animal Behaviour Science 2006, 97:312-322.
28. Herrera-Pérez J.J., Martínez-Mota L., Fernández-Guasti A. Aging increases the susceptibility to develop anhedonia in male rats. Progress in Neuro-Psychopharmacology & Biological Psychiatry 2008, 32:1798-1803.
29. Hotz G., Helm-Estabrooks N. Perseveration. Part I: a review. Brain Injury 1995, 9:151-159.
30. Hursh S.R. Economic concepts for the analysis of behavior. Journal of the Experimental Analysis of Behavior 1980, 34:219-238.
31. Hutt C. Exploration, arousal and autism. Psychologische Forschung 1969, 33:1-8.
32. Imhof J.T., Coelho Z.M.I., Schmitt M.L., Morato G.S., Carobrez A.P. Influence of gender and age on performance of rats in the elevated plus maze apparatus. Behavioural Brain Research 1993, 56:177-180.
33. Kennes D., Ödberg F.O., Bouquet Y., De Rycke P.H. Changes in naloxone and haloperidol effects during the development of captivity-induced jumping stereotypy in bank voles. European Journal of Pharmacology 1988, 153:19-24.
34. Kurt F., Hartl G.B. Asian elephants (Elephas maximus) in captivity: a challenge for zoo biological research. Research and Captive Propagation 1995, 310-326. Filander Verlag, Fürth. U. Ganslosser, J.K. Hodges, W. Kaumanns (Eds.).
35. Latham, N. R. 2004. Refining the role of stereotypic behaviour in the assessment of welfare: stress, general motor persistence and early environment in the development of abnormal behaviours. Ph.D. thesis, University of Oxford.
36. Latham N., Mason G. Frustration and perseveration in stereotypic captive animals: is a taste of enrichment worse than none at all?. Behavioural Brain Research 2010, 211:96-104.
37. Lewis M.H., Tanimura Y., Lee L.W., Bodfish J.W. Animal models of restricted repetitive behavior in autism. Behavioural Brain Research 2007, 176:66-74.
38. Line S.W., Morgan K.N., Markowitz H. Simple toys do not alter the behavior of aged rhesus monkeys. Zoo Biology 1991, 10:473-484.
39. Loh E.A., Roberts D.C.S. Break-points on a progressive ratio schedule reinforced by intravenous cocaine increase following depletion of forebrain serotonin. Psychopharmacology 1990, 101:262-266.
40. Martin P., Bateson P. Measuring Behaviour: An Introductory Guide 2007, Cambridge University Press, Cambridge. 3rd edn.
41. Mason G.J. Stereotypies and suffering. Behavioural Processes 1991, 25:103-115.
42. Mason G.J. Age and context affect the stereotypies of caged mink. Behaviour 1993, 127:191-229.
43. Mason G.J. Stereotypic behaviour in captive animals: fundamentals and implications for welfare and beyond. Stereotypic Animal Behaviour: Fundamentals and Applications to Welfare 2006, 325-356. CABI, Wallingford. 2nd edn. G. Mason, J. Rushen (Eds.).
44. Mason G.J., Latham N.R. Can't stop, won't stop: is stereotypy a reliable animal welfare indicator?. Animal Welfare 2004, 13:S57-S69.
45. Mason G.J., Cooper J., Clarebrough C. Frustrations of fur-farmed mink. Nature 2001, 410:35-36.
46. Mason G., Clubb R., Latham N., Vickery S. Why and how should we use environmental enrichment to tackle stereotypic behaviour?. Applied Animal Behaviour Science 2007, 102:163-188.
47. Meehan C.L., Garner J.P., Mench J.A. Isosexual pair housing improves the welfare of young Amazon parrots. Applied Animal Behaviour Science 2003, 81:73-88.
48. Meyer-Holzapfel M. Abnormal behaviour in zoo animals. Abnormal Behaviour in Animals 1968, 476-503. Saunders, London. M.W. Fox (Ed.).
49. Mirochnic S., Wolf S., Staufenbiel M., Kemperman G. Age effects on the regulation of adult hippocampal neurogenesis by physical activity and environmental enrichment in the APP23 mouse model of Alzheimer disease. Hippocampus 2009, 19:1008-1018.
50. Morris D. The response of animals to a restricted environment. Symposia of the Zoological Society of London 1964, 13:99-118.
51. Nevison C.M., Hurst J.L., Barnard C.J. Strain-specific effects of cage enrichment in male laboratory mice (Mus musculus). Animal Welfare 1999, 8:361-379.
52. Novak M.A., Musante A., Munroe H., O'Neill P.L., Price C., Suomi S.J. Old, socially housed rhesus monkeys manipulate objects. Zoo Biology 1993, 12:285-298.
53. Ödberg F.O. Introduction to round table on abnormal behaviours (stereotypies). Proceedings of the 1st World Congress Ethology Applied to Zootechnics (Editorial Garsi) pp. 475-480 1978, 475-480. Industrias Gráficas España, Madrid.
54. Olsson I.A.S., Keeling L.J. The push-door for measuring motivation in hens: laying hens are motivated to perch at night. Animal Welfare 2002, 11:11-19.
55. Papp M., Willner P., Muscat R. An animal model of anhedonia: attenuation of sucrose consumption and place preference conditioning by chronic unpredictable mild stress. Psychopharmacology 1991, 104:255-259.
56. Pietropaolo S., Branchi I., Chiarotti F., Alleva E. Utilisation of a physically enriched environment by laboratory mice: age and gender differences. Applied Animal Behaviour Science 2004, 88:149-162.
57. Ridderinkhof K.R., Span M.M., van der Molen M.W. Perseverative behavior and adaptive control in older adults: performance monitoring, rule induction, and set shifting. Brain and Cognition 2002, 49:382-401.
58. Roper T.J. Nest material and food as reinforcers for fixed-ratio responding in mice. Learning and Motivation 1975, 6:327-343.
59. Saucier D.M., Yager J.Y., Armstrong E., Keller A., Shultz S. Enriched environment and the effect of age on ischemic brain damage. Brain Research 2007, 1170:31-36.
60. Shepherdson D., Mellen J., Hutchins M. Second Nature: Environmental Enrichment for Captive Animals 1998, Smithsonian Institution Press, Washington.
61. Sherwin C.M. Observations on the prevalence of nest-building in non-breeding TO strain mice and their use of two nesting materials. Laboratory Animals 1997, 31:125-132.
62. Sherwin C.M. Social context affects the motivation of laboratory mice, Mus musculus, to gain access to resources. Animal Behaviour 2003, 66:649-655.
63. Shyne A. Meta-analytic review of the effects of enrichment on stereotypic behavior in zoo mammals. Zoo Biology 2006, 25:317-337.
64. Snaith P. Anhedonia: a neglected symptom of psychopathology. Psychological Medicine 1993, 23:957-966.
65. Sohal R.S., Ferguson M., Sohal B.H., Forster M.J. Life span extension in mice by food restriction depends on an energy imbalance. Journal of Nutrition 2009, 139:533-539.
66. Stevenson M. The captive environment: its effect on exploratory and related behavioural responses in wild animals. Exploration in Animals and Humans 1983, 176-197. Van Nostrand Reinhold, New York. J. Archer, L.I.A. Birke (Eds.).
67. Swaisgood R.R., Shepherdson D.J. Scientific approaches to enrichment and stereotypies in zoo animals: what's been done and where should we go next?. Zoo Biology 2005, 24:499-518.
68. Swaisgood R., Shepherdson D. Environmental enrichment as a strategy for mitigating stereotypies in zoo animals: a literature review and meta-analysis. Stereotypic Animal Behaviour: Fundamentals and Applications to Welfare 2006, 256-285. CABI, Wallingford. 2nd edn. G. Mason, J. Rushen (Eds.).
69. Turner M. Repetitive behaviour in autism: a review of psychological research. Journal of Child Psychology and Psychiatry 1999, 40:839-849.
70. Van de Weerd H.A., Van Loo P.L.P., Van Zutphen L.F.M., Koolhaas J.M., Baumans V. Nesting material as environmental enrichment has no adverse effects on behavior and physiology of laboratory mice. Physiology & Behavior 1997, 62:1019-1028.
71. Van de Weerd H.A., Van Loo P.L.P., Van Zutphen L.F.M., Koolhaas J.M., Baumans V. Strength of preference for nesting material as environmental enrichment for laboratory mice. Applied Animal Behaviour Science 1998, 55:369-382.
72. Van de Weerd H.A., Van Loo P.L.P., Van Zutphen L.F.M., Koolhaas J.M., Baumans V. Preferences for nest boxes as environmental enrichment for laboratory mice. Animal Welfare 1998, 7:11-25.
73. Van de Weerd H.A., Aarsen E.L., Mulder A., Kruitwagen C.L.J.J., Hendriksen C.F.M., Baumans V. Effects of environmental enrichment for mice: variation in experimental results. Journal of Applied Animal Welfare Science 2002, 5:87-109.
74. Van Loo P.L.P., Kruitwagen C.L.J.J., Koolhaas J.M., Van de Weerd H.A., Van Zutphen L.F.M., Baumans V. Influence of cage enrichment on aggressive behaviour and physiological parameters in male mice. Applied Animal Behaviour Science 2002, 76:65-81.
75. Vickery, S. S. 2003. Stereotypic behaviour in caged bears: individual and husbandry factors. Ph.D. thesis, University of Oxford.
76. Weidenmayer C. Causation of the ontogenetic development of stereotypic digging in gerbils. Animal Behaviour 1997, 53:461-470.
77. Würbel H. The motivational basis of caged rodents' stereotypies. Stereotypic Animal Behaviour: Fundamentals and Applications to Welfare 2006, 86-120. CABI, Wallingford. 2nd edn. G. Mason, J. Rushen (Eds.).
78. Würbel H., Chapman R., Rutland C. Effect of feed and environmental enrichment on development of stereotypic wire-gnawing in laboratory mice. Applied Animal Behaviour Science 1998, 60:69-81.
79. Young R.J. Environmental Enrichment for Captive Animals 2003, Universities Federation for Animal Welfare, Wheathampstead.