Spontaneous stereotypy and environmental enrichment in deer mice (Peromyscus maniculatus): Reversibility of experience

Applied Animal Behaviour Science

Pillay

2011

a b s t r a c tUnderstanding how birth origin (whether born in the wild or captivity) influences behavioural development is important for fundamental and applied ethology, especially when captive-bred (CB) individuals from wild species are used in research or conservation. CB animals are typically much more prone to stereotypic behaviour (SB) than are wild caught (WC) conspecifics, an effect which in striped mice is accompanied by increased tendencies to form behavioural routines. However, WC mice, if stereotypic, are far more severely affected than CB mice and are also more physiologically stressed and inactive than CB mice, regardless of their stereotypy status. Capturing subjects from the wild to further study these latter effects raises serious practical, ethical and potentially conservation concerns. Here, we therefore tested whether rearing CB striped mice in enriched conditions and then placing them in standard cages could provide a more suitable model for investigating how wild-caught (WC) conspecifics respond to the reduced environmental complexity they experience after capture. Compared with striped mice which were always standard-housed (n = 36), enriched striped mice (n = 24) were four times less likely to develop SB and, similarly to the benefits of being wild born, early environmental enrichment (30-170 days) successfully protected CB striped mice from the emergence of SB after transfer to standard caging (171-240 days). However, unlike WC mice, previously enriched CB striped mice which then became stereotypic did not develop markedly more severe SBs; they showed diverse forms, unlike stereotypic WC mice which exclusively circuit ran; and they were not more inactive once SB levels were controlled for. These findings thus show that early environmental complexity can have lasting suppressive effects on SB, suggesting that early enrichment protocols could indeed provide a practicable, potentially more ethical model for investigating the causal mechanisms underpinning birth origin effects on SB. Furthermore, they add to a corpus of data for this species showing that more naturalistic early experiences, both social and physical, lastingly protect against SB development. These results also highlight how unpredictable and poorly understood early enrichment effects are (since in some species early enrichment exacerbates later SB); and moreover reveal that early environmental complexity is not the sole factor shaping behavioural phenotypes in WC animals, with differential social experience and human contact being other likely causes of developmental divergence.

Section: Discussionmentioning

confidence: 99%

Early environmental enrichment protects captive-born striped mice against the later development of stereotypic behaviour

Jones

Applied Animal Behaviour Science

Pillay

2011

“…The beneficial effects of added enrichments vary in magnitude: different enrichments vary in efficacy [47,49,50] and individuals vary in their responses, e.g. elderly animals' stereotypic behaviours are often resistant to enrichment [4,14,54]. However, the direction of effects is largely consistent: stereotypic behaviours are almost always attenuated by the addition of enrichments, and sometimes even abolished altogether.…”

Section: Introductionmentioning

confidence: 99%

“…Furthermore, to complicate the picture further, in yet other cases environmental enrichment can appear to protect animals against later developing stereotypic behaviour, even after its removal. Thus in many mammalian species, individuals caught from the wild and caged as adults are less stereotypic than captive-born conspecifics (reviewed [24]); while bank voles (Clethrionomys glareolus) and deer mice (Peromyscus maniculatus) reared in large, enriched cages remain less stereotypic when transferred to standard cages than conspecifics housed in such conditions all their lives [14,34,38]. Thus removing enrichments has inconsistent effects, variously increasing or decreasing stereotypic behaviour relative to animals exposed to life-long barren housing.…”

Section: Introductionmentioning

confidence: 99%

Frustration and perseveration in stereotypic captive animals: Is a taste of enrichment worse than none at all?

Latham

Behavioural Brain Research

2010

a b s t r a c tStereotypic behaviours are common in animals in impoverished housing, arising from two complementary processes: (1) thwarted attempts to perform motivated behaviours; (2) forebrain dysfunction impeding normal behavioural inhibition. When enriched animals are moved to impoverished housing, they are sometimes protected against developing stereotypic behaviour, but in other cases become even more stereotypic than animals housed lifelong without enrichment. Negative contrast-induced frustration must occur in both scenarios. We hypothesise that sustained behavioural responses to this frustration are prevented in the former by normalised forebrain function, but exacerbated in the latter by forebrain dysfunction. ICRCD-1 mice reared in enriched or standard cages were re-caged at 3 months to standard conditions. Here, previously-enriched mice became far more stereotypic than mice reared from birth in such conditions. To investigate the role of frustration, we assessed both corticosterone output and motivation (break-point) to regain enrichments. We also assessed perseveration via extinction learning. As predicted, previously-enriched mice were as perseverative as standard-raised mice, and frustration seemed to play a causal role in their exacerbated stereotypic behaviour. Previously-enriched mice showed higher motivations to access enrichments, and only in this group did these correlate with corticosterone levels after re-caging; furthermore only in previously-enriched mice did corticosterone responses to re-caging predict stereotypic behaviour 30 days later (males only). All results need replicating and further investigation. However, they suggest for the first time that individual risk factors related to the HPA axis predict stereotypic behaviour following enrichment-removal, and that previously-enriched mice have lasting motivational differences from standard-raised mice, suggesting sustained behavioural effects related to the frustration of enrichment-loss.

“…Rodents with anhedonia, as can be induced by long-term impoverished caging [26] and also varies with strain [27] may also fail to show much interaction with enrichments that to other rodents act as valued incentives. Overall, variation between rodents in neophobia and anhedonia may thus help explain why not just strain, but also sex, age and individual characteristics can influence experimental outcomes, even when enrichments are carefully standardized [28][29][30][31][32][33][34][35]. Here, we therefore used individual variation in responses to standardized enrichments to conduct preliminary tests of the hypotheses that neophobia and anhedonia affect the extent to which mice interact with environmental enrichments.…”

mentioning

confidence: 99%

Reprint of Female C57BL/6 mice show consistent individual differences in spontaneous interaction with environmental enrichment that are predicted by neophobia

Walker

Behavioural Brain Research

2012

a b s t r a c tEnvironmental enrichment typically improves learning, increases cortical thickness and hippocampal neurogenesis, reduces anxiety, and reduces stereotypic behaviour, yet sometimes such effects are absent or even reversed. We investigated whether neophobia governs how mice interact with enrichments, since this could explain why enrichments vary in impact. Female C57BL/6 mice, previously screened for neophobia, had free access to enriched cages connected to their standard cages. The relative consumption of food in each cage revealed approximate dwelling times; the use of two enrichments was also measured. High neophobia significantly predicted reduced use of the enriched cage. Thus even within this homogeneous population, provided with identical enrichments, differential neophobia predicted differential enrichment use.