Cited by 120Animal Behavior and Welfare StudiesAnimal testing and alternativesVeterinary Pharmacology and Anesthesia

Effects of cage enrichment on behavior, welfare and outcome variability in female mice

Open access
Bailoo, Jeremy D., Murphy, Eimear, Boada-Saña, Maria, Varholick, Justin A., Hintze, Sara, Baussière, Caroline, Hahn, Kerstin C., Göpfert, Christine +3 more·2018·Frontiers in Behavioral Neuroscience

Abstract

The manner in which laboratory rodents are housed is driven by economics (minimal use of space and resources), ergonomics (ease of handling and visibility of animals), hygiene, and standardization (reduction of variation). This has resulted in housing conditions that lack sensory and motor stimulation and restrict the expression of species-typical behavior. In mice, such housing conditions have been associated with indicators of impaired welfare, including abnormal repetitive behavior (stereotypies, compulsive behavior), enhanced anxiety and stress reactivity, and thermal stress. However, due to concerns that more complex environmental conditions might increase variation in experimental results, there has been considerable resistance to the implementation of environmental enrichment beyond the provision of nesting material. Here, using 96 C57BL/6 and SWISS female mice, respectively, we systematically varied environmental enrichment across four levels spanning the range of common enrichment strategies: (1) bedding alone; (2) bedding + nesting material; (3) deeper bedding + nesting material + shelter + increased vertical space; and (4) semi-naturalistic conditions, including weekly changes of enrichment items. We studied how these different forms of environmental enrichment affected measures of animal welfare, including home-cage behavior (time-budget and stereotypic behavior), anxiety (open field behavior, elevated plus-maze behavior), growth (food and water intake, body mass), stress physiology (glucocorticoid metabolites in fecal boluses and adrenal mass), brain function (recurrent perseveration in a two-choice guessing task) and emotional valence (judgment bias). Our results highlight the difficulty in making general recommendations across common strains of mice and for selecting enrichment strategies within specific strains. Overall, the greatest benefit was observed in animals housed with the greatest degree of enrichment. Thus, in the super-enriched housing condition, stereotypic behavior, behavioral measures of anxiety, growth and stress physiology varied in a manner consistent with improved animal welfare compared to the other housing conditions with less enrichment. Similar to other studies, we found no evidence, in the measures assessed here, that environmental enrichment increased variation in experimental results.

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Crossref · 10.3389/fnbeh.2018.00232

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92 of 92 references verified0 citation errors · 0 not checkable

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  • Environmental enrichment reduces anxiety and promotes positive affective states in rodents.

    “Environmental enrichment has previously been shown to reduce anxiety and promote positive affective states in rodents [10–12], making it a suitable paradigm to study long-term positive olfactory memory.”

    From Positive early-life olfactory memory is rooted in the olfactory bulb and triggers large-scale changes beyond the olfactory system (2026) · cites this paper as [10]

    The Introduction and Discussion report reduced anxiety-related measures in enriched mice. The Outcome Variables section reports that enriched housing was associated with more optimistic judgments in rats, a measure of emotional valence; the Discussion says this study did not establish a comparable change in emotional valence in mice. The claim therefore overgeneralizes the positive-affect finding to rodents without that qualification. (LLM, conf=0.86)

    Experimental — accuracy not yet measured
  • An enriched playful environment enhances animal well-being.

    “an enriched playful environment, which is reported to enhance animal well-being [10–12].”

    From Positive early-life olfactory memory is rooted in the olfactory bulb and triggers large-scale changes beyond the olfactory system (2026) · cites this paper as [10]

    The Discussion reports improved welfare in female mice housed with the most extensive enrichment. It also says lesser levels of enrichment did not consistently improve welfare. The source therefore supports a qualified claim about extensive cage enrichment in mice, but not the broader implication that enriched environments generally enhance animal well-being; it does not establish a distinct effect of playfulness. (LLM, conf=0.84)

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Research works printed but not linked: 2

  1. National Research Council (2011). Guide for the Care and Use of Laboratory Animals. 8th Edn. Washington, DC: The National Academies Press.
  2. Stauffacher M. (1992). Tiergerechte haltung von hauskaninchen: neue konzepte für die zucht und haltung von labor-und fleischmastkaninchen. Deutsch. Tierarztl. Wochenschr. 99, 9– 15. 1555520

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Authors
Bailoo, J. D., Murphy, E., Boada-Saña, M., Varholick, J. A., Hintze, S., Baussière, C., Hahn, K. C., Göpfert, C., Palme, R., Voelkl, B., & Würbel, H.
Affiliations
  • University of Bern (CH)
  • BOKU University (AT)
  • University of Veterinary Medicine Vienna (AT)
Corresponding author
Bailoo, Jeremy D.
Venue
Frontiers in Behavioral Neuroscience
Published
2018-10-26
Volume
12
Pages
232-232
ISSN
1662-5153 (ISSN-L)
OpenAlex
W2898172643
Cited by
120
References
92
Citations by year
2026: 14 · 2025: 8 · 2024: 23 · 2023: 18 · 2022: 16 · 2021: 18 · 2020: 14 · 2019: 9
FWCI
15.05
Type
journal article
Language
en
Open access
Locations
  • Frontiers in Behavioral Neuroscience (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Bern Open Repository and Information System (University of Bern) (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Open Access CRIS of the University of Bern
Funders
FP7 Ideas: European Research Council (322576)
Topics
  • Health Sciences › Veterinary › Small Animals › Animal Behavior and Welfare Studies
  • Health Sciences › Veterinary › Small Animals › Animal testing and alternatives
  • Health Sciences › Veterinary › Small Animals › Veterinary Pharmacology and Anesthesia
Keywords
cage enrichment, animal welfare, stereotypy, anxiety, stress physiology, glucocorticoid metabolites, adrenal mass, perseveration, judgment bias, nesting material, shelter, vertical space, C57BL/6 mice, Swiss mice, strain differences

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