Cited by 18Animal Behavior and Welfare StudiesAnimal testing and alternativesVeterinary Pharmacology and Anesthesia

The use of ball pits and playpens in laboratory Lister Hooded male rats induces ultrasonic vocalisations indicating a more positive affective state and can reduce the welfare impacts of aversive procedures.

Open access
Hinchcliffe, Justyna K, Jackson, Megan G, Robinson, Emma SJ·2022·Laboratory Animals

Abstract

The advancement and quality of science rely on research that is robust and unbiased in its experimental design, execution, analysis, and reproducibility. In preclinical research, a better understanding of animal emotions and refinement of their husbandry, housing, and handling are important goals in providing good animal welfare in a laboratory setting which underpins rigorous research quality. Induction of positive emotional state in animals is a key component of their well-being, and one approach is to increase their environmental complexity using, for example, ball pits or playpens in rats. In this study, we recorded 50 kHz ultrasonic vocalisations (USVs) during animals’ exposure to the ball pit and playpen. We have previously shown that 50 kHz USVs provide a graded and quantifiable measure of an animal’s emotional state, and here find that access to the ball pit and playpen increases 50 kHz USVs, indicative of a more positive affective state. Using our affective bias test (ABT) we next quantified the animals’ emotional response to an aversive intervention and whether this could be attenuated by access to a playpen. The playpen exposure completely mitigated the negative affective state induced by an anxiogenic drug when compared with animals who experienced the drug in the home cage. Together, these findings suggest ball pits and playpens provide a simple and effective method to improve the welfare of laboratory rats and reduce the cumulative suffering they experience from their housing conditions and minor, aversive procedures.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1177/00236772211065920

Cites

2 of 2 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 24

  1. [1]Paul ES Harding EJ Mendl M. Measuring emotional processes in animals: The utility of a cognitive approach. Neurosci Biobehav Rev 2005; 29: 469– 491. 15820551
  2. [2]Mendl M Burman OH Paul ES. An integrative and functional framework for the study of animal emotion and mood. Proc Biol Sci 2010; 277: 2895– 2904. 20685706 PMC2982018
  3. [3]Burgdorf J Panksepp J. Tickling induces reward in adolescent rats. Physiol Behav 2001; 72: 167– 173. 11239994
  4. [5]Knutson B Burgdorf J Panksepp J. Ultrasonic vocalizations as indices of affective states in rats. Psychol Bull 2002; 128: 961– 977. 12405139
  5. [7]Hinchcliffe JK Mendl M Robinson ESJ. Rat 50 kHz calls reflect graded tickling-induced positive emotion. Curr Biol 2020; 30: R1034– R1035. 32961155 PMC7533284
  6. [9]National Centre for the Replacement, Refinement and Reduction of Animals in Research (NC3Rs); https://www.nc3rs.org.uk/iat-congress-2017-workshop-summary-playtime-rats (accessed 21 September 2021).
  7. [10]Makowska IJ Weary DM. The importance of burrowing, climbing and standing upright for laboratory rats. R Soc Open Sci 2016; 3: 160136. 27429772 PMC4929907
  8. [11]Baumans V. Environmental enrichment for laboratory rodents and rabbits: Requirements of rodents, rabbits, and research. Ilar J 2005; 46: 162– 170. 15775025
  9. [12]Morton DB, Jennings M, Batchelor GR. Refinements in rabbit husbandry: Second report of the BVAAWF/FRAME/RSPCA/UFAW joint working group on refinement. Lab Anim 1993; 27: 301– 329. 8277705
  10. [13]Ottesen JL Weber A Gürtler H, et al. New housing conditions: Improving the welfare of experimental animals. Altern Lab Anim 2004; 32 Suppl 1B: 397– 404. 23581108
  11. [14]Honess PE Marin CM. Enrichment and aggression in primates. Neurosci Biobehav Rev 2006; 30: 413– 436. 16055188
  12. [15]Reinhardt V. Environmental enrichment and refinement of handling procedures. In: Wolfe-Coote S (ed) The laboratory primate. New York: Academic Press, 2005. pp. 209– 227.
  13. [16]Stuart SA Butler P Munafo MR, et al. A translational rodent assay of affective biases in depression and antidepressant therapy. Neuropsychopharmacology 2013; 38: 1625– 1635. 23503126 PMC3717539
  14. [17]Stuart SA Butler P Munafo MR, et al. Distinct neuropsychological mechanisms may explain delayed- versus rapid-onset antidepressant efficacy. Neuropsychopharmacology 2015; 40: 2165– 2174. 25740288 PMC4487826
  15. [18]Hinchcliffe JK Stuart SA Mendl M, et al. Further validation of the affective bias test for predicting antidepressant and pro-depressant risk: Effects of pharmacological and social manipulations in male and female rats. Psychopharmacology (Berl) 2017; 234: 3105– 3116. 28735366 PMC5597685
  16. [19]Abou-Ismail UA. The effects of cage enrichment on agonistic behaviour and dominance in male laboratory rats (Rattus norvegicus). Res Vet Sci 2011; 90: 346– 351. 20594567
  17. [20]Gonzalez-Lima F Ferchmin PA Eterovic VA, et al. Metabolic activation of the brain of young rats after exposure to environmental complexity. Dev Psychobiol 1994; 27: 343– 351. 8001724
  18. [21]Faherty CJ Kerley D Smeyne RJ. A Golgi-Cox morphological analysis of neuronal changes induced by environmental enrichment. Brain Res Dev Brain Res 2003; 141: 55– 61. 12644248
  19. [22]Leggio MG Mandolesi L Federico F, et al. Environmental enrichment promotes improved spatial abilities and enhanced dendritic growth in the rat. Behav Brain Res 2005; 163: 78– 90. 15913801
  20. [23]Kemppinen N Hau J Meller A, et al. Impact of aspen furniture and restricted feeding on activity, blood pressure, heart rate and faecal corticosterone and immunoglobulin A excretion in rats (Rattus norvegicus) housed in individually ventilated cages. Lab Anim 2010; 44: 104– 112. 19854757
  21. [24]Spangenberg EM Augustsson H Dahlborn K, et al. Housing-related activity in rats: Effects on body weight, urinary corticosterone levels, muscle properties and performance. Lab Anim 2005; 39: 45– 57. 15703124
  22. [25]van der Harst JE Fermont PCJ Bilstra AE, et al. Access to enriched housing is rewarding to rats as reflected by their anticipatory behaviour. Anim Behav 2003; 66: 493– 504.
  23. [26]Pritchett-Corning KR. Environmental complexity and research outcomes. ILAR J 2020; 60: 239– 251. 32559304
  24. [27]Whittaker AL Hickman DL. The impact of social and behavioral factors on reproducibility in terrestrial vertebrate models. ILAR J 2020; 60: 252– 269. 32720675

Cited by

Sorted by citations

Authors
Hinchcliffe, J. K., Jackson, M. G., & Robinson, E. S.
Affiliations
University of Bristol (GB)
Corresponding author
Robinson, Emma SJ
Venue
Laboratory Animals
Published
2022-01-13
Volume
56
Issue
4
Pages
370-379
ISSN
  • 0023-6772 (ISSN-L)
  • 1758-1117
OpenAlex
W4205294772
Cited by
18
References
2
Citations by year
2026: 2 · 2025: 5 · 2024: 6 · 2023: 3 · 2022: 2
FWCI
4.42
Type
journal article
Language
en
Open access
Locations
  • Laboratory Animals (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Explore Bristol Research (publishedVersion, cc-by)
  • Bristol Research (University of Bristol) (submittedVersion, cc-by)
Funders
  • National Centre for the Replacement Refinement and Reduction of Animals in Research (NC/T001380/1)
  • Biotechnology and Biological Sciences Research Council (BB/N015762/1)
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
playpen, laboratory rats, ultrasonic vocalizations, positive affective states, animal welfare, anxiogenic drugs, environmental enrichment, housing conditions, 3Rs
MeSH terms
Animals, Animal Welfare, Emotions, Male, Ultrasonics, Vocalization, Animal, Reproducibility of Results, Rats

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review