Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

A mapping review of refinements to laboratory rat housing and husbandry

Abstract

Refining the housing and husbandry of laboratory rats is an important goal, both for ethical reasons and to allow better quality research. We conducted a mapping review of 1,017 studies investigating potential refinements of housing and husbandry of the laboratory rat to assess what refinements have, and have not, been studied, and to briefly assess whether there is evidence to support any impact on rat welfare. Among the many refinements studied, the majority involve changes to the cage, but some also involve alterations to the wider environment. The effects of these refinements were assessed using a range of readouts, many of which are difficult to interpret from a welfare perspective. Preference studies, which are easier to interpret, provide evidence that rats prefer complex environments, including shelters and multiple objects, which offer different areas/resources allowing the rat to engage in diverse behaviors. The reporting of methodology in papers was often poor, indicating that studies were potentially subject to biases. Given that many refinements co-occurred, it was often difficult to tease apart which ones were most beneficial for rat welfare. Effects of refinements were also moderated by a number of factors including age, sex, strain and photoperiod. Altogether our findings show that a one-size-fits-all approach to refinements is not appropriate, because different refinements will impact different rats in different ways. Our review has also produced a database of >1,000 articles that can be used for further and more detailed analyses. Our findings have also highlighted areas where future research is likely to be valuable, including refinements to rat transport, handling and the use of training.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: The literature review process.
Fig. 2: The publication year of included articles.
Fig. 3: The number of articles using different types of refinements.
Fig. 4: The number of articles using each of the top 30 most common outcome measures (excluding preference).
Fig. 5: The number of articles using different measures of preference across the different refinements.

Similar content being viewed by others

Data availability

Data are provided in Supplementary Table 1.

References

  1. Report from the Commision to the European Parliament and the Council on the Implementation of Directive 2010/63/EU on the Protection of Animals Used for Scientific Purposes in the Member States of the European Union (European Commission, 2020).

  2. Poole, T. Happy animals make good science. Lab. Anim. 31, 116–124 (1997).

    Article  CAS  PubMed  Google Scholar 

  3. Prescott, M. J. & Lidster, K. Improving quality of science through better animal welfare: the NC3Rs strategy. Lab Anim. 46, 152–156 (2017).

    Article  Google Scholar 

  4. Cait, J., Cait, A., Scott, R. W., Winder, C. B. & Mason, G. J. Conventional laboratory housing increases morbidity and mortality in research rodents: results of a meta-analysis. BMC Biol. 20, 1–22 (2022).

    Article  Google Scholar 

  5. Ormandy, E. H. & Schuppli, C. A. Public attitudes toward animal research: a review. Animals 4, 391–408 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  6. Voelkl, B. et al. Reproducibility of animal research in light of biological variation. Nat. Rev. Neurosci. 21, 384–393 (2020).

    Article  CAS  PubMed  Google Scholar 

  7. Jilka, R. L. The road to reproducibility in animal research. J. Bone Miner. Res. 31, 1317–1319 (2016).

    Article  PubMed  Google Scholar 

  8. Meerpohl, J. J., Herrle, F., Antes, G. & von Elm, E. Scientific value of systematic reviews: survey of editors of core clinical journals. PLoS ONE 7, 3–7 (2012).

    Article  Google Scholar 

  9. O’Hagan, E. C., Matalon, S. & Riesenberg, L. A. Systematic reviews of the literature: a better way of addressing basic science controversies. Am. J. Physiol. Lung Cell. Mol. Physiol. 314, L439–L442 (2018).

    Article  PubMed  Google Scholar 

  10. Mason, G. & Mendl, M. Why is there no simple way of measuring animal welfare? Anim. Welf. 2, 301–319 (1993).

    Article  Google Scholar 

  11. Broom, D. M. Considering animals’ feelings. Anim. Sentience 5, 1–12 (2016).

    Google Scholar 

  12. Dawkins, M. S. The science of animal suffering. Ethology 114, 937–945 (2008).

    Article  Google Scholar 

  13. Mendl, M. & Paul, E. S. Consciousness, emotion and animal welfare: insights from cognitive science. Anim. Welf. 13, 17–25 (2004).

    Article  Google Scholar 

  14. Browning, H. The natural behavior debate: two conceptions of animal welfare. J. Appl. Anim. Welf. Sci. 23, 325–337 (2020).

    Article  CAS  PubMed  Google Scholar 

  15. Mendl, M. Assessing the welfare state. Nature 410, 31–32 (2001).

    Article  CAS  PubMed  Google Scholar 

  16. Broom, D. M. The scientific assessment of animal welfare. Appl. Anim. Behav. Sci. 20, 5–19 (1988).

    Article  Google Scholar 

  17. Mendl, M. & Paul, E. S. Animal affect and decision-making. Neurosci. Biobehav. Rev. 112, 144–163 (2020).

    Article  PubMed  Google Scholar 

  18. Paul, E. S., Harding, E. J. & Mendl, M. Measuring emotional processes in animals: the utility of a cognitive approach. Neurosci. Biobehav. Rev. 29, 469–491 (2005).

    Article  PubMed  Google Scholar 

  19. Overstreet, D. H. Modeling depression in animal models. Methods Mol. Biol. 829, 125–144 (2012).

    Article  CAS  PubMed  Google Scholar 

  20. Willner, P., Muscat, R. & Papp, M. Chronic mild stress-induced anhedonia: a realistic animal model of depression. Neurosci. Biobehav. Rev. 16, 525–534 (1992).

    Article  CAS  PubMed  Google Scholar 

  21. Lagisz, M. et al. Optimism, pessimism and judgement bias in animals: a systematic review and meta-analysis. Neurosci. Biobehav. Rev. 118, 3–17 (2020).

    Article  PubMed  Google Scholar 

  22. McArthur, R. & Borsini, F. Animal models of depression in drug discovery: a historical perspective. Pharmacol. Biochem. Behav. 84, 436–452 (2006).

    Article  CAS  PubMed  Google Scholar 

  23. Willner, P. The validity of animal models of depression. Psychopharmacology 83, 1–16 (1984).

    Article  CAS  PubMed  Google Scholar 

  24. Neville, V. et al. Pharmacological manipulations of judgement bias: a systematic review and meta-analysis. Neurosci. Biobehav. Rev. 108, 269–286 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Fraser, D. & Matthews, L. R. in Animal Welfare (eds Appleby, M. C. & Hughes, B. O.) 159–173 (CAB International, 1997).

  26. Hughes, B. O. & Duncan, I. J. H. The notion of ethological ‘need’, models of motivation and animal welfare. Anim. Behav. 36, 1696–1707 (1988).

    Article  Google Scholar 

  27. Sherwin, C. M. & Nicol, C. J. Behavioural demand functions of caged laboratory mice for additional space. Anim. Behav. 53, 67–74 (1997).

    Article  Google Scholar 

  28. Sherwin, C. & Nicol, C. A demanding task: using economic techniques to assess animal priorities. A reply to Mason et al. Anim. Behav. 55, 1079–1081 (1998).

    Article  CAS  PubMed  Google Scholar 

  29. Dawkins, M. S. From an animal’s point of view: motivation, fitness, and animal welfare. Behav. Brain Sci. 13, 1–61 (1990).

    Article  Google Scholar 

  30. Rolls, E. T. Emotion and Decision-Making Explained (Oxford Univ. Press, 2014).

  31. Paul, E. S. & Mendl, M. T. Animal emotion: descriptive and prescriptive definitions and their implications for a comparative perspective. Appl. Anim. Behav. Sci. 205, 202–209 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  32. Leenaars, C. et al. Reviewing the animal literature: how to describe and choose between different types of literature reviews. Lab. Anim. 55, 129–141 (2021).

    Article  CAS  PubMed  Google Scholar 

  33. Smith, A. J., Clutton, R. E., Lilley, E., Hansen, K. E. A. & Brattelid, T. PREPARE: guidelines for planning animal research and testing. Lab. Anim. 52, 135–141 (2018).

    Article  CAS  PubMed  Google Scholar 

  34. du Sert, N. P. et al. Reporting animal research: explanation and elaboration for the arrive guidelines 2.0. PLoS Biol. 18, e3000411 (2020).

  35. Bradshaw, A. L. & Poling, A. Choice by rats for enriched versus standard home cages: plastic pipes, wood platforms, wood chips, and paper towels as enrichment items. J. Exp. Anal. Behav. 55, 245–250 (1991).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Chmiel, D. J. Jr. et al. Preference of laboratory rats for potentially enriching stimulus objects. Lab. Anim. 30, 97–101 (1996).

    Article  PubMed  Google Scholar 

  37. Denny, M. S. The rat’s long-term preference for complexity in its environment. Anim. Learn. Behav. 3, 245–249 (1975).

    Article  Google Scholar 

  38. Williams, C. M., Riddell, P. M. & Scott, L. A. Comparison of preferences for object properties in the rat using paired- and free-choice paradigms. Appl. Anim. Behav. Sci. 112, 146–157 (2008).

    Article  Google Scholar 

  39. Williams, C. M., Hanmer, L. A. & Riddell, P. M. The effect of the functional attributes of objects within the caged environment on interaction time in laboratory rats. Appl. Anim. Behav. Sci. 120, 208–215 (2009).

    Article  Google Scholar 

  40. Abou-Ismail, U. A. Are the effects of enrichment due to the presence of multiple items or a particular item in the cages of laboratory rat? Appl. Anim. Behav. Sci. 134, 72–82 (2011).

    Article  Google Scholar 

  41. Lambert, K. et al. Natural-enriched environments lead to enhanced environmental engagement and altered neurobiological resilience. Neuroscience 330, 386–394 (2016).

    Article  CAS  PubMed  Google Scholar 

  42. Abou-Ismail, U. A. & Mendl, M. T. The effects of enrichment novelty versus complexity in cages of group-housed rats (Rattus norvegicus). Appl. Anim. Behav. Sci. 180, 130–139 (2016).

    Article  Google Scholar 

  43. Will, B., Pallaud, B., Ungerer, A. & Ropartz, P. Effects of rearing in different environments on subsequent environmental preference in rats. Dev. Psychobiol. 12, 151–160 (1979).

    Article  CAS  PubMed  Google Scholar 

  44. De Villiers, C. & Seal, J. V. Solid floor versus wire floor housing for rats revisited: influence of age and the presence of nest boxes. Anim. Technol. Welf. 9, 31–36 (2010).

    Google Scholar 

  45. Townsend, P. Use of in-cage shelters by laboratory rats. Anim. Welf. 6, 95–103 (1997).

    Article  Google Scholar 

  46. Krohn, T. C. et al. The ability of SD-rats to distinguish between three different housing environments. Scand. J. Lab. Anim. Sci. 38, 21 (2011).

    CAS  Google Scholar 

  47. Manser, C. E., Broom, D. M., Overend, P. & Morris, T. H. Investigations into the preferences of laboratory rats for nest-boxes and nesting materials. Lab. Anim. 32, 23–35 (1998).

    Article  CAS  PubMed  Google Scholar 

  48. Collier, G. H., Johnson, D. F., Cybulski, K. A. & McHale, C. A. Activity patterns in rats (Rattus norvegicus) as a function of the cost of access to four resources. J. Comp. Psychol. 104, 53–65 (1990).

    Article  CAS  PubMed  Google Scholar 

  49. Manser, C. E., Broom, D. M., Overend, P. & Morris, T. H. Operant studies to determine the strength of preference in laboratory rats for nest-boxes and nesting materials. Lab. Anim. 32, 36–41 (1998).

    Article  CAS  PubMed  Google Scholar 

  50. Greenwood, B. N. et al. Long-term voluntary wheel running is rewarding and produces plasticity in the mesolimbic reward pathway. Behav. Brain Res. 217, 354–362 (2011).

    Article  PubMed  Google Scholar 

  51. Blom, H. J. M., Van Tintelen, G., Van Vorstenbosch, C. J. A. H. V., Baumans, V. & Beynen, A. C. Preferences of mice and rats for types of bedding material. Lab. Anim. 30, 234–244 (1996).

    Article  CAS  PubMed  Google Scholar 

  52. Krohn, T. C. & Hansen, A. K. Evaluation of corncob as bedding for rodents. Scand. J. Lab. Anim. Sci. 35, 231–236 (2008).

    CAS  Google Scholar 

  53. Ras, T. et al. Rats’ preferences for corn versus wood-based bedding and nesting materials. Lab. Anim. 36, 420–425 (2002).

    Article  CAS  PubMed  Google Scholar 

  54. Van De Weerd, H. A., Van Den Broek, F. A. R. & Baumans, V. Preference for different types of flooring in two rat strains. Appl. Anim. Behav. Sci. 46, 251–261 (1996).

    Article  Google Scholar 

  55. Patterson-Kane, E. G., Hunt, M. & Harper, D. Rats demand social contact. Anim. Welf. 11, 327–332 (2002).

    Article  CAS  Google Scholar 

  56. Sørensen, D. B. et al. Enriching the metabolic cage: effects on rat physiology and behaviour. Anim. Welf. 17, 395–403 (2008).

    Article  Google Scholar 

  57. Kumar, D., Kumar, V. M. & Mallick, H. N. Ambient temperature-dependent thermoregulatory role of REM sleep. J. Therm. Biol 37, 392–396 (2012).

    Article  Google Scholar 

  58. Kumar, D., Mallick, H. N. & Kumar, V. M. Ambient temperature that induces maximum sleep in rats. Physiol. Behav. 98, 186–191 (2009).

    Article  CAS  PubMed  Google Scholar 

  59. Ray, B., Mallick, H. & Kumar, V. M. Role of the medial preoptic area in thermal preference of rats. Indian J. Physiol. Pharmacol. 45, 445–450 (2001).

    CAS  PubMed  Google Scholar 

  60. Refinetti, R. & Horvath, S. M. Thermopreferendum of the rat: inter- and intra-subject variabilities. Behav. Neural Biol. 52, 87–94 (1989).

    Article  CAS  PubMed  Google Scholar 

  61. Briese, E. Rats prefer ambient temperatures out of phase with their body temperature circadian rhythm. Brain Res. 345, 389–393 (1985).

    Article  CAS  PubMed  Google Scholar 

  62. Gordon, C. J. 24-Hour control of body temperature in rats. I. Integration of behavioral and autonomic effectors. Am. J. Physiol. Regul. Integr. Comp. Physiol. 267, R71–R77 (1994).

    Article  CAS  Google Scholar 

  63. Brown, J. W. & Pham-Le, N. M. The effect of thermopreference on circadian thermoregulation in Sprague-Dawley and Fisher 344 rats. J. Therm. Biol 37, 309–315 (2012).

    Article  Google Scholar 

  64. Gordon, C. J. Relationship between preferred ambient temperature and autonomic thermoregulatory function in rat. Am. J. Physiol. Regul. Integr. Comp. Physiol. 252, R1130–R1137 (1987).

    Article  CAS  Google Scholar 

  65. Gordon, C. J., Lee, K. L. A., Chen, T. L. A., Killough, P. & Ali, J. S. Dynamics of behavioral thermoregulation in the rat. Am. J. Physiol. Regul. Integr. Comp. Physiol. 261, 705–711 (1991).

    Article  Google Scholar 

  66. Gordon, C. J. Simultaneous measurement of preferred ambient temperature and metabolism in rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 254, R229–R234 (1988).

    Article  CAS  Google Scholar 

  67. Villarreal, J. A. et al. Thermal environment affects morphological and behavioral development of Rattus norvegicus. Physiol. Behav. 91, 26–35 (2007).

    Article  CAS  PubMed  Google Scholar 

  68. Jans, J. E. & Leon, M. Determinants of mother–young contact in Norway rats. Physiol. Behav. 30, 919–935 (1983).

    Article  CAS  PubMed  Google Scholar 

  69. Hillebrand, J. J. G. et al. Voluntary access to a warm plate reduces hyperactivity in activity-based anorexia. Physiol. Behav. 85, 151–157 (2005).

    Article  CAS  PubMed  Google Scholar 

  70. Manser, C. E., Morris, T. H. & Broom, D. M. An investigation into the effects of solid or grid cage flooring on the welfare of laboratory rats. Lab. Anim. 29, 353–363 (1995).

    Article  CAS  PubMed  Google Scholar 

  71. Manser, C. E., Elliott, H., Morris, H. & Broom, D. M. The use of a novel operant test to determine the strength of preference for flooring in laboratory rats. Lab. Anim. 30, 1–6 (1996).

    Article  CAS  PubMed  Google Scholar 

  72. Krohn, T. C. & Hansen, A. K. Weighing used for the automatic registration of preferences when testing rats. Scand. J. Lab. Anim. Sci. 28, 223–229 (2001).

    Google Scholar 

  73. Syme, L. A. & Syme, G. J. Spatial interaction between cage and test environments: position preferences of young isolated and pair-housed rats. Anim. Learn. Behav. 4, 396–400 (1976).

    Article  Google Scholar 

  74. Heikkilä, M., Sarkanen, R., Voipio, H. M., Mering, S. & Nevalainen, T. Cage position preferences of rats. Scand. J. Lab. Anim. Sci. 28, 65–74 (2001).

    Google Scholar 

  75. Voipio, H. M. et al. Cage material and food hopper as determinants. Scand. J. Lab Anim. Sci. 35, 69–77 (2008).

    CAS  Google Scholar 

  76. Blom, H. J. M., Van, G. T., Baumans, V., Van Den, B. J. & Beynen, A. C. Development and application of a preference test system to evaluate housing conditions for laboratory rats. Appl. Anim. Behav. Sci. 43, 279–290 (1995).

    Article  Google Scholar 

  77. Le Magnen, J. Effect of a multiplicity of food stimuli on the amount eaten by the rat. Appetite 33, 36–39 (1999).

    Article  PubMed  Google Scholar 

  78. Naim, M., Brand, J. G., Christensen, C. M., Kare, M. R. & Van Buren, S. Preference of rats for food flavors and texture in nutritionally controlled semi-purified diets. Physiol. Behav. 37, 15–21 (1986).

    Article  CAS  PubMed  Google Scholar 

  79. Wadhera, D. et al. The rewarding effects of number and surface area of food in rats. Learn. Behav. 46, 242–255 (2018).

    Article  PubMed  Google Scholar 

  80. Hegab, I. M. et al. Effects of physical attributes and chemical composition of novel foods on food selection by Norway rats (Rattus norvegicus). J. Pest Sci. 87, 99–106 (2014).

    Article  Google Scholar 

  81. Welker, W. I. & King, W. A. Effects of stimulus novelty on gnawing and eating by rats. J. Comp. Physiol. Psychol. 55, 838–842 (1962).

    Article  CAS  PubMed  Google Scholar 

  82. Johnson, S. R., Patterson-Kane, E. G. & Niel, L. Foraging enrichment for laboratory rats. Anim. Welf. 13, 305–312 (2004).

    Article  CAS  Google Scholar 

  83. Labouré, H., Saux, S. & Nicolaidis, S. Effects of food texture change on metabolic parameters: short- and long-term feeding patterns and body weight. Am. J. Physiol. Regul. Integr. Comp. Physiol. 280, 780–789 (2001).

    Article  Google Scholar 

  84. Sako, N., Okamoto, K., Mori, T. & Yamamoto, T. The hardness of food plays an important role in food selection behavior in rats. Behav. Brain Res. 133, 377–382 (2002).

    Article  PubMed  Google Scholar 

  85. Burgdorf, J. & Panksepp, J. Tickling induces reward in adolescent rats. Physiol. Behav. 72, 167–173 (2001).

    Article  CAS  PubMed  Google Scholar 

  86. Bombail, V. et al. Odour conditioning of positive affective states: rats can learn to associate an odour with being tickled. PLoS ONE 14, 1–17 (2019).

    Article  Google Scholar 

  87. Paredes-Ramos, P. et al. Tickling in juvenile but not adult female rats conditions sexual partner preference. Physiol. Behav. 107, 17–25 (2012).

    Article  CAS  PubMed  Google Scholar 

  88. Krohn, T. C., Hansen, A. K. & Dragsted, N. The impact of cage ventilation on rats housed in IVC systems. Lab. Anim. 37, 85–93 (2003).

    Article  CAS  PubMed  Google Scholar 

  89. Krohn, T. C., Hansen, A. K. & Dragsted, N. The impact of low levels of carbon dioxide on rats. Lab. Anim. 37, 94–99 (2003).

    Article  CAS  PubMed  Google Scholar 

  90. Patterson-Kane, E. G., Hunt, M. & Harper, D. Short communication: rat’s demand for group size. J. Appl. Anim. Welf. Sci. 7, 267–272 (2004).

    Article  CAS  PubMed  Google Scholar 

  91. Sorensen, D. et al. Preferences for limited versus no contact in SD rats. Lab. Anim. 44, 274–277 (2010).

    Article  PubMed  Google Scholar 

  92. Cloutier, S. & Newberry, R. C. Physiological and behavioural responses of laboratory rats housed at different tier levels and levels of visual contact with conspecifics and humans. Appl. Anim. Behav. Sci. 125, 69–79 (2010).

    Article  Google Scholar 

  93. Krohn, T. C., Salling, B. & Hansen, A. K. How do rats respond to playing radio in the animal facility? Lab. Anim. 45, 141–144 (2011).

    Article  CAS  PubMed  Google Scholar 

  94. Marr, J. N. & Gardner, L. E. Early olfactory experience and the later social behavior in the rat: preference, sexual responsiveness, and care of young. J. Genet. Psychol. 107, 167–174 (1965).

    Article  CAS  PubMed  Google Scholar 

  95. Montgomery, K. C. The relation between fear induced by novel stimulation and exploratory drive. J. Comp. Physiol. Psychol. 48, 254 (1955).

    Article  CAS  PubMed  Google Scholar 

  96. Hall, C. S. Emotional behavior in the rat. I. Defecation and urination as measures of individual differences in emotionality. J. Comp. Psychol. 18, 385 (1934).

    Article  Google Scholar 

  97. Pich, E. M. & Samanin, R. A two-compartment exploratory model to study anxiolytic/anxiogenic effects of drugs in the rat. Pharmacol. Res. 21, 595–602 (1989).

    Article  CAS  Google Scholar 

  98. Porsolt, R. D., Anton, G., Blavet, N. & Jalfre, M. Behavioural despair in rats: a new model sensitive to antidepressant treatments. Eur. J. Pharmacol. 47, 379–391 (1978).

    Article  CAS  PubMed  Google Scholar 

  99. Pellow, S., Chopin, P., File, S. E. & Briley, M. Validation of open: closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J. Neurosci. Methods 14, 149–167 (1985).

    Article  CAS  PubMed  Google Scholar 

  100. Prut, L. & Belzung, C. The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review. Eur. J. Pharmacol. 463, 3–33 (2003).

    Article  CAS  PubMed  Google Scholar 

  101. Borsini, F., Podhorna, J. & Marazziti, D. Do animal models of anxiety predict anxiolytic-like effects of antidepressants? Psychopharmacology 163, 121–141 (2002).

    Article  CAS  PubMed  Google Scholar 

  102. Molendijk, M. L. & de Kloet, E. R. Immobility in the forced swim test is adaptive and does not reflect depression. Psychoneuroendocrinology 62, 389–391 (2015).

    Article  PubMed  Google Scholar 

  103. Borsini, F. & Meli, A. Is the forced swimming test a suitable model for revealing antidepressant activity? Psychopharmacology 94, 147–160 (1988).

    Article  CAS  PubMed  Google Scholar 

  104. West, A. P. Neurobehavioral studies of forced swimming: the role of learning and memory in the forced swim test. Prog. Neuropsychopharmacol. Biol. Psychiatry 14, 863–877 (1990).

    Article  CAS  PubMed  Google Scholar 

  105. Carvalho, C., Herrmann, K., Marques, T. A. & Knight, A. Time to abolish the forced swim test in rats for depression research? J. Appl. Anim. Ethics Res. https://doi.org/10.1163/25889567-bja10026 (2021).

  106. Dichter, G. S., Smoski, M. J., Kampov-Polevoy, A. B., Gallop, R. & Garbutt, J. C. Unipolar depression does not moderate responses to the sweet taste test. Depress. Anxiety 27, 859–863 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  107. Berlin, I., Givry-Steiner, L., Lecrubier, Y. & Puech, A. J. Measures of anhedonia and hedonic responses to sucrose in depressive and schizophrenic patients in comparison with healthy subjects. Eur. Psychiatry 13, 303–309 (1998).

    Article  CAS  PubMed  Google Scholar 

  108. Campos, A. C., Fogaça, M. V., Aguiar, D. C. & Guimarães, F. S. Animal models of anxiety disorders and stress. Rev. Bras. Psiquiatr. 35, 101–111 (2013).

    Article  Google Scholar 

  109. Krohn, T. C., Hejgaard, K. & Hansen, A. K. Methods for general assessment of the welfare of laboratory rats. Acta Agric. Scand. A 51, 118–123 (2001).

    Google Scholar 

  110. Ralph, C. R. & Tilbrook, A. J. Invited review: the usefulness of measuring glucocorticoids for assessing animal welfare. J. Anim. Sci. 94, 457–470 (2016).

    Article  CAS  PubMed  Google Scholar 

  111. Ruhé, H. G., Mason, N. S. & Schene, A. H. Mood is indirectly related to serotonin, norepinephrine and dopamine levels in humans: a meta-analysis of monoamine depletion studies. Mol. Psychiatry 12, 331–359 (2007).

    Article  PubMed  Google Scholar 

  112. Perona, M. T. G. et al. Animal models of depression in dopamine, serotonin, and norepinephrine transporter knockout mice: prominent effects of dopamine transporter deletions. Behav. Pharmacol. 19, 566–574 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Shohayeb, B., Diab, M., Ahmed, M. & Ng, D. C. H. Factors that influence adult neurogenesis as potential therapy. Transl. Neurodegener. 7, 4 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  114. Paul, E. S. et al. Assessing animal welfare: a triangulation of preference, judgement bias and other candidate welfare indicators. Anim. Behav. 186, 151–177 (2022).

    Article  Google Scholar 

  115. Leung, V., Rousseau-Blass, F., Beauchamp, G. & Pang, D. S. J. Arrive has not arrived: support for the ARRIVE (animal research: reporting of in vivo experiments) guidelines does not improve the reporting quality of papers in animal welfare, analgesia or anesthesia. PLoS ONE 13, 1–13 (2018).

    Article  Google Scholar 

  116. Code of Practice for the Housing and Care of Animals Bred, Supplied or Used for Scientific Purposes (United Kingdom Home Office, 2014).

  117. Clarkson, J. M., Dwyer, D. M., Flecknell, P. A., Leach, M. C. & Rowe, C. Handling method alters the hedonic value of reward in laboratory mice. Sci. Rep. 8, 1–8 (2018).

    Article  Google Scholar 

  118. Gouveia, K. & Hurst, J. L. Reducing mouse anxiety during handling: effect of experience with handling tunnels. PLoS ONE 8, e66401 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Gouveia, K. & Hurst, J. L. Improving the practicality of using non-aversive handling methods to reduce background stress and anxiety in laboratory mice. Sci. Rep. 9, 1–19 (2019).

    Article  Google Scholar 

  120. Hurst, J. L. & West, R. S. Taming anxiety in laboratory mice. Nat. Methods 7, 825–826 (2010).

    Article  CAS  PubMed  Google Scholar 

  121. Leidinger, C. S., Kaiser, N., Baumgart, N. & Baumgart, J. Using clicker training and social observation to teach rats to voluntarily change cages. J. Vis. Exp. https://doi.org/10.3791/58511 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  122. Schapiro, S. J., Perlman, J. E., Thiele, E. & Lambeth, S. Training nonhuman primates to perform behaviors useful in biomedical research. Lab Anim. 34, 37–42 (2005).

    Article  Google Scholar 

  123. Laule, G. & Whittaker, M. Enhancing nonhuman primate care and welfare through the use of positive reinforcement training. J. Appl. Anim. Welf. Sci. 10, 31–38 (2007).

    Article  CAS  PubMed  Google Scholar 

  124. Rutledge, R. B., Skandali, N., Dayan, P. & Dolan, R. J. A computational and neural model of momentary subjective well-being. Proc. Natl Acad. Sci. USA 111, 12252–12257 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Eldar, E., Rutledge, R. B., Dolan, R. J. & Niv, Y. Mood as representation of momentum. Trends Cogn. Sci. 20, 15–24 (2015).

    Article  PubMed  Google Scholar 

  126. Bassett, L. & Buchanan-Smith, H. M. Effects of predictability on the welfare of captive animals. Appl. Anim. Behav. Sci. 102, 223–245 (2007).

    Article  Google Scholar 

  127. Joffe, J. M., Rawson, R. A. & Mulick, J. A. Control of their environment reduces emotionality in rats. Science 180, 1383–1384 (1973).

    Article  CAS  PubMed  Google Scholar 

  128. Swanson, J. C. & Morrow-Tesch, J. Cattle transport: historical, research, and future perspectives. J. Anim. Sci. 79, E102 (2001).

    Article  Google Scholar 

  129. de Witte, K. Development of the Australian Animal Welfare Standards and Guidelines for the Land Transport of Livestock: process and philosophical considerations. J. Vet. Behav. Clin. Appl. Res. 4, 148–156 (2009).

    Article  Google Scholar 

  130. Knutson, B., Burgdorf, J. & Panksepp, J. Ultrasonic vocalizations as indices of affective states in rats. Psychol. Bull. 128, 961–977 (2002).

    Article  PubMed  Google Scholar 

  131. Brudzynski, S. M. Biological functions of rat ultrasonic vocalizations, arousal mechanisms, and call initiation. Brain Sci. 11, 605 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  132. Coffey, K. R., Marx, R. G. & Neumaier, J. F. DeepSqueak: a deep learning-based system for detection and analysis of ultrasonic vocalizations. Neuropsychopharmacology 44, 859–868 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  133. Ouzzani, M., Hammady, H., Fedorowicz, Z. & Elmagarmid, A. Rayyan—a web and mobile app for systematic reviews. Syst. Rev. 5, 1–10 (2016).

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by the UK Biotechnology and Biological Sciences Research Council (BBSRC) grant BB/T002654/1 (principal investigator: M.M.) and a Universities Federation for Animal Welfare (UFAW) small project award (principal investigator: V.N.). For the purpose of open access, the authors have applied a Creative Commons Attribution (CC BY) licence to any Author Accepted Manuscript version arising.

Author information

Authors and Affiliations

Authors

Contributions

V.N., E.S.P. and M.M. were responsible for conceptualization and methodology. V.N., J.L., E.M. and N.E.C. were responsible for data collection. V.N. analyzed the data and wrote the original draft. All authors wrote, reviewed and edited the manuscript.

Corresponding author

Correspondence to Vikki Neville.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Lab Animal thanks Cathalijn Leenaars, Patricia Turner and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Text 1.

Supplementary Tables

Supplementary Tables 1–4.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Neville, V., Lind, J., Mendl, E. et al. A mapping review of refinements to laboratory rat housing and husbandry. Lab Anim 52, 63–74 (2023). https://doi.org/10.1038/s41684-023-01124-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41684-023-01124-1

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing