Cited by 193Animal Behavior and Welfare StudiesAnimal testing and alternativesMemory and Neural Mechanisms

Optimising reliability of mouse performance in behavioural testing: the major role of non-aversive handling

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Gouveia, Kelly, Hurst, Jane L.·2017·Scientific Reports

Abstract

Handling laboratory animals during test procedures is an important source of stress that may impair reliability of test responses. Picking up mice by the tail is aversive, stimulating stress and anxiety. Responses among anxious animals can be confounded further by neophobia towards novel test environments and avoidance of test stimuli in open areas. However, handling stress can be reduced substantially by using a handling tunnel, or cupping mice without restraint on the open hand. Here we establish whether non-aversive handling, brief prior familiarisation with the test arena and alternative stimulus placement could significantly improve performance of mice in behavioural tests. We use a simple habituation-dishabituation paradigm in which animals must discriminate between two urine stimuli in successive trials, a task that mice can easily perform. Tail handled mice showed little willingness to explore and investigate test stimuli, leading to poor test performance that was only slightly improved by prior familiarisation. By contrast, those handled by tunnel explored readily and showed robust responses to test stimuli regardless of prior familiarisation or stimulus location, though responses were more variable for cup handling. Our study shows that non-aversive tunnel handling can substantially improve mouse performance in behavioural tests compared to traditional tail handling.

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  1. Wahlsten D. In Mouse Behavioral Testing: How to Use Mice in Behavioral Neuroscience (ed. Wahlsten D.) 177– 201 (Academic Press, 2011).
  2. Bailey K. R., Rustay N. R. & Crawley J. N. Behavioral phenotyping of transgenic and knockout mice: practical concerns and potential pitfalls. ILAR J 47, 124– 131 (2006). 16547369
  3. Mandillo S.. Reliability, robustness, and reproducibility in mouse behavioral phenotyping: a cross-laboratory study. Physiol Genomics 34, 243– 255, doi: 10.1152/physiolgenomics.90207.2008 (2008). 18505770 PMC2519962 · DOI
  4. Deacon R. M. Housing, husbandry and handling of rodents for behavioral experiments. Nat Protoc 1, 936– 946, doi: 10.1038/nprot.2006.120 (2006). 17406327 · DOI · Paper page
  5. Crabbe J. C., Wahlsten D. & Dudek B. C. Genetics of mouse behavior: Interactions with laboratory environment. Science 284, 1670– 1672 (1999). 10356397
  6. Festing M. F. & Altman D. G. Guidelines for the design and statistical analysis of experiments using laboratory animals. ILAR J 43, 244– 258 (2002). 12391400
  7. van der Staay F. J., Arndt S. S. & Nordquist R. E. Evaluation of animal models of neurobehavioral disorders. Behav Brain Funct 5, 11, doi: 10.1186/1744-9081-5-11 (2009). 19243583 PMC2669803 · DOI
  8. Hurst J. L. & West R. S. Taming anxiety in laboratory mice. Nat Methods 7, 825– 826, doi: 10.1038/nmeth.1500 (2010). 20835246 · DOI · Paper page
  9. Gouveia K. & Hurst J. L. Reducing mouse anxiety during handling: effect of experience with handling tunnels. PLoS One 8, e66401, doi: 10.1371/journal.pone.0066401 (2013). 23840458 PMC3688777 · DOI
  10. Ghosal S.. Mouse handling limits the impact of stress on metabolic endpoints. Physiol Behav 150, 31– 37, doi: 10.1016/j.physbeh.2015.06.021 (2015). 26079207 PMC4546855 · DOI
  11. Turner V. P. In Laboratory Animal Welfare (eds Baynes K. & Turner V. P.) 171– 196 (Academic Press Elsevier, 2013).
  12. Johnston R. E. Memory for individual scent in hamsters (Mesocricetus auratus) as assessed by habituation methods. J Comp Psychol 107, 201– 207 (1993). 8370274
  13. Lee A. W., Emsley J. G., Brown R. E. & Hagg T. Marked differences in olfactory sensitivity and apparent speed of forebrain neuroblast migration in three inbred strains of mice. Neuroscience 118, 263– 270 (2003). 12676156
  14. Schellinck H., Price S. R. & Wong M. J. In Chemical Signals in Vertebrates 11 (eds Hurst J. L., Beynon R. J., Roberts S. G. & Wyatt T. D.) (Springer, 2008).
  15. Moreno M. M.. Olfactory perceptual learning requires adult neurogenesis. Proc Natl Acad Sci USA 106, 17980– 17985, doi: 10.1073/pnas.0907063106 (2009). 19815505 PMC2764902 · DOI
  16. Macknin J. B., Higuchi M., Lee V. M., Trojanowski J. Q. & Doty R. L. Olfactory dysfunction occurs in transgenic mice overexpressing human tau protein. Brain Res 1000, 174– 178, doi: 10.1016/j.brainres.2004.01.047 (2004). 15053964 · DOI
  17. Yang M. & Crawley J. N. Simple behavioral assessment of mouse olfaction. Curr Protoc Neurosci 48, 8.24:28.24.21-28.24.12, doi: 10.1002/0471142301.ns0824s48 (2009). PMC2753229 19575474 · DOI
  18. Martel K. L. & Baum M. J. Sexually dimorphic activation of the accessory, but not the main, olfactory bulb in mice by urinary volatiles. Eur J Neurosci 26, 463– 475, doi: 10.1111/j.1460-9568.2007.05651.x (2007). 17623023 PMC2258410 · DOI
  19. Jakupovic J., Kang N. & Baum M. J. Effect of bilateral accessory olfactory bulb lesions on volatile urinary odor discrimination and investigation as well as mating behavior in male mice. Physiol Behav 93, 467– 473, doi: 10.1016/j.physbeh.2007.10.005 (2008). 17991495 PMC2274908 · DOI
  20. Lehmkuhl A. M., Dirr E. R. & Fleming S. M. Olfactory assays for mouse models of neurodegenerative disease. J Vis Exp, e51804, doi: 10.3791/51804 (2014). PMC4827975 25177842 · DOI
  21. Walsh R. N. & Cummins R. A. The Open-Field Test: a critical review. Psychol Bull 83, 482– 504 (1976). 17582919
  22. Gould T. D., Dao D. T. & Kovacsics C. E. In Mood and Anxiety-related Phenotypes in Mice: Characterization Using Behavioral Tests (ed. Gould T. D.) 1– 20 (Humana Press, 2009).
  23. Bourin M., Petit-Demouliere B., Dhonnchadha B. N. & Hascoet M. Animal models of anxiety in mice. Fundam Clin Pharmacol 21, 567– 574, doi: 10.1111/j.1472-8206.2007.00526.x (2007). 18034657 · DOI
  24. Zanettini C.. Postnatal handling reverses social anxiety in serotonin receptor 1A knockout mice. Genes Brain Behav 9, 26– 32, doi: 10.1111/j.1601-183X.2009.00531.x (2010). 19740091 · DOI
  25. Fridgeirsdottir G. A., Hillered L. & Clausen F. Escalated handling of young C57BL/6 mice results in altered Morris water maze performance. Ups J Med Sci 119, 1– 9, doi: 10.3109/03009734.2013.847511 (2014). 24172203 PMC3916711 · DOI
  26. Leger M.. Object recognition test in mice. Nat Protoc 8, 2531– 2537, doi: 10.1038/nprot.2013.155 (2013). 24263092 · DOI · Paper page
  27. Besheer J. & Bevins R. A. The role of environmental familiarization in novel-object preference. Behavioural Processes 50, 19– 29 (2000). 10925033
  28. Stefanko D. P., Barrett R. M., Ly A. R., Reolon G. K. & Wood M. A. Modulation of long-term memory for object recognition via HDAC inhibition. Proc Natl Acad Sci USA 106, 9447– 9452, doi: 10.1073/pnas.0903964106 (2009). 19470462 PMC2695069 · DOI
  29. Oliveira A. M. M., Hawk J. D., Abel T. & Havekes R. Post-training reversible inactivation of the hippocampus enhances novel object recognition memory. Learning and Memory 17, 155– 160 (2010). 20189960 PMC2832924
  30. Walf A. A. & Frye C. A. The use of the elevated plus maze as an assay of anxiety-related behavior in rodents. Nat Protoc 2, 322– 328, doi: 10.1038/nprot.2007.44 (2007). 17406592 PMC3623971 · DOI · Paper page
  31. Labots M., Van Lith H. A., Ohl F. & Arndt S. S. The modified hole board–measuring behavior, cognition and social interaction in mice and rats. J Vis Exp 98, e52529, doi: 10.3791/52529 (2015). PMC4541485 25938188 · DOI
  32. Hanell A. & Marklund N. Structured evaluation of rodent behavioral tests used in drug discovery research. Front Behav Neurosci 8, 252, doi: 10.3389/fnbeh.2014.00252 (2014). 25100962 PMC4106406 · DOI
  33. Baumans V. Science-based assessment of animal welfare: laboratory animals. Rev Sci Tech 24, 503– 513 (2005). 16358504
  34. Novak J., Bailoo J. D., Melotti L., Rommen J. & Wurbel H. An exploration based cognitive bias test for mice: Effects of handling method and stereotypic behaviour. PLoS One 10, e0130718, doi: 10.1371/journal.pone.0130718 (2015). 26154309 PMC4496074 · DOI
  35. Augustsson H., Dahlborn K. & Meyerson B. J. Exploration and risk assessment in female wild house mice (Mus musculus musculus) and two laboratory strains. Physiol Behav 84, 265– 277, doi: 10.1016/j.physbeh.2004.12.002 (2005). 15708778 · DOI
  36. Depino A. M. & Gross C. Simultaneous assessment of autonomic function and anxiety-related behavior in BALB/c and C57BL/6 mice. Behav Brain Res 177, 254– 260, doi: 10.1016/j.bbr.2006.11.025 (2007). 17204340 · DOI
  37. Roy V., Merali Z., Poulter M. O. & Anisman H. Anxiety responses, plasma corticosterone and central monoamine variations elicited by stressors in reactive and nonreactive mice and their reciprocal F1 hybrids. Behav Brain Res 185, 49– 58, doi: 10.1016/j.bbr.2007.07.008 (2007). 17692933 · DOI
  38. Blanchard R. J., Yudko E. B., Rodgers R. J. & Blanchard D. C. Defense system psychopharmacology: an ethological approach to the pharmacology of fear and anxiety. Behav Brain Res 58, 155– 165 (1993). 7907880
  39. Molewijk H. E., van der Poel A. M. & Olivier B. The ambivalent behaviour “stretched approach posture” in the rat as a paradigm to characterize anxiolytic drugs. Psychopharmacology (Berl) 121, 81– 90 (1995). 8539344

Cited by

Sorted by citations

Authors
Gouveia, K., & Hurst, J. L.
Affiliations
University of Liverpool (GB)
Corresponding author
Hurst, Jane L.
Venue
Scientific Reports
Published
2017-03-21
Volume
7
Issue
1
Pages
44999-44999
ISSN
2045-2322 (ISSN-L)
OpenAlex
W2599467169
Cited by
193
References
1
Citations by year
2026: 18 · 2025: 23 · 2024: 23 · 2023: 18 · 2022: 23 · 2021: 33 · 2020: 25 · 2019: 15 · 2018: 14 · 2017: 1
FWCI
23.79
Type
journal article
Language
en
Open access
Locations
  • Scientific Reports (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Funders
National Centre for the Replacement, Refinement and Reduction of Animals in Research (NC/K500446/1)
Topics
  • Health Sciences › Veterinary › Small Animals › Animal Behavior and Welfare Studies
  • Health Sciences › Veterinary › Small Animals › Animal testing and alternatives
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Keywords
mouse handling, handling stress, anxiety, neophobia, test reliability, habituation-dishabituation, behavioral assessment
MeSH terms
Behavior Rating Scale, Animals, Behavior, Animal, Female, Reproducibility of Results, Mice

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