Cited by 52Animal Behavior and Welfare StudiesAnimal testing and alternativesVeterinary Pharmacology and Anesthesia

Tickling, a Technique for Inducing Positive Affect When Handling Rats.

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Cloutier, Sylvie, LaFollette, Megan R., Gaskill, Brianna N., Panksepp, Jaak, Newberry, Ruth C.·2018·Journal of Visualized Experiments

Abstract

Handling small animals such as rats can lead to several adverse effects. These include the fear of humans, resistance to handling, increased injury risk for both the animals and the hands of their handlers, decreased animal welfare, and less valid research data. To minimize negative effects on experimental results and human-animal relationships, research animals are often habituated to being handled. However, the methods of habituation are highly variable and often of limited effectiveness. More potently, it is possible for humans to mimic aspects of the animals' playful rough-and-tumble behavior during handling. When applied to laboratory rats in a systematic manner, this playful handling, referred to as tickling, consistently gives rise to positive behavioral responses. This article provides a detailed description of a standardized rat tickling technique. This method can contribute to future investigations into positive affective states in animals, make it easier to handle rats for common husbandry activities such as cage changing or medical/research procedures such as injection, and be implemented as a source of social enrichment. It is concluded that this method can be used to efficiently and practicably reduce rats' fearfulness of humans and improve their welfare, as well as reliably model positive affective states.

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Research works printed but not linked: 32

  1. Gartner K Buttner D Dohler K Friedel R Lindena J Trautschold I Stress response of rats to handling and experimental procedures Lab Anim 1980 14 3 267 274 7191933
  2. Brudzynski SM Ociepa D Ultrasonic vocalization of laboratory rats in response to handling and touch Physiol Behav 1992 52 4 655 660 1409936
  3. Hurst JL West RS Taming anxiety in laboratory mice Nat Methods 2010 7 10 825 20835246
  4. Burgdorf J Panksepp J Tickling induces reward in adolescent rats Physiol Behav 2001 72 1-2 167 173 11239994
  5. Cloutier S Wahl K Baker C Newberry RC The social buffering effect of playful handling on responses to repeated intraperitoneal injections in laboratory rats J Am Assoc Lab Anim Sci 2014 53 2 168 173 24602543 PMC3966273
  6. Panksepp J Affective neuroscience: The foundations of human and animal emotions 1998 New York, NY Oxford University Press
  7. Panksepp J The ontogeny of play in rats Dev Psychobiol 1981 14 4 327 332 7250521
  8. Lampe JF Burman O Würbel H Melotti L Context-dependent individual differences in playfulness in male rats Dev Psychobiol 2017 59 4 460 472 28247407
  9. Panksepp J Burgdorf J 50-kHz chirping (laughter?) in response to conditioned and unconditioned tickle-induced reward in rats: Effects of social housing and genetic variables Behav Brain Res 2000 115 1 25 38 10996405
  10. Mason GJ Hampton C Würbel H Wilson D Non-invasively assessing disturbance and stress in laboratory rats by scoring chromodacryorrhoea Altern Lab Anim 2004 32 32 153 159 23577451
  11. Brudzynski SM Communication of adult rats by ultrasonic vocalization: biological, sociobiological, and neuroscience approaches ILAR J 2009 50 1 43 50 19106451
  12. Wintink AJ Brudzynski SM The related roles of dopamine and glutamate in the initiation of 50-kHz ultrasonic calls in adult rats Pharmacol Biochem Behav 2001 70 2 317 323 11701203
  13. Burgdorf J Panksepp J Brudzynski SM Kroes R Moskal JR Breeding for 50-kHz positive affective vocalization in rats Behav Genet 2005 35 1 67 72 15674533
  14. Knutson B Burgdorf J Panksepp J Ultrasonic vocalizations as indices of affective states in rats Psychol Bull 2002 128 6 961 977 12405139
  15. Panksepp J Burgdorf J "Laughing" rats and the evolutionary antecedents of human joy? Physiol Behav 2003 79 3 533 547 12954448
  16. Burgdorf J Panksepp J The neurobiology of positive emotions Neurosci Biobehav Rev 2006 30 2 173 187 16099508
  17. National Research Council Guide for the care and use of laboratory animals 1996 Washington, D.C National Academies Press
  18. National Research Council Guide for the care and use of laboratory animals 2011 Washington, D.C National Academies Press
  19. Natusch C Schwarting RKW Using bedding in a test environment critically affects 50-kHz ultrasonic vocalizations in laboratory rats Pharmacol Biochem Behav 2010 96 3 251 259 20493210
  20. Panksepp J Yovell Y Preclinical modeling of primal emotional affects (SEEKING, PANIC and PLAY): gateways to the development of new treatments for depression Psychopathology 2014 47 6 383 393 25341411
  21. Hori M Hayashi T Nakagawa Y Sakamoto S Urayama O Murakami K Positive emotion-specific changes in the gene expression profile of tickled rats Mol Med Rep 2009 2 2 157 161 21475806
  22. Yamamuro T Neurogenesis in the dentate gyrus of the rat hippocampus enhanced by tickling stimulation with positive emotion Neurosci Res 2010 68 4 285 289 20851720
  23. Wohr M Schwarting RKW Affective communication in rodents: ultrasonic vocalizations as a tool for research on emotion and motivation Cell Tissue Res 2013 354 1 81 97 23576070
  24. Hori M Effects of repeated tickling on conditioned fear and hormonal responses in socially isolated rats Neurosci Lett 2013 536 1 85 89 23313827
  25. Hori M Tickling during adolescence alters fear-related and cognitive behaviors in rats after prolonged isolation Physiol Behav 2014 131 62 67 24727339
  26. Pellis S Pellis V The playful brain: venturing to the limits of neuroscience 2009 Oxford Oneworld Publications
  27. Spinka M Newberry RC Bekoff M Mammalian play: training for the Unexpected Q Rev Biol 2001 76 2 141 168 11409050
  28. Burgdorf J Kroes RA Beinfeld MC Panksepp J Moskal JR Uncovering the molecular basis of positive affect using rough-and-tumble play in rats: a role for insulin-like growth factor I Neuroscience 2010 168 3 769 777 20350589
  29. Burgdorf J The effects of selective breeding for differential rates of 50-kHz ultrasonic vocalizations on emotional behavior in rats Dev Psychobiol 2009 51 1 34 46 18819097
  30. Mällo T Tickling-induced 50-kHz ultrasonic vocalization is individually stable and predicts behaviour in tests of anxiety and depression in rats Behav Brain Res 2007 184 1 57 71 17675169
  31. Pellis SM Field EF Smith LK Pellis VC Multiple differences in the play fighting of male and female rats. Implications for the causes and functions of play Neurosci Biobehav Rev 1997 21 1 105 120 8994213
  32. Burgdorf J Wood PL Kroes RA Moskal JR Panksepp J Neurobiology of 50-kHz ultrasonic vocalizations in rats: electrode mapping, lesion, and pharmacology studies Behav Brain Res 2007 182 2 274 283 17449117

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Authors
Cloutier, S., LaFollette, M. R., Gaskill, B. N., Panksepp, J., & Newberry, R. C.
Affiliations
  • Canadian Council on Animal Care (CA)
  • Purdue University West Lafayette (US)
  • Washington State University (US)
  • Norwegian University of Life Sciences (NO)
Venue
Journal of Visualized Experiments
Published
2018-05-08
Issue
135
ISSN
1940-087X (ISSN-L)
OpenAlex
W2802197686
Cited by
52
References
4
Citations by year
2026: 5 · 2025: 10 · 2024: 3 · 2023: 5 · 2022: 7 · 2021: 12 · 2020: 3 · 2019: 5 · 2018: 2
FWCI
8.07
Type
journal article
Language
en
Open access
Licence
cc-by-nc-nd
Locations
  • Journal of Visualized Experiments (publishedVersion)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • BIBSYS Brage (BIBSYS (Norway)) (acceptedVersion, cc-by-nc-nd)
  • NORA - Norwegian Open Research Archives (submittedVersion, cc-by-nc-nd)
Funders
  • Purdue University
  • Washington State University
  • American Association for Laboratory Animal Science
  • Animal Welfare Institute
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
tickling, laboratory rats, positive affect, animal handling, rough-and-tumble play, habituation, animal welfare, fear of humans, social enrichment, positive affective states, injection procedures
MeSH terms
Animals, Animal Welfare, Behavior, Animal, Male, Play and Playthings, Rats

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