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Tickling, a Technique for Inducing Positive Affect When Handling Rats Journal of Visualized Experiments www.jove.com Video Article Tickling, a Technique for Inducing Positive Affect When Handling Rats Sylvie Cloutier1,2, Megan R. LaFollette3, Brianna N. Gaskill3, Jaak Panksepp1, Ruth C. Newberry4 1 Center for the Study of Animal Well-being, Department of Integrative Physiology and Neuroscience, Washington State University 2 Canadian Council on Animal Care 3 Department of Animal Sciences, Center for Animal Welfare Science, College of Agriculture, Purdue University 4 Department of Animal and Aquacultural Sciences, Faculty of Biosciences, Norwegian University of Life Sciences Correspondence to: Sylvie Cloutier at [email protected] URL: https://www.jove.com/video/57190 DOI: doi:10.3791/57190 Keywords: Behavior, Issue 135, Domesticated rats, husbandry, handling, injection, medical procedure, behavior, social play, ultrasonic vocalization, affective state, habituation, positive emotions, laboratory animal welfare Date Published: 5/8/2018 Citation: Cloutier, S., LaFollette, M.R., Gaskill, B.N., Panksepp, J., Newberry, R.C. Tickling, a Technique for Inducing Positive Affect When Handling Rats. J. Vis. Exp. (135), e57190, doi:10.3791/57190 (2018). 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. Video Link The video component of this article can be found at https://www.jove.com/video/57190/ Introduction Handling of small animals, such as domestic rats (Rattus norvegicus) kept in laboratories and as pets, can cause significant increases in behavioral and physiological indicators of stress1, as well as aversive responses suggestive of emotional distress2. Handling rats can trigger fear- based responses towards humans3,4, which may make further handling more difficult, increase the risk of injury to both animal and handler, and limit the validity of experimental data5. To avoid negative effects of handling on experimental results and human-animal relationships, it is common practice to allow some time for newly acquired young animals to habituate to human interaction prior to assigning them to experimental treatments. During this acclimation period, caretakers may expose rats to a series of events that can be highly variable in both form and duration. These may include passive exposure to people, touching, lifting, petting, holding, talking, and offering food treats. Although combinations of such procedures have been reported to reduce fear of humans6, it is unclear which specific practices are most effective for use by busy animal caretakers. There are reports that rats can have either adverse responses, or at least no favorable response, to some of these individual techniques2,7,8,9. In contrast, abundant evidence supports the conclusion that tickling, a handling technique that mimics aspects of the playful rough-and-tumble behavior of rats, is a robustly beneficial form of social contact, especially for juvenile rats10,11,12,13. Rats are highly social mammals, which is clear from observing the time they spend playing together as juveniles14 and their strong motivation to re-establish and maintain social contact with conspecifics15,16,17. Rat tickling draws upon the playful social nature of rats to convert handling into a positive experience. This concept was originally developed as a model for investigating the neurobiological basis of positive affective states evoked by social play behavior7. Since then, rat tickling has been used in over 56 different experiments, 22 of which compared tickling to other handling techniques13. 18,19 The rat's rough-and-tumble play is characterized by two key behaviors: "dorsal contact" and "pin" (Figure 1) . During rough-and-tumble play, a rat initiates play by making dorsal contact with the partner's nape. The recipient responds by rolling supine and is pinned down by the initiator standing above19. The play continues with the rats taking turns being in each position, on top and below18. Human handlers are able to mimic the two key components of rough-and-tumble play by alternating between contact with a rat's nape (dorsal contact) and ventral surface (pin) using vigorous, quick movements of the fingers similar to those used when tickling a child. Of course, tickling is not an exact copy of rat rough- and-tumble play because rats cannot pin the human hand during tickling. Indeed, the level of engagement of individuals in rough-and-tumble play and tickling can differ20,21. Despite this, it appears that tickling invokes the same reward mechanisms as rough-and-tumble play among Copyright © 2018 Creative Commons Attribution-NonCommercial-NoDerivs 3.0 Unported May 2018 | 135 | e57190 | Page 1 of 10 License Journal of Visualized Experiments www.jove.com conspecifics. Tickling is actively solicited by the animals and can serve as a reward for operant learning, contributing evidence that being tickled is substantially rewarding for young rats7,11,12,13,22. Even though rats have also been reported to learn an operant task in exchange for gentle stroking as the reward, they were faster to approach the hand of a person offering tickling compared to stroking7. The pins used in tickling may seem similar to common restraint procedures but there is evidence that rats perceive these types of handling differently. When rats are repeatedly restrained, such as for an injection procedure, they secrete excessive porphyrins resulting in chromodacryorrhea ("red tears")8. Chromodacryorrhea occurs in response to acute stressors and causes the skin and fur around the eyes and nose to become stained a reddish color23. When repeatedly held down and restrained on the back as in a pin, rats showed less attraction to humans than when tickled12. These outcomes imply that the repeated brief restraints and releases during tickling are perceived differently than non-playful restraint. Thus, the precise technique used in tickling has important implications for generating a positive affective state as opposed to contributing to handling stress. Monitoring the effect of tickling on rat affective state can be easily accomplished by attending to the rats' vocalizations. Rats typically produce two categories of ultrasonic vocalizations (USVs), at around 22-kHz and 50-kHz, in addition to audible vocalizations. The 22-kHz USVs typically occur when anticipating aversive events and are accompanied by elevated brain cholinergic activity24. Therefore, 22-kHz USVs are deemed to indicate a negative affective state of anxiety. The 50-kHz USVs, especially of the frequency-modulated "trill" type (Figure 2), are generally associated with rewarding situations and stimuli and are accompanied by increased brain dopaminergic activity24,25. Accordingly, expression of abundant 50-kHz USVs is considered to reflect a positive affective state24,26,27,28. Finally, audible vocalizations are usually associated with, and therefore used as markers of, physical pain and discomfort. The differential production of these three forms of vocalizations thus offers a reliable record of changes in the affective state of rats26. Rats produce USVs at around 22-kHz during exposure to predators, exposure to painful stimuli such as foot shock, and inter-male fighting28. Stroking has also been reported to elicit multiple 22-kHz USVs in naïve rats, inferred as indicating negative affect2. In contrast, when tickled by humans, as when engaged in rough-and-tumble play with other rats, rats produce numerous 50-kHz USVs. It follows that the rate of 50-kHz USVs provides a graded measure of the positive affective response generated by tickling29,30. Existing descriptions of "how to tickle a rat" are rather brief and can lead to variable results. Further, novice "rat ticklers" may be overly tentative in their attempts to mimic rough-and-tumble play. The words "tickle vigorously" are easier to understand when demonstrated visually. Therefore, the goal of this article is to provide a detailed description and demonstration of how to mimic rats' positive playful interactions in an effective and consistent manner that reliably elicits positive responses from most rats when handled. This protocol describes a standardized tickling technique, and explains how tickling can be combined with procedures such as restraint and injection to mitigate potentially unpleasant affective experiences.
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