Crying With Laughter: Adapting the Tickling Protocol to Address Individual Differences Among Rats in Their Response to Playful Handling.

Abstract

It has been over 20 years since the first scientific papers on rat tickling were published (1, 2). Rats were found to emit ultrasonic vocalizations in the 50-kHz range (hereafter referred to as USVs) when a human performed rapid manual stimulation on their dorsoventral region. Such tickling of rats by a human hand is trying to imitate the rough-and-tumble play seen in young rats of both sexes (3, 4). Emission of USVs by the rat indicates that it enjoys being tickled (5–7), as USVs have been linked with positive emotions (8, 9), are emitted in anticipation of, and during, social play (10, 11), and have been suggested to be homologous to human laughter (12). To date, more than 70 scientific articles on rat tickling have been published1, and the consensus is that tickling induces positive emotions in rats. Indeed, in a systematic review, LaFollette et al. (13) found that tickling increased USVs and human hand approach behavior, and decreased measures of anxiety in rats. In this Opinion paper, we consider whether current methods of tickling overemphasize the use of pinning (Figure 1) to which there may be a wider response variation than commonly acknowledged. We do not dispute that tickling can be a positive way to handle juvenile rats, but tickling may not always be perceived as a positive interaction by the rat, and we raise the possibility that tickling methods need to be revised. In particular, we suggest incorporating more aspects of play during tickling (increased diversity) and adapting the method to individual rats' responses (increased flexibility) to achieve positive emotions and increased welfare across a wider cohort of rats. Open in a separate window Figure 1 (A) Pinning is a component of social play in rats, where one rat has its dorsal surface pinned to the ground, while the other rat is in a dominant posture above. (B,C) Pinning has become the main component of the methodology used when tickling rats, as it elicits 50-kHz ultrasonic vocalizations (USVs). Pinning has been used in the past as a means to quantify rough-and-tumble play between rats (14). However, rough-and-tumble play is much more than just pinning, and USVs during pinning are frequent when being tickled by a human (1), but less so when being pinned during play (10, 15). Drawings are by Tayla J. Hammond.