Odour conditioning of positive affective states: Rats can learn to associate an odour with being tickled

Abstract

Most associative learning tests in rodents use negative stimuli, such as electric shocks. We investigated if young rats can learn to associate the presence of an odour with the experience of being tickled (i.e. using an experimenter’s hand to mimic rough-and-tumble play), shown to elicit 50 kHz ultrasonic vocalisations (USVs), which are indicative of positive affect. Male, pair-housed Wistar rats (N = 24) were all exposed to two neutral odours (A and B) presented in a perforated container on alternate days in a test arena. Following 60s of exposure, the rats were either tickled on days when odour A (n = 8) or odour B (n = 8) was present, or never tickled (n = 8). When tickled, rats produced significantly more 50 kHz USVs compared to the days when not being tickled, and compared to control rats. The level of anticipatory 50 kHz USVs in the 60s prior to tickling did not differ significantly between the tickled and control rats. As a retrieval test following the odour conditioning, rats were exposed successively in the same arena to three odours: an unknown neutral odour, extract of fox faeces, and either odours A or B. Compared to controls, 50 kHz USVs of tickled rats increased when exposed to the odour they had previously experienced when tickled, indicating that these rats had learned to associate the odour with the positive experience of being tickled. In a test with free access for 5 min to both arms of a T-maze, each containing one of the odours, rats tickled with odour A spent more time in the arm with this odour. This work is the first to test in a fully balanced design whether rats can learn to associate an odour with tickling, and indicates that positive odour conditioning has potential to be used as an alternative to negative conditioning tests.

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

“…Our description of playful handling may come across as subjective, but playful handling can be used scientifically, as demonstrated in a number of trials ( 5 , 51 , 52 ). Just like we adjust drug dosage to body weight, or train rats for different durations depending on their learning skills, maximizing enjoyment of playful handling requires adaptation to the individual rat's behavioral responses to interactions with the human hand.…”

“…However, this study used adult rats, with tickling sessions lasting 10 min, and without adjusting the manipulations to the rat's response. In contrast, Bombail et al ( 5 ) used various tactile manipulations resembling the elements of play listed in the section on From play to tickling , and with their type and vigor adjusted to the response of each rat, and found USVs increasing from 83 to 233 per minute, on average, from the first to the fifth playful handling session. In comparison, using the Panksepp method, Burgdorf et al ( 45 ) recorded around 90 USVs/min during the fourth tickling session in their randomly selected line.…”

“…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 ).…”

Sex‐dependent impact of microbiota status on cerebral μ‐opioid receptor density in fischer rats

“…Makrolon cages containing sterile beddings made of wood shavings hosted the GF animals within the isolators. The CON rats were kept under a standard laboratory environment (Bombail et al, 2019). GF rats were given free access to autoclaved tap water and a gamma-irradiated (45 kGy) standard diet (R03; Scientific Animal Food and Engineering, Augy, France).…”

Sensory Abilities of Horses and Their Importance for Equitation Science

“…Moreover, conditioning horses to associate a certain odor with a pleasant experience could take the use of odors a step further. Odorant conditioning has barely been explored in livestock, but rats can learn to associate an odor with positive human tactile stimulation (94). Such positive odor conditioning has the potential to be used as an alternative to food rewards or as a calming addition in otherwise stressful situations.…”