Adolescent tickling incorporating handling is associated with reduced stress- and fear-related behaviors in socially isolated male rats

Abstract

Social interactions are essential for neuronal development and emotional behavior. In particular, play behavior during adolescence facilitates neural and social development, whereas social isolation is detrimental and increases stress vulnerability in rodents. Furthermore, stress exposure during the juvenile and adolescent periods increases the risk of post-traumatic stress disorder in adulthood. Adolescent male rats emit 50-kHz ultrasonic vocalizations that reflect positive affect induced by rough-and-tumble play or tickling. We previously demonstrated that tickling, which mimics play behavior, induces positive affect and modulates fear-related behaviors as well as sympathoadrenal stress responses. Building on these findings, the present study investigated whether positive emotional experiences induced by this tickling procedure during adolescence can mitigate with long-term alterations in stress vulnerability following early-life stress exposure at weaning. Male Fischer rats were reared under three conditions from postnatal day 21: group-housed (three per cage), isolated (one per cage), or tickled (isolated and receiving 5 min of daily tickling stimulation). In adulthood, animals were subjected to a battery of behavioral tests, including the open-field, elevated plus-maze, forced swim, and fear conditioning tests. In rats that were socially isolated after weaning, repeated tickling incorporating handling during adolescence was associated with fewer behavioral alterations induced by juvenile foot-shock exposure and social isolation, particularly in the forced swim and fear conditioning tests. These findings suggest an association between positive experiences during adolescence and more favorable emotional outcomes following early-life stress.