Rat Anterior Insula Symmetrically Represents Tickling-Induced Playful Emotions

Social play, an integral aspect of animal behavior, is inherently associated with positive emotions, yet the neuronal underpinnings of these playful states remain inadequately explored. We examined the anterior insula’s involvement in processing tickle-induced playful emotions in rats. Our findings revealed diverse patterns of insular activity during tickling, with 20% of the recorded units displaying strong activation, and another 20% exhibiting inhibition. These units responded similarly to other playful contexts, such as gentle touch and hand chase, but not to neutral locomotion. Tickle-activated units demonstrated a positive correlation of firing rates with appetitive vocalization rates, whereas tickle-inhibited units showed a negative correlation. Distinct spike waveforms were associated with the tickle response patterns, suggesting potential cell-type dependencies. However, pharmacological manipulation of the global anterior insula did not yield observable effects on play behavior in rats. Anterograde tracing revealed extensive insular projections to areas including the amygdala and nucleus accumbens. Taken together, our findings suggest that the anterior insula symmetrically represents tickle-induced playful emotional states.