Neural and Behavioral Correlates of Rapid Familiarization to Novel Taste

Abstract

Gustatory cortex (GC) plays a pivotal role in taste perception, expressing neural ensemble dynamics that reflect, in sequence, taste quality and hedonics, and that influence taste-guided behavior. The circuitry underlying these responses has traditionally been described as fixed and hardwired in adult rodents, although GC taste responses are known to change across multiple timescales of experience, including between sessions of novel taste exposure. Here, we show that responses change on an even smaller timescale—that in fact rapid, experience-dependent changes in GC responses occur across the first handful of taste exposure trials. Specifically, we show that the first 6–9 responses to novel taste stimuli in experimentally naive female lab rats are distinct from later trials in the same session: these earliest responses show less “stereotypical” dynamics and encode both taste identity and palatability less reliably than later responses; “normal” rat taste responses are not preexisting but rather develop across the first several minutes of taste exposure. This phenomenon, which is not taste-specific, is nonexistent (or nearly so) in later sessions. Furthermore, this rapid neural response plasticity is paralleled in changing licking behavior in response to the same stimuli. Together, these results provide novel insights into the real-time dynamics of sensory processing across novel-taste familiarization, essentially demonstrating that the taste system, rather than being hardwired, becomes “tuned up” by use.