Neural and Behavioral Correlates of Rapid Familiarization to Novel Taste

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 hard-wired in adult rodents, although GC taste responses are known to change across multiple time-scales of experience, including between sessions of novel taste exposure. Here, we show that responses change on an even smaller time-scale—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-naïve 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; the oft-described rat taste responses are not pre-existing, 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 hard-wired, becomes “tuned up” by use. Significance Statement It is ubiquitously assumed that adult sensory systems process incoming stimuli normally starting with the first delivery—a property of hard-wired circuits. Here we leverage our understanding of single-trial taste-response dynamics to demonstrate that this is not the case, showing that gustatory cortical (GC) sensory responses “tune up” over the initial 9-10 trials of novel taste delivery; these initial responses carry less stimulus and palatability-related content, and fail to show the “mature” dynamics described in many previous papers. Further testing revealed this process to be functional, in that normal preferences for palatable tastes develop across this same time period, in a process analogous to but faster than attenuation of neophobia. It appears that rats must learn to taste.