Stimulus-Specific and Generalized Taste Aversion Behaviors and Their Relationship to Cortical Dynamics

Aversive taste behaviors, such as gaping, are commonly viewed as fixed, hard-wired responses important for ejecting potentially toxic tastes from the mouth. Yet, taste responses are highly susceptible to modulation by experience and context; for instance, conditioned taste aversion (CTA), a form of learning in which rats are made to respond aversively to a sweet taste after it has been paired with gastric malaise, can cause gaping to previously acceptable tastes. Here, we compare aversive responses to saccharin sodium (sacc CS) caused by repeated aversive experience (in the form of CTA training) to those caused by naturally aversive quinine HCl, and how these responses are aligned with gustatory cortical (GC) activity. Using simultaneous single-neuron ensemble recordings in GC and electromyography (EMG) recordings in the jaw-opener muscle in awake, freely-moving rats and a machine-learning based behavioral classifier, we not only identified two classes of gaping, but characterized how these classes reflect different mechanisms driving aversive behavioral outputs. The first gape class is taste-specific and emerges following GC ensemble dynamics associated with taste identity and palatability coding, leading to canonical gaping responses to naturally or learned-aversive stimuli. The second is rapid-onset (<200 ms following taste delivery), internal state-dependent gaping the animal exhibits to all tastes in a state of heightened vigilance. This generalized aversion is subsequently suppressed once palatability-related responses emerge in GC, such that only gapes to truly aversive tastes remain. Together, these findings demonstrate that gaping is not a unitary reflex but is instead driven by multiple aversion judgment systems active in different contexts.