Cortical taste processing evolves through benign taste exposures.

Abstract

Experience impacts learning and perception. Familiarity with stimuli that later become the conditioned stimulus (CS) in a learning paradigm, for instance, reduces the strength of that learning-a fact well documented in studies of conditioned taste aversion (CTA; De la Casa & Lubow, 1995;Lubow, 1973;Lubow & Moore, 1959). Recently, we have demonstrated that even experience with "incidental" (i.e., non-CS) stimuli influences CTA learning: Long Evans rats pre-exposed to salty and/or sour tastes later learn unusually strong aversions to novel sucrose (Flores et al., 2016), and exhibit enhanced sucroseresponsiveness after learning in gustatory cortex (GC;Flores et al., 2018). These findings suggest that incidental taste exposure (TE) may change spiking responses that have been shown to underlie the processing of tastes in GC. Here, we test this hypothesis, evaluating whether GC neuron spiking responses change across 3 days of taste exposure. Our results demonstrate that the discriminability of GC ensemble taste responses increases with this familiarization. Analysis of single-neuron responses recorded across multiple sessions reveals that taste exposure not only enriches identity and palatability information in tasteevoked activity but also enhances the discriminability of even novel tastes. These findings demonstrate that "mere" familiarization with incidental episodes of tasting changes the neural spiking responses of taste processing and provides specific insight into how such TE may impact later learning.

The impact of familiarity on cortical taste coding

“…These results indicate that at least in the population of stable taste-responsive GC cells, neural responses evolve from a pattern of dissimilarity to all novel taste stimuli, to one where stimuli evoking similar behavioral responses elicit similar neural patterns. At first glance, these results seem at odds with a recent physiological study in GC in rats, where 3 days of experience with NaCl, citric acid, and water led to an increase in the distinctness of the neural patterns evoked by these stimuli (Flores et al, 2022). However, stimulus delivery was via IO cannulas, so the specific behaviors evoked by the pair of tastants are inferred -it is possible that the citric acid remains aversive over days to rats, unlike the change seen in mice.…”

“…They reported that the average response to the stimulus actually increased as the taste became familiar, although this change was only apparent in the late phase of the response. In contrast, Flores et al (Flores et al, 2022) found no change in overall GC responsiveness with three days of familiarization training with two stimuli and water, but did find changes in how these stimuli were encoded (see below). These studies necessarily focused on the responses of only taste-responsive cells.…”

“…However, stimulus delivery was via IO cannulas, so the specific behaviors evoked by the pair of tastants are inferred – it is possible that the citric acid remains aversive over days to rats, unlike the change seen in mice. Furthermore, in both this and the earlier study, changes over days were found in the late phase response, i.e.,> 1 s after drinking onset (Bahar et al, 2004; Flores et al, 2022); by this time point, GC neurons are encoding a palatability-related response (Katz et al, 2001; Levitan et al, 2019). It is possible, then, that the increased correlations among avidly licked stimuli found here (and the lack of correlation with quinine) represent a palatability-related population response that increases in strength across days.…”

“…For example, animals become familiar with novel tastes over successive encounters. This process of familiarization is important to the animal both in driving future ingestive decisions (Domjan, 1976; Harder et al, 1989; Mura et al, 2018) as well as impacting subsequent learning (Lubow, 2009; Flores et al, 2016; Flores et al, 2018; Flores et al, 2022).…”

“…In contrast, a study of multiunit activity in the GC in rats actively sampling a taste stimulus over several days found that the average response to the stimulus actually increased as the taste became familiar, although this change was only apparent in the late phase of the response (Bahar et al, 2004). More recently, Flores et al (Flores et al, 2022) conducted recordings in awake rats and described both an increase in taste discriminability and enhancement of the late-phase palatability response in GC neurons, as animals were exposed to a pair of tastants and water over 3 days.…”