Intrinsic excitability in layer IV-VI anterior insula to basolateral amygdala projection neurons correlates with the confidence of taste valence encoding.

Kolatt Chandran, Sailendrakumar; Yiannakas, Adonis; Kayyal, Haneen; Salalha, Randa; Cruciani, Federica; Mizrahi, Liron; Khamaisy, Mohammad; Stern, Shani; Rosenblum, Kobi (2023). Intrinsic excitability in layer IV-VI anterior insula to basolateral amygdala projection neurons correlates with the confidence of taste valence encoding. eNeuro, 10(1) Society for Neuroscience 10.1523/ENEURO.0302-22.2022

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Avoiding potentially harmful, and consuming safe food is crucial for the survival of living organisms. However, the perceived valence of sensory information can change following conflicting experiences. Pleasurability and aversiveness are two crucial parameters defining the perceived valence of a taste and can be impacted by novelty. Importantly, the ability of a given taste to serve as the conditioned stimulus (CS) in conditioned taste aversion (CTA), is dependent on its valence. Activity in anterior insula (aIC) layer IV-VI pyramidal neurons projecting to the basolateral amygdala (BLA) is correlated with, and necessary for CTA learning and retrieval, as well as the expression of neophobia towards novel tastants, but not learning taste familiarity. Yet, the cellular mechanisms underlying the updating of taste valence representation in this specific pathway are poorly understood. Here, using retrograde viral tracing and whole -cell patch-clamp electrophysiology in trained mice, we demonstrate that the intrinsic properties of deep-lying layer IV-VI, but not superficial layer I-III aIC-BLA neurons, are differentially modulated by both novelty and valence, reflecting the subjective predictability of taste valence arising from prior experience. These correlative changes in the profile of intrinsic properties of LIV-VI aIC-BLA neurons were detectable following both simple taste experiences, as well as following memory retrieval, extinction learning and reinstatement.Significance statementLearning to form aversive or safe taste memories is dependent on genetic predisposition as well as previous experiences. In mice, anterior insula neurons projecting to the basolateral amygdala (aIC-BLA) are indispensable for learning and retrieving learned taste aversion. Kolatt Chandran et al. demonstrate that the intrinsic properties of aIC-BLA neurons, represent the certainty of taste valence prediction, but not percept. Predictive valence-specific changes are reflected through excitability, being low when taste outcome is highly predictive (i.e., following aversive taste memory retrieval or unreinforced familiarization), and high when taste valence is uncertain (i.e., following novelty or aversive taste memory extinction). In addition, the results propose a neuronal mechanism underlying the long delay between taste and visceral discomfort in conditioned taste aversion.

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