Intrinsic Excitability in Layer IV–VI Anterior Insula to Basolateral Amygdala Projection Neurons Correlates with the Confidence of Taste Valence Encoding

Abstract

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 toward 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.

Dissection of insular cortex layer 5 reveals two sublayers with opposing modulatory roles in appetitive drinking behavior

“…In addition to by taste qualities, motivation for feeding/drinking can be affected by taste-independent contexts, including homeostatic, emotional, and external circumstances, although all of which can be associated with any type of taste by learning and lead to anticipatory behaviors. 5 , 6 , 7 , 8 , 9 , 10 , 11 , 12 Thus, clarifying the properties of sensory and contextual inputs to each L5 sublayer of the insula and the necessity of the neuronal populations for behavioral decisions driven by those inputs is also a critical issue for future studies. In the present study, the L5 opto-stimulation was limited to water drinking epochs and also to an experimental context and, therefore, it remains to be addressed whether a sustained activation of the L5 sublayer can alter daily water consumption, which might be crucial for understanding the insula’s role in anorexia/hyperorexia.…”

“…The insular cortex (insula) mediates top-down modulation of feeding and drinking behaviors in response to taste quality, 1 , 2 homeostatic/visceral states, 3 , 4 innate threat, 3 and learned stimuli, 5 , 6 , 7 , 8 , 9 , 10 , 11 , 12 as well as the modulation of emotional 13 and social 3 , 14 , 15 behaviors. In particular, the modulation of feeding or drinking is differentially regulated by distinct subregions of the insula along the anterior-posterior (A-P) axis, 1 and region-specific projections to the amygdala complex are suggested to underlie the behavioral control.…”

Neural coding in gustatory cortex reflects consumption decisions: Evidence from conditioned taste aversion

“…CTA learning occurs when neutral or appetitive tastes are temporally associated with illness, with the result that animals will display subsequent aversion to those tastes. A large body of research has characterized potential neural circuits and mechanisms that underlie CTA formation and expression, including evidence for a significant role of GC (Braun et al, 1982; Yamamoto et al, 1995; Grossman et al, 2008; Barki-Harrington et al, 2009; Schier et al, 2014; Lavi et al, 2018; Kayyal et al, 2019; Abe et al, 2020; Yiannakas et al, 2021; Jung et al, 2022; Kolatt Chandran et al, 2023). What is less certain is whether and how CTA affects the neuronal activity of the GC itself, and whether a change in activity following learning directly reflects or predicts aversion of the conditioned taste stimulus (CS).…”