LTD at amygdalocortical synapses as a novel mechanism for hedonic learning.

Melissa S Haley,Alfredo Fontanini,Stephen Bruno,Arianna Maffei

doi:10.7554/elife.55175

Melissa S Haley, Alfredo Fontanini + Show 2 more

Open Access

https://doi.org/10.7554/elife.55175

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Journal: eLife	Publication Date: Nov 10, 2020
Citations: 22	License type: CC BY 4.0

Affiliation: Stony Brook University

Abstract

A novel, pleasant taste stimulus becomes aversive if associated with gastric malaise, a form of learning known as conditioned taste aversion (CTA). CTA is common to vertebrates and invertebrates and is an important survival response: eating the wrong food may be deadly. CTA depends on the gustatory portion of the insular cortex (GC) and the basolateral nucleus of the amygdala (BLA) however, its synaptic underpinnings are unknown. Here we report that CTA was associated with decreased expression of immediate early genes in rat GC of both sexes, and with reduced amplitude of BLA-GC synaptic responses, pointing to long-term depression (LTD) as a mechanism for learning. Indeed, association of a novel tastant with induction of LTD at the BLA-GC input in vivo was sufficient to change the hedonic value of a taste stimulus. Our results demonstrate a direct role for amygdalocortical LTD in taste aversion learning.

Highlights

Sensory stimuli are perceived and processed according to their physicochemical and affective signatures
In order to investigate whether learning induces synaptic plasticity at amygdalocortical synapses in GC, we trained male and female rats in a conditioned taste aversion paradigm where novel, palatable sucrose (0.1M in water) was paired with gastric malaise induced by an intraperitoneal
355 the lack of changes in intrinsic excitability indicate that the profound effects taste aversion learning has on GC pyramidal neurons is via modulations at specific synaptic inputs and 357 not an alteration in intrinsic membrane properties. This set of findings confirms the central role of the basolateral nucleus of the amygdala (BLA)-GC connection in conditioned taste aversion (CTA) learning, and demonstrates a role for plasticity of BLA-evoked synaptic responses onto L2/3 pyramidal neurons in hedonic learning. 361 Postsynaptically expressed long term depression (LTD) at amygdalocortical synapses as a mechanism for CTA When we compared the effect of CTA on two different forms of LTD, induced by patterns of stimulation designed to mimic BLA neurons’ activity in different behavioral states (Fontanini et al., 2009; Parsana et al, 2012), we found a selective occlusion of plasticity induced by a phasic pattern of activity

Summary

Introduction

Sensory stimuli are perceived and processed according to their physicochemical and affective signatures. CTA can be induced in rats by association of sucrose consumption with a gastric malaise-inducing intraperitoneal (ip) injection of lithium chloride In naïve rats, this association reliably produces a persistent hedonic shift capable of driving avoidance even after a single conditioning trial. Inactivation studies point to the involvement of the gustatory portion of the insular cortex (Braun et al, 1972; Flynn et al, 1991; Yamamoto et al, 1995; Cubero et al, 1999) and the basolateral amygdala (Morris et al, 1999) as key regions necessary for CTA Evidence from these studies is further corroborated by experiments investigating the interaction between these two regions. Recent studies suggest that the expression of aversive behaviors related to taste depend on the output of GC to the amygdala (Lavi et al, 2018; Schiff et al, 2018; Kayyal et al, 2019)

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