Photostimulation of Ventral Tegmental Area-Insular Cortex Dopaminergic Inputs Enhances the Salience to Consolidate Aversive Taste Recognition Memory via D1-Like Receptors

Elvi Gil-Lievana,Ranier Gutierrez,Gerardo Ramírez-Mejía,Jorge Luis-Islas,Federico Bermúdez-Rattoni,Oscar Urrego-Morales

doi:10.3389/fncel.2022.823220

Abstract

Taste memory involves storing information through plasticity changes in the neural network of taste, including the insular cortex (IC) and ventral tegmental area (VTA), a critical provider of dopamine. Although a VTA-IC dopaminergic pathway has been demonstrated, its role to consolidate taste recognition memory remains poorly understood. We found that photostimulation of dopaminergic neurons in the VTA or VTA-IC dopaminergic terminals of TH-Cre mice improves the salience to consolidate a subthreshold novel taste stimulus regardless of its hedonic value, without altering their taste palatability. Importantly, the inhibition of the D1-like receptor into the IC impairs the salience to facilitate consolidation of an aversive taste recognition memory. Finally, our results showed that VTA photostimulation improves the salience to consolidate a conditioned taste aversion memory through the D1-like receptor into the IC. It is concluded that the dopamine activity from the VTA into IC is required to increase the salience enabling the consolidation of a taste recognition memory. Notably, the D1-like receptor activity into the IC is required to consolidate both innate and learned aversive taste memories but not appetitive taste memory.

Highlights

Taste memory evolves as a critical system for animal survival through the detection of taste attributes related to the hedonic value, degree of familiarity, and to remember their nutritive or toxic consequences of food to form a memory for future acceptance or avoidance responses (Bermúdez-Rattoni, 2004; Scott, 2005)
During the memory test, Enhanced yellow fluorescent protein (eYFP) mice did not consolidate a taste recognition memory (TRM) to low concentrated saccharin or quinine solutions. These results suggest that ventral tegmental area (VTA) dopaminergic neurons increase the salience of low concentration appetitive and aversive taste stimuli to consolidate into TRM
Since the results showed that the VTA-insular cortex (IC) dopaminergic pathways potentiated the salience of an innate aversive taste stimulus to consolidate a TRM through the D1-like receptors; we extended our research to study whether the same pathway is required to process the salience of associative aversive taste memories, such as a conditioned taste aversion memory

Summary

Introduction

Taste memory evolves as a critical system for animal survival through the detection of taste attributes related to the hedonic value, degree of familiarity, and to remember their nutritive or toxic consequences of food to form a memory for future acceptance or avoidance responses (Bermúdez-Rattoni, 2004; Scott, 2005). Several studies have demonstrated that taste learning requires dopaminergic neurotransmission to consolidate the memory representation of tastants (Guzmán-Ramos and BermúdezRattoni, 2011; Yiannakas and Rosenblum, 2017) In this regard, the VTA is a vital dopamine supplier that serves a central role in motivating behavior and reward processing. Evidence shows VTA dopaminergic neurons increase their activity after the presentation of an aversive stimuli (Brischoux et al, 2009; Bromberg-Martin et al, 2010; Núñez-Jaramillo et al, 2010). In this sense, it has been reported that the modulation of the dopaminergic neurons by rewarding or aversive stimuli depends on the brain area(s) to which these dopaminergic neurons project (Lammel et al, 2011; de Jong et al, 2019)

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