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

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.

Transforming experiences: Neurobiology of memory updating/editing

“…Dopamine is a modulatory neurotransmitter associated with the regulation of perceptual salience. This memory process modulates the integration of inconspicuous stimuli into a relevant memory facilitating the transition from novelty to familiarity without enhancing the initial sensory perception in recognition memory ( Gil-Lievana et al, 2022 ; Osorio-Gómez et al, 2022 ). In this regard, the integral functionality of the dopaminergic inputs from the ventral tegmental area and the locus coeruleus is required for novelty detection, comparing the presented information to previously integrated memories ( Lisman and Grace, 2005 ; Lisman et al, 2011 ).…”

Dopamine activity on the perceptual salience for recognition memory

“…Evidence indicates that the insular cortex is a crucial node of the salience network (Uddin, 2015 ), integrating exteroceptive and interoceptive information (Seeley et al, 2007 ). The insular cortex might be involved in salience because of the multiple inputs arising from the amygdala, VTA, the dorsomedial nucleus of the thalamus, and the prefrontal cortex (Bermudez-Rattoni, 2014 ; Uddin, 2015 ; Gil-Lievana et al, 2020 , 2022 ; Chen et al, 2022 ).…”

“…There are illustrative examples of perceptual salience modulation via dopaminergic regulation. Optogenetic stimulation of the dopaminergic neurons within the VTA enhances behavioral response (taste neophobia) to the low-intensity stimulus facilitating taste recognition memory consolidation (Gil-Lievana et al, 2022 ). This effect was probably to bottom-up salience enhancement since augmented behavioral responses were observed during stimulation (acquisition).…”

“…However, optogenetic stimulation of dopaminergic terminals from the VTA to the insular cortex does not modify the behavioral response (lack of neophobia) to the subthreshold stimuli while facilitating taste recognition memory performance during retrieval. It is essential to mention that optogenetic activation of VTA neurons or terminals does not alter the valence of the stimulus (Gil-Lievana et al, 2022 ), suggesting an increased effect over memory consolidation despite the low salient stimulus. Consequently, dopaminergic stimulation within the insular cortex enhances the perceptual salience for low-intensity stimulus.…”

“…These results suggest that the memory trace formation expressed in short-term memory is not dopamine-dependent, but its activity enables long-term and persistent storage (Balderas et al, 2013a ; Moreno-Castilla et al, 2017 ; Vargas et al, 2020 ). In contrast, the blockade of D1-like receptor activity within the insular cortex impedes perceptual salience enhancement (Gil-Lievana et al, 2022 ). Hence, dopaminergic stimulation promotes the consolidation and persistence of stimuli that under normal conditions are not possible considering their subthreshold properties.…”