The Role of Identified Neurotransmitter Systems in the Response of Insular Cortex to Unfamiliar Taste: Activation of ERK1–2 and Formation of a Memory Trace

Abstract

In the behaving rat, the consumption of an unfamiliar taste activates the extracellular signal-regulated kinase 1-2 (ERK1-2) in the insular cortex, which contains the taste cortex. In contrast, consumption of a familiar taste has no effect. Furthermore, activation of ERK1-2, culminating in modulation of gene expression, is obligatory for the encoding of long-term, but not short-term, memory of the new taste (Berman et al., 1998). Which neurotransmitter and neuromodulatory systems are involved in the activation of ERK1-2 by the unfamiliar taste and in the long-term encoding of the new taste information? Here we show, by the use of local microinjections of pharmacological agents to the insular cortex in the behaving rat, that multiple neurotransmitters and neuromodulators are required for encoding of taste memory in cortex. However, these systems vary in the specificity of their role in memory acquisition and in their contribution to the activation of ERK1-2. NMDA receptors, metabotropic glutamate receptors, muscarinic, and beta-adrenergic and dopaminergic receptors, all contribute to the acquisition of the new taste memory but not to its retrieval. Among these, only NMDA and muscarinic receptors specifically mediate taste-dependent activation of ERK1-2, whereas the beta-adrenergic function is independent of ERK1-2, and dopaminergic receptors regulate also the basal level of ERK1-2 activation. The data are discussed in the context of postulated novelty detection circuits in the central taste system.

Internal body state influences topographical plasticity of sensory representations in the rat gustatory cortex

“…However, the consensus is that GC is necessary for an effective acquisition of CTA (12). Approaches aimed to unravel the molecular machinery of taste learning established that GC is fundamental for the formation of short-and long-term aversion memories (35)(36)(37)(38)(39)(40). The changes we observed in the saccharin activated patterns between the control and the CTA rats might therefore be explained by a long-term retention of saccharin aversion.…”

d-Cycloserine enhances conditioned taste aversion learning in rats

“…Central NMDA receptors are required for full CTA learning, as demonstrated using NMDA receptor antagonists. For example, APV (a competitive antagonist) or CPP (a noncompetitive antagonist) administered into the gustatory cortex prior to or immediately after the pairing of saccharin and LiCl attenuates CTA acquisition (Berman et al, 2000;Escobar et al, 2002;Escobar et al, 1998;Ferreira et al, 2002;Gutierrez et al, 1999;Rosenblum et al, 1997).…”

“…In particular, competitive antagonists (e.g. APV or CPP) block CTA learning when injected into the gustatory cortex before or around the time of CTA acquisition (Berman et al, 2000;Escobar et al, 2002;Escobar et al, 1998;Ferreira et al, 2002;Gutierrez et al, 1999;Rosenblum et al, 1997). In addition, the 2B subunit of the NMDA receptor in the gustatory cortex undergoes tyrosine phosphorylation when rats drink a novel taste solution (Rosenblum et al, 1997), suggesting that posttranslational modification of NMDA receptor may also be important during the association of a novel taste and a toxic effect.…”

The Insular Cortex and the Amygdala: Shared Functions and Interactions

“…A large number of studies using transient pharmacological manipulations of the gustatory IC have shown that the IC has a role in CTA to novel tastes [117,161], familiar tastes (also known as latent inhibition) [155,162] and the extinction of CTA [115,117]. Interestingly, IC lesions only partially affect CTA acquisition [145,146,148,149,163] but, when performed after CTA learning, IC lesions completely disrupt CTA memory retention [143,145,146,164,165] leading to the original preference for the taste [148].…”