Learning-Related Plasticity of Temporal Coding in Simultaneously Recorded Amygdala–Cortical Ensembles

Abstract

Emotional learning requires the coordinated action of neural populations in limbic and cortical networks. Here, we performed simultaneous extracellular recordings from gustatory cortical (GC) and basolateral amygdalar (BLA) neural ensembles as awake, behaving rats learned to dislike the taste of saccharin [via conditioned taste aversion (CTA)]. Learning-related changes in single-neuron sensory responses were observed in both regions, but the nature of the changes was region specific. In GC, most changes were restricted to relatively late aspects of the response (starting ϳ1.0 s after stimulus administration), supporting our hypothesis that in this paradigm palatability-related information resides exclusively in later cortical responses. In contrast, and consistent with data suggesting the amygdala's primary role in judging stimulus palatability, CTA altered all components of BLA taste responses, including the earliest. Finally, learning caused dramatic increases in the functional connectivity (measured in terms of cross-correlation peak heights) between pairs of simultaneously recorded BLA and GC neurons, increases that were evident only during taste processing. Our simultaneous assays of the activity of single neurons in multiple relevant brain regions across learning suggest that the transmission of taste information through amygdala-cortical circuits plays a vital role in CTA memory formation.

The Way an Odor Is Experienced during Aversive Conditioning Determines the Extent of the Network Recruited during Retrieval: A Multisite Electrophysiological Study in Rats

“…Studying beta oscillatory activities, we described two differential subnetworks involved in COA according to primary odor experience. The present study strongly suggests that structures in the network communicate during olfactory processing as suggested by other studies (Ferreira et al, 2005;Grossman et al, 2008). In the future, we would address the hypothesis of temporal interactions in the beta range within these networks and evaluate how critical they could be used for aversive olfactory learning.…”

Simultaneous but not independent anisomycin infusions in insular cortex and amygdala hinder stabilization of taste memory when updated

“…The observed facilitation of CTA induced by amygdala electrical or chemical stimulation was reversed by cortical infusions of NMDA receptor antagonist (Escobar et al 2002;Miranda et al 2002;Ferreira et al 2005). Furthermore, it has been demonstrated that simultaneous electrical recordings of the amygdala and IC during CTA encoding show significant enhancement of functional connectivity between these two structures (Grossman et al 2008). Accordingly, the present results suggest that both the amygdala and IC are important to consolidate and maintain the aversive taste memory trace for a long term when updated.…”

Diffusion tensor imaging segments the human amygdala in vivo

“…Figures 1 and 4 show the blue component labeling the dorso-ventral orientation. Experimental findings describe a well established connection between the lateral amygdala and somatosensory cortical areas (Shi and Cassell 1998;Pikkarainen and Pitkänen 2001;Grossman et al 2008). …”