Perceptual processing of tastes is performed by the amygdala-cortical loop

Abstract

Gustatory cortical (GC) and basolateral amygdalar (BLA) taste responses consist of an inter-regionally coherent 3-part state sequence. This coherence suggests that reciprocal BLA-GC connectivity is important for taste processing, but it remains unknown: 1) whether BLA-GC coherence actually reflects a reciprocal "conversation" (as opposed to one region simply driving the other); and 2) whether such a "conversation" has anything to do with the taste processing observed within GC response dynamics. Here, we address these questions using network and single-neuron analysis of simultaneously-recorded GC and BLA taste responses in awake rats. We find asymmetric, reciprocal {micro}-frequency influences that reflect taste processing dynamics: BLA[->]GC influence dominates between 300 and 1000msec (the epoch in which BLA codes palatability); afterward, when GC responses become palatability-related and GC has been shown to release a behavior-relevant signal, the direction of influence reverses, becoming GC[->]BLA. Follow-up analyses demonstrate that this "turn-taking" exists alongside effectively synchronous amygdala-cortical coupling--the two regions functioning as a unified structure. Finally, to assess the implications of these interactions for single-neuron responses, we tested the response properties of GC neurons categorized by their inferred connectivity with BLA: GC neurons influenced by BLA produce stronger taste-specific and palatability-related responses than other GC neurons, and the strongest taste encoding is specifically found in GC neurons that both influence and receive influence from BLA--those most deeply embedded in the reciprocal circuit. These results, consistent with findings in multiple systems, support the novel conclusion that taste processing and decision-making is a function of the amygdala-cortical loop. New & NoteworthyConventionally, taste circuitry is considered feedforward, travelling up from the brainstem, with each additional node containing more sophisticated information. We challenge this convention by demonstrating that amygdala and cortex instead influence each other bidirectionally, yet in a direction-specific and asymmetric manner. These influences appear to drive different parts of the taste response, with distinct patterns for decision-making and behavioral output; furthermore, involvement in cortex-amygdala functional connectivity determines the strength of encoding in cortical single neurons.