Sensory and palatability coding of taste stimuli in cortex involves dynamic and asymmetric cortico-amygdalar interactions

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 μ-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.