Thalamic Contribution to Cortical Processing of Taste and Expectation

Abstract

Taste-related information reaches the gustatory cortex (GC) through two routes: a thalamic and a limbic pathway. While evidence is accumulating on limbic-cortical interactions in taste, very little information is available on the function of the gustatory thalamus in shaping GC activity. Here we rely on behavioral electrophysiological techniques to study taste-evoked activity in GC before and after inactivation of the parvicellular portion of the ventroposteromedial nucleus of thalamus (VPMpc; i.e., the gustatory thalamus). Gustatory stimuli were presented to rats either alone or preceded by an anticipatory cue. The reliance on two different behavioral contexts allowed us to investigate how the VPMpc mediates GC responses to uncued tastants, cued tastants, and anticipatory cues. Inactivation of the thalamus resulted in a dramatic reduction of taste processing in GC. However, responses to anticipatory cues were unaffected by this manipulation. The use of a cue-taste association paradigm also allowed for the identification of two subpopulations of taste-specific neurons: those that responded to gustatory stimulation and to the cue (i.e., cue-and-taste) and those that responded to tastants only (i.e., taste-only). Analyses of these two populations revealed differences in response dynamics and connectivity with the VPMpc. The results provide novel evidence for the role of VPMpc in shaping GC activity and demonstrate a previously unknown association between responsiveness to behavioral events, temporal dynamics, and thalamic connectivity in GC.