SUMMARY Animals are not passive spectators of the sensory world in which they live. In natural conditions they often sense objects on the bases of expectations initiated by predictive cues. Expectation profoundly modulates neural activity by altering the background state of cortical networks and modulating sensory processing. The link between these two effects is not known. Here, we studied how cue-triggered expectation of stimulus availability influences processing of sensory stimuli in the gustatory cortex (GC). We found that expected tastants were coded more rapidly than unexpected stimuli. The faster onset of sensory coding related to anticipatory priming of GC by associative auditory cues. Simultaneous recordings and pharmacological manipulations of GC and basolateral amygdala revealed the role of top-down inputs in mediating the effects of anticipatory cues. Altogether these data provide a new model for how cue-triggered expectation changes the state of sensory cortices to achieve rapid processing of natural stimuli.

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Many species employ chemical signals to convey messages between members of the same species (conspecific), but chemosignals may also provide information to another species (heterospecific). Here, we found that conspecific chemosignals (male, female mouse urine) increased immediate early gene-protein (IEG) expression in both anterior and posterior medial amygdala of male mice, whereas most heterospecific chemosignals (e.g.: hamster vaginal fluid, steer urine) increased expression only in anterior medial amygdala. This categorization of responses in medial amygdala conforms to our previously reported findings in male hamsters. The same characteristic pattern of IEG expression appears in the medial amygdala of each species in response to conspecific stimuli for that species. These results suggest that the amygdala categorizes stimuli according to the biological relevance for the tested species. Thus, a heterospecific predator (cat collar) stimulus, which elicited behavioral avoidance in mice, increased IEG expression in mouse posterior medial amygdala (like conspecific stimuli). Further analysis suggests reproduction related and potentially threatening stimuli produce increased IEG expression in different sub-regions of posterior medial amygdala (dorsal and ventral, respectively). These patterns of IEG expression in medial amygdala may provide glimpses of a tertiary sorting of chemosensory signals beyond the primary-level selectivity of chemosensory neurons and the secondary sorting in main and accessory olfactory bulbs.

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.