Whereas many laboratory-studied decisions involve a highly trained animal identifying an ambiguous stimulus, many naturalistic decisions do not. Consumption decisions, for instance, involve determining whether to eject or consume an already identified stimulus in the mouth and are decisions that can be made without training. By standard analyses, rodent cortical single-neuron taste responses come to predict such consumption decisions across the 500 ms preceding the consumption or rejection itself; decision-related firing emerges well after stimulus identification. Analyzing single-trial ensemble activity using hidden Markov models, we show these decision-related cortical responses to be part of a reliable sequence of states (each defined by the firing rates within the ensemble) separated by brief state-to-state transitions, the latencies of which vary widely between trials. When we aligned data to the onset of the (late-appearing) state that dominates during the time period in which single-neuron firing is correlated to taste palatability, the apparent ramp in stimulusaligned choice-related firing was shown to be a much more precipitous coherent jump. This jump in choice-related firing resembled a step function more than it did the output of a standard (ramping) decision-making model, and provided a robust prediction of decision latency in single trials. Together, these results demonstrate that activity related to naturalistic consumption decisions emerges nearly instantaneously in cortical ensembles.

Sensation and action are necessarily coupled during stimulus perception – while tasting, for instance, perception happens while an animal decides to expel or swallow the substance in the mouth (the former via a behavior known as ‘gaping’). Taste responses in the rodent gustatory cortex (GC) span this sensorimotor divide, progressing through firing-rate epochs that culminate in the emergence of action-related firing. Population analyses reveal this emergence to be a sudden, coherent and variably-timed ensemble transition that reliably precedes gaping onset by 0.2–0.3s. Here, we tested whether this transition drives gaping, by delivering 0.5s GC perturbations in tasting trials. Perturbations significantly delayed gaping, but only when they preceded the action-related transition - thus, the same perturbation impacted behavior or not, depending on the transition latency in that particular trial. Our results suggest a distributed attractor network model of taste processing, and a dynamical role for cortex in driving motor behavior.

A great deal is known about the broad coding and neural ensemble dynamics characterizing forebrain taste processing in awake rats, and about the relationship between these firing rate dynamics and behavior. With regard to mice, in contrast, data concerning cortical taste coding are few, inconclusive, and largely restricted to imaging, which lacks the temporal sensitivity necessary for evaluation of fast response dynamics. Here we have recorded the spiking activity of ensembles of gustatory cortical (GC) single neurons while presenting representatives of the basic taste modalities (sweet, salty, sour and bitter) to awake mice. Our results reveal deep similarities between rat and mouse taste processing. Many recorded murine GC neurons (~66%) responded distinctly to different tastes, and entropy analysis (which measures the breadth of taste coding) further confirmed that the majority of taste neurons in fact responded to 3 or 4 tastes. Temporal coding analyses revealed that single mouse GC neurons sequentially coded taste identity and palatability-the latter responses emerging ~0.5s after the former-a dynamic that population analysis suggested reflects a reliable sequence of network states activated by taste delivery (i.e., ensembles of simultaneously-recorded neurons transitioned suddenly and coherently from coding taste identity to coding taste palatability). All of the above results held across the anterior-posterior and dorsal-ventral axes of GC-neither between-nor within-mouse mapping revealed regions of narrow or temporally simple taste responses. In conclusion, our data indicates that mouse GC, like rat GC, codes multiple aspects of taste in a coarse, time-varying manner.

Electrophysiological analysis has revealed much about the broad coding and neural ensemble dynamics that characterize gustatory cortical (GC) taste processing in awake rats and about how these dynamics relate to behavior. With regard to mice, however, data concerning cortical taste coding have largely been restricted to imaging, a technique that reveals average levels of neural responsiveness but that (currently) lacks the temporal sensitivity necessary for evaluation of fast response dynamics; furthermore, the few extant studies have thus far failed to provide consensus on basic features of coding. We have recorded the spiking activity of ensembles of GC neurons while presenting representatives of the basic taste modalities (sweet, salty, sour, and bitter) to awake mice. Our first central result is the identification of similarities between rat and mouse taste processing: most mouse GC neurons (~66%) responded distinctly to multiple (3–4) tastes; temporal coding analyses further reveal, for the first time, that single mouse GC neurons sequentially code taste identity and palatability, the latter responses emerging ~0.5 s after the former, with whole GC ensembles transitioning suddenly and coherently from coding taste identity to coding taste palatability. The second finding is that spatial location plays very little role in any aspect of taste responses: neither between- (anterior-posterior) nor within-mouse (dorsal-ventral) mapping revealed anatomic regions with narrow or temporally simple taste responses. These data confirm recent results showing that mouse cortical taste responses are not “gustotopic” but also go beyond these imaging results to show that mice process tastes through time. NEW & NOTEWORTHY Here, we analyzed taste-related spiking activity in awake mouse gustatory cortical (GC) neural ensembles, revealing deep similarities between mouse cortical taste processing and that repeatedly demonstrated in rat: mouse GC ensembles code multiple aspects of taste in a coarse-coded, time-varying manner that is essentially invariant across the spatial extent of GC. These data demonstrate that, contrary to some reports, cortical network processing is distributed, rather than being separated out into spatial subregion.

The strength of learned associations between pairs of stimuli is affected by multiple factors, the most extensively studied of which is prior experience with the stimuli themselves. In contrast, little data is available regarding how experience with "incidental" stimuli (independent of any conditioning situation) impacts later learning. This lack of research is striking given the importance of incidental experience to survival. We have recently begun to fill this void using conditioned taste aversion (CTA), wherein an animal learns to avoid a taste that has been associated with malaise. We previously demonstrated that incidental exposure to salty and sour tastes (taste preexposure-TPE) enhances aversions learned later to sucrose. Here, we investigate the neurobiology underlying this phenomenon. First, we use immediate early gene (c-Fos) expression to identify gustatory cortex (GC) as a site at which TPE specifically increases the neural activation caused by taste-malaise pairing (i.e., TPE did not change c-Fos induced by either stimulus in isolation). Next, we use site-specific infection with the optical silencer Archaerhodopsin-T to show that GC inactivation during TPE inhibits the expected enhancements of both learning and CTA-related c-Fos expression, a full day later. Thus, we conclude that GC is almost certainly a vital part of the circuit that integrates incidental experience into later associative learning.