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.

Abstract-In-vivo electrophysiology, the recording of neurons in the brains of awake, behaving animals, is currently undergoing paradigm shifts. There is a push towards moving to open-source technologies that can: 1) be adjusted to specific experiments; 2) be shared with ease; and 3) more affordably record from larger numbers of electrodes simultaneously. Here we describe our construction of a system that satisfies these three desirable properties using the scientific Python stack and Linux. Using a Raspberry Pi to control experimental paradigms, we build a completely open-source, HDF5-based analysis (spike sorting) toolkit in Python. This toolkit can be easily parallelized and scales to incorporate increasing electrode counts and longer recordings. Our rig costs about $5000, an order of magnitude less than many comparable commercially available electrophysiology systems.

Conditioned taste aversion (CTA) is a form of one-trial learning dependent on basolateral amygdala projection neurons (BLApn). Its underlying cellular and molecular mechanisms remain poorly understood. RNAseq from BLApn identified changes in multiple candidate learning-related transcripts including the expected immediate early gene Fos and Stk11, a master kinase of the AMP-related kinase pathway with important roles in growth, metabolism and development, but not previously implicated in learning. Deletion of Stk11 in BLApn blocked memory prior to training, but not following it and increased neuronal excitability. Conversely, BLApn had reduced excitability following CTA. BLApn knockout of a second learning-related gene, Fos, also increased excitability and impaired learning. Independently increasing BLApn excitability chemogenetically during CTA also impaired memory. STK11 and C-FOS activation were independent of one another. These data suggest key roles for Stk11 and Fos in CTA long-term memory formation, dependent at least partly through convergent action on BLApn intrinsic excitability.