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.

Experience impacts learning and perception. Familiarity with stimuli that later become the conditioned stimulus (CS) in a learning paradigm, for instance, reduces the strength of that learning-a fact well documented in studies of conditioned taste aversion (CTA; De la Casa & Lubow, 1995;Lubow, 1973;Lubow & Moore, 1959). Recently, we have demonstrated that even experience with "incidental" (i.e., non-CS) stimuli influences CTA learning: Long Evans rats pre-exposed to salty and/or sour tastes later learn unusually strong aversions to novel sucrose (Flores et al., 2016), and exhibit enhanced sucroseresponsiveness after learning in gustatory cortex (GC;Flores et al., 2018). These findings suggest that incidental taste exposure (TE) may change spiking responses that have been shown to underlie the processing of tastes in GC. Here, we test this hypothesis, evaluating whether GC neuron spiking responses change across 3 days of taste exposure. Our results demonstrate that the discriminability of GC ensemble taste responses increases with this familiarization. Analysis of single-neuron responses recorded across multiple sessions reveals that taste exposure not only enriches identity and palatability information in tasteevoked activity but also enhances the discriminability of even novel tastes. These findings demonstrate that "mere" familiarization with incidental episodes of tasting changes the neural spiking responses of taste processing and provides specific insight into how such TE may impact later learning.

Decisions as to whether to continue with an ongoing activity or to switch to an alternative are a constant in an animal’s natural world, and in particular underlie foraging behavior and performance in food preference tests. Stimuli experienced by the animal both impact the choice and are themselves impacted by the choice, in a dynamic back and forth. Here, we present model neural circuits, based on spiking neurons, in which the choice to switch away from ongoing behavior instantiates this back and forth, arising as a state transition in neural activity. We analyze two classes of circuit, which differ in whether state transitions result from a loss of hedonic input from the stimulus (an “entice to stay” model) or from aversive stimulus-input (a “repel to leave” model). In both classes of model, we find that the mean time spent sampling a stimulus decreases with increasing value of the alternative stimulus, a fact that we linked to the inclusion of depressing synapses in our model. The competitive interaction is much greater in “entice to stay” model networks, which has qualitative features of the marginal value theorem, and thereby provides a framework for optimal foraging behavior. We offer suggestions as to how our models could be discriminatively tested through the analysis of electrophysiological and behavioral data.

Taste palatability is centrally involved in consumption decisions—we ingest foods that taste good and reject those that don't. Gustatory cortex (GC) and basolateral amygdala (BLA) almost certainly work together to mediate palatability-driven behavior, but the precise nature of their interplay during taste decision-making is still unknown. To probe this issue, we discretely perturbed (with optogenetics) activity in rats’ BLA→GC axons during taste deliveries. This perturbation strongly altered GC taste responses, but while the perturbation itself was tonic (2.5 s), the alterations were not—changes preferentially aligned with the onset times of previously-described taste response epochs, and reduced evidence of palatability-related activity in the ‘late-epoch’ of the responses without reducing the amount of taste identity information available in the ‘middle epoch.’ Finally, BLA→GC perturbations changed behavior-linked taste response dynamics themselves, distinctively diminishing the abruptness of ensemble transitions into the late epoch. These results suggest that BLA ‘organizes’ behavior-related GC taste dynamics.

9Animals need to remember the locations of nourishing and toxic food sources for survival, a fact 10 that necessitates a mechanism for associating taste experiences with particular places. We 11 have previously identified such responses within hippocampal place cells [1], the activity of 12 which is thought to aid memory-guided behavior by forming a mental map of an animal's 13 environment that can be reshaped through experience [2][3][4][5][6][7]. It remains unknown, however, 14 whether taste-responsiveness is intrinsic to a subset of place cells, or emerges as a result of 15 experience that reorganizes spatial maps. Here, we recorded from neurons in the dorsal CA1 16 region of rats running for palatable tastes delivered via intra-oral cannulae at specific locations 17 on a linear track. We identified a subset of taste-responsive cells that, even prior to taste 18 exposure, had larger place fields than non-taste-responsive cells overlapping with stimulus 19 delivery zones. Taste-responsive cells' place fields then contracted, as a result of taste 20 experience, leading to a stronger representation of stimulus delivery zones on the track. Taste-21 responsive units exhibited increased sharp-wave ripple co-activation during the taste delivery 22 session and subsequent rest periods, which correlated with the degree of place field 23 contraction. Our results reveal that novel taste experience evokes responses within a 24 preconfigured network of taste-responsive hippocampal place cells with large fields, whose 25 spatial representations are refined by sensory experience to signal areas of behavioral salience. 26This represents a possible mechanism by which animals identify and remember locations where 27 ecologically relevant stimuli are found within their environment. 28 29 Results and Discussion 33To investigate how hippocampal place cells responded to tastes during running, we recorded 34 the activity of CA1 neurons (n = 143, mean ± SEM: 28.6 ± 4.49 neurons/session; Figure S1A) 35 as rats (n = 5) ran back and forth on a linear track during a novel taste experience (Figure 1A). 36Each experimental day consisted of three track-running sessions ('Pre,' 'Tastes,' and 'Post') 37interleaved with rest sessions in a sleep box. During the 'Pre' and 'Post' probe sessions, rats 38 explored the track in the absence of tastes. During the 'Tastes' session, rats received aliquots of 39 either sweet or salty tastes, delivered directly to the tongue via intra-oral cannula when the rats 40 reached either of two designated locations along the track. Only experimental days that marked 41 rats' first exposure to this paradigm (in which animals were naïve to both the tastants and 42 delivery locations) were considered for further analysis. Isolated units were classified as putative 43 pyramidal cells (82.5%, 118/143) or interneurons (17.5%, 25/143) based on spike width and 44 firing rate (Figure S1B). Most pyramidal cells (99.2%, 117/118) could be categorized as place 45 cells (see STAR Methods, [1, 8]) and exhibited spatially reliable...