Donald Brian Katz

As is true in humans, no two rodents prefer precisely the same tastes. Furthermore, no one rodent keeps precisely the same taste preferences forever. Here, we have made use of this between- and within-animal variability to generate and test novel hypotheses about the stability and malleability of neural perceptual coding. We used a brief-access task (BAT) to reveal both individual differences in taste preferences and shifting preferences within individual rats (quantified in terms of lick bout lengths). We moved on to show that these phenomena are not simply random variation: first, by demonstrating that gustatory cortical (GC) taste response dynamics, the late part of which reflect palatability, match that individual rat’s BAT preferences (evaluated almost 2 weeks prior) better than canonical preference patterns; that is, individual differences in preferences reflect differences in neural taste processing. This match, however, links neural taste processing only to the most recent BAT session—GC palatability processing does not reflect performance in earlier BAT sessions. We hypothesized that any tasting experience might impact taste processing (i.e., not just BAT licking), and tested this hypothesis by adding a second session of GC taste-response recordings; palatability-epoch taste responses in this later session no longer matched the most recent pre-recording BAT session, demonstrating that responses following the first electrophysiology session had changed. Together, these data demonstrate that every tasting experience (regardless of the method of taste delivery) changes the rat’s processing of those tastes.

As is true in humans, no two rodents prefer precisely the same tastes. Furthermore, no one rodent keeps precisely the same taste preferences forever. Here, we have made use of this between- and within-animal variability to generate and test novel hypotheses about the stability and malleability of neural perceptual coding. We used a brief-access task (BAT) to reveal both individual differences in taste preferences and shifting preferences within individual rats (quantified in terms of lick bout lengths). We moved on to show that these phenomena are not simply random variation: first, by demonstrating that gustatory cortical (GC) taste response dynamics, the late part of which reflect palatability, match that individual rat’s BAT preferences (evaluated almost 2 weeks prior) better than canonical preference patterns; that is, individual differences in preferences reflect differences in neural taste processing. This match, however, links neural taste processing only to the most recent BAT session—GC palatability processing does not reflect performance in earlier BAT sessions. An implication of the fact that rats’ perceptual preferences shift across BAT sessions is that any tasting experience might impact taste processing, an implication that we tested by performing a second session of GC taste-response recordings—sessions in which tastes were delivered by intra-oral cannula to passive rats—and found that palatability-epoch taste responses in this later session no longer matched the most recent pre-recording BAT session. Together, these data demonstrate that every tasting experience (regardless of the method of taste delivery) changes the rat’s processing of those tastes.

Gustatory cortex (GC) plays a pivotal role in taste perception, expressing neural ensemble dynamics that reflect, in sequence, taste quality and hedonics, and that influence taste-guided behavior. The circuitry underlying these responses has traditionally been described as fixed and hardwired in adult rodents, although GC taste responses are known to change across multiple timescales of experience, including between sessions of novel taste exposure. Here, we show that responses change on an even smaller timescale—that in fact rapid, experience-dependent changes in GC responses occur across the first handful of taste exposure trials. Specifically, we show that the first 6–9 responses to novel taste stimuli in experimentally naive female lab rats are distinct from later trials in the same session: these earliest responses show less “stereotypical” dynamics and encode both taste identity and palatability less reliably than later responses; “normal” rat taste responses are not preexisting but rather develop across the first several minutes of taste exposure. This phenomenon, which is not taste-specific, is nonexistent (or nearly so) in later sessions. Furthermore, this rapid neural response plasticity is paralleled in changing licking behavior in response to the same stimuli. Together, these results provide novel insights into the real-time dynamics of sensory processing across novel-taste familiarization, essentially demonstrating that the taste system, rather than being hardwired, becomes “tuned up” by use.

Upon delivery of a taste onto the tongue, gustatory neural activity determines whether the stimulus is ingested or rejected. While some work in rodents has been devoted to investigating the neural activity leading to the rejection decision and its associated orofacial movements, little is known about what behaviors lead to ingestion of palatable tastes (and what neural activity is associated with that decision), largely because identifying ingestion-related behaviors is a difficult challenge—and probably undoable with video analysis given that the behaviors are largely intraoral. To address this gap in our understanding, we analyzed simultaneously-collected electromyographic (EMG) activity of the jaw opener muscle and the firing of gustatory cortical (GC) ensembles. We developed a machine-learning classifier to identify individual orofacial movements from EMG signals, demonstrating that it outperforms previously developed methods and using the technique to reveal three novel subtypes of ingestion-related tongue/mouth movements. Investigating the dynamics of these behaviors, we found that the frequency of occurrence of each type subtype shifts significantly at the time of the consumption decision, and is both tightly coupled with and reliably follows the transition in GC population activity into the state reflecting the tastant’s emotional/hedonic value. However, rather than the onset of single “ingestion” movement (as occurs for rejection decisions in the form of gapes), we show that the transition to ingestion is instead characterized by a collective change in the frequencies all ingestion-related behaviors. These findings demonstrate a direct link between neural dynamics in GC and the orchestration of the physical movements that define ingestive behavior, highlighting GC’s general role in taste perception, decision making, and the control of motor actions.

Conventionally, taste circuitry is considered feedforward, traveling up from the brainstem, with each additional node containing more sophisticated information. We challenge this convention by demonstrating that amygdala and cortex instead influence each other bidirectionally, yet in a direction-specific and asymmetric manner. These influences appear to drive different parts of the taste response, with distinct patterns for decision-making and behavioral output; furthermore, involvement in cortex-amygdala functional connectivity determines the strength of encoding in cortical single neurons.

Consumption varies across the stages (metestrus, diestrus, proestrus, estrus) of a rat's estrous cycle, changing in ways that might be expected to reflect, in part, a direct impact of hormones on taste palatability. Evidence regarding this hypothesis has been mixed, however, and critical within-subject experiments comparing consumption of multiple tastes with distinct valences across all estrous phases have been few. Here, we assayed female rats' licking of palatable (saccharin, sucrose, NaCl) and aversive (quinine-HCl, citric acid) tastes in brief-access trials, while tracking their estrous cycles through vaginal cytology. We observed sucrose palatability to be high at metestrus, the same phase at which the palatability of the aversive citric acid was low. These patterns were consistent across tastes of similar palatability, despite vast differences between the substances' receptor mechanisms and central impacts. Together, these results reveal a general (i.e., independent of particular tastant identity) magnification of palatability—higher than average for palatable tastes and lower for aversive tastes—centered largely on metestrus. We tested whether this phenomenon reflects lateral hypothalamic (LH) estradiol processing, by infusing LH with an estrogen receptor blocker (ICI182, 780) across five consecutive tasting sessions. Control infusions replicated the metestrus magnification of palatability; as predicted, ICI infusions blocked this effect, but estrogen receptor inhibition failed to render preferences “cycle free,” instead delaying the palatability magnification until diestrus. In summary, the estrous cycle directly mediates taste palatability in a manner involving hypothalamic actions of estradiol, but this effect is only one of several impacting consumption across the estrous cycle.

Upon delivery of a taste onto the tongue, gustatory neural activity determines whether the stimulus is ingested or rejected. While some work in rodents has been devoted to investigating the neural activity leading to the rejection decision and its associated orofacial movements, little is known about what behaviors lead to ingestion of palatable tastes (and what neural activity is associated with that decision), largely because identifying ingestion-related behaviors is a difficult challenge—and probably undoable with video analysis given that the behaviors are largely intraoral. To address this gap in our understanding, we analyzed simultaneously-collected electromyographic (EMG) activity of the jaw opener muscle and the firing of gustatory cortical (GC) ensembles. We developed a machine-learning classifier to identify individual orofacial movements from EMG signals, demonstrating that it outperforms previously developed methods and using the technique to reveal three novel subtypes of ingestion-related tongue/mouth movements. Investigating the dynamics of these behaviors, we found that the frequency of occurrence of each type subtype shifts significantly at the time of the consumption decision, and is both tightly coupled with and reliably follows the transition in GC population activity into the state reflecting the tastant’s emotional/hedonic value. However, rather than the onset of single “ingestion” movement (as occurs for rejection decisions in the form of gapes), we show that the transition to ingestion is instead characterized by a collective change in the frequencies all ingestion-related behaviors. These findings demonstrate a direct link between neural dynamics in GC and the orchestration of the physical movements that define ingestive behavior, highlighting GC’s general role in taste perception, decision making, and the control of motor actions.

Gustatory cortical (GC) and basolateral amygdalar (BLA) taste responses consist of an inter-regionally coherent 3-part state sequence. This coherence suggests that reciprocal BLA-GC connectivity is important for taste processing, but it remains unknown: 1) whether BLA-GC coherence actually reflects a reciprocal "conversation" (as opposed to one region simply driving the other); and 2) whether such a "conversation" has anything to do with the taste processing observed within GC response dynamics. Here, we address these questions using network and single-neuron analysis of simultaneously-recorded GC and BLA taste responses in awake rats. We find asymmetric, reciprocal μ-frequency influences that reflect taste processing dynamics: BLA→GC influence dominates between 300 and 1000msec (the epoch in which BLA codes palatability); afterward, when GC responses become palatability-related and GC has been shown to release a behavior-relevant signal, the direction of influence reverses, becoming GC→BLA. Follow-up analyses demonstrate that this "turn-taking" exists alongside effectively synchronous amygdala-cortical coupling-the two regions functioning as a unified structure. Finally, to assess the implications of these interactions for single-neuron responses, we tested the response properties of GC neurons categorized by their inferred connectivity with BLA: GC neurons influenced by BLA produce stronger taste-specific and palatability-related responses than other GC neurons, and the strongest taste encoding is specifically found in GC neurons that both influence and receive influence from BLA-those most deeply embedded in the reciprocal circuit. These results, consistent with findings in multiple systems, support the novel conclusion that taste processing and decision-making is a function of the amygdala-cortical loop.

The basolateral amygdala (BLA) is crucial for assigning emotional valence to sensory experiences, driving approach or avoidance behaviors during subsequent encounters. Particularly, the BLA plays a critical role in the coding, storage and retrieval of emotional learning. While traditionally viewed through the lens of memory consolidation, cholinergic signaling—mediated by dense inputs from the basal forebrain and abundant muscarinic receptors (mAChRs) in the BLA—plays a far more dynamic role. Acetylcholine, often described as a “memory molecule”, is central to this process, with scopolamine induced amnesia models underscoring its importance. Recent evidence suggests that cholinergic activity not only supports memory formation but also imparts emotional valence under specific conditions. This review examines the molecular and cellular mechanisms by which mAChR-mediated cholinergic signaling modulates BLA processing and the storage of emotional memories. We integrate psychopharmacological insights with loss and gain-of-function studies to demonstrate how cholinergic signaling in the BLA shapes approach and avoidance behaviors. Based on this evidence, we propose that acetylcholine’s influence in the BLA is highly context-dependent, reflecting its versatile role in emotional processing beyond mere memory consolidation.