Spatially Distributed Representation of Taste Quality in the Gustatory Insular Cortex of Behaving Mice.
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ABSTRACT:
SUBMITTER: Chen K
PROVIDER: S-EPMC7855361 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Research over the past decade has established the gustatory insular cortex (GC) as a model for studying how primary sensory cortices integrate sensory, affective, and cognitive signals. This integration occurs through time-varying patterns of neural activity. Selective silencing of GC activity during specific temporal windows provided evidence for GC's role in mediating taste palatability and expectation. Recent results also suggest that this area may play a role in decision making. However, existing data are limited to GC involvement in controlling the timing of stereotyped, orofacial reactions to aversive tastants during consumption. Here, we present electrophysiological, chemogenetic, and optogenetic results demonstrating the key role of GC in the execution of a taste-guided, reward-directed decision-making task. Mice were trained in a two-alternative choice task, in which they had to associate tastants sampled from a central spout with different actions (i.e., licking either a left or a right spout). Stimulus sampling and action were separated by a delay period. Electrophysiological recordings revealed chemosensory processing during the sampling period and the emergence of task-related, cognitive signals during the delay period. Chemogenetic silencing of GC impaired task performance. Optogenetic silencing of GC allowed us to tease apart the contribution of activity during sampling and delay periods. Although silencing during the sampling period had no effect, silencing during the delay period significantly impacted behavioral performance, demonstrating the importance of the cognitive signals processed by GC in driving decision making. Altogether, our data highlight a novel role of GC in controlling taste-guided, reward-directed choices and actions.
| S-EPMC7239762 | biostudies-literature
Project description:Previous studies have shown that the conceptual representation of food involves brain regions associated with taste perception. The specificity of this response, however, is unknown. Does viewing pictures of food produce a general, nonspecific response in taste-sensitive regions of the brain? Or is the response specific for how a particular food tastes? Building on recent findings that specific tastes can be decoded from taste-sensitive regions of insular cortex, we asked whether viewing pictures of foods associated with a specific taste (e.g., sweet, salty, and sour) can also be decoded from these same regions, and if so, are the patterns of neural activity elicited by the pictures and their associated tastes similar? Using ultrahigh-resolution functional magnetic resonance imaging at high magnetic field strength (7-Tesla), we were able to decode specific tastes delivered during scanning, as well as the specific taste category associated with food pictures within the dorsal mid-insula, a primary taste responsive region of brain. Thus, merely viewing food pictures triggers an automatic retrieval of specific taste quality information associated with the depicted foods, within gustatory cortex. However, the patterns of activity elicited by pictures and their associated tastes were unrelated, thus suggesting a clear neural distinction between inferred and directly experienced sensory events. These data show how higher-order inferences derived from stimuli in one modality (i.e., vision) can be represented in brain regions typically thought to represent only low-level information about a different modality (i.e., taste).
| S-EPMC7812770 | biostudies-literature
Project description:BackgroundRight insular cortex is involved in taste discrimination, but its functional organization is still poorly known. In general, sensory cortices represent the spatial prevalence of relevant features for each sensory modality (visual, auditory, somatosensory) in an ordered way across the cortical space. Following this analogy, we hypothesized that primary taste cortex is organized in similar ordered way in response to six tastes with known receptorial mechanisms (sweet, bitter, sour, salt, umami, CO2).DesignTen normal subjects were enrolled in a pilot study. We used functional magnetic resonance imaging (fMRI), a high resolution cortical registration method, and specialized procedures of feature prevalence localization, to map fMRI responses within the right insular cortex, to water solutions of quinine hydrochloride (bitter), Acesulfamate K (sweet), sodium chloride (salt), mono potassium glutamate + inosine 5' mono phosphate (Umami), citric acid (sour) and carbonated water (CO2). During an fMRI scan delivery of the solutions was applied in pseudo-random order interleaved with cleaning water.ResultsTwo subjects were discarded due to excessive head movements. In the remaining subjects, statistically significant activations were detected in the fMRI responses to all tastes in the right insular cortex (p<0.05, family-wise corrected for multiple comparisons). Cortical representation of taste prevalence highlighted two spatially segregated clusters, processing two and three tastes coupled together (sweet-bitter and salt-umami-sour), with CO2 in between.ConclusionsCortical representation of taste prevalence within the right primary taste cortex appears to follow the ecological purpose of enhancing the discrimination between safe nutrients and harmful substances.
| S-EPMC5744997 | biostudies-literature
Project description:The mammalian tongue contains gustatory receptors tuned to basic taste types, providing an evolutionarily old hedonic compass for what and what not to ingest. Although representation of these distinct taste types is a defining feature of primary gustatory cortex in other animals, their identification has remained elusive in humans, leaving the demarcation of human gustatory cortex unclear. Here we used distributed multivoxel activity patterns to identify regions with patterns of activity differentially sensitive to sweet, salty, bitter, and sour taste qualities. These were found in the insula and overlying operculum, with regions in the anterior and middle insula discriminating all tastes and representing their combinatorial coding. These findings replicated at super-high 7 T field strength using different compounds of sweet and bitter taste types, suggesting taste sensation specificity rather than chemical or receptor specificity. Our results provide evidence of the human gustatory cortex in the insula.
| S-EPMC6401093 | biostudies-literature
Project description:Novel taste memories, critical for animal survival, are consolidated to form long term memories which are dependent on translation regulation in the gustatory cortex We used microarray for identification of genes involved in novel taste learning at two time points- 1 and 3 hours following memory formation for novel taste Adult rats were separated into two groups- novel tatse (0.1% sacchain) and water, two time points were used 1, 3 hours following learnin. Rna was extracted and hybridized on Affymetrix microarray
2016-03-23 | E-GEOD-74546 | biostudies-arrayexpress
Project description:Through learning processes, cues associated with emotionally salient reinforcing outcomes can come to act as substitutes for the reinforcer itself. According to one account of this phenomenon, the predictive cue associatively elicits a representation of the expected outcome by reactivating cells responsible for encoding features of the primary reinforcer. We tested this hypothesis by examining the role of neural ensembles in gustatory cortex (GC) during receipt of gustatory stimuli (sucrose and water) and cues associated with those stimuli using the immediate early genes (IEGs) Arc and Homer1a. Because these plasticity-related IEGs are expressed in the neuronal nucleus 5 and 30 min, respectively, after salient events, we examined how individual neurons encoded these stimuli in two separate behavioral epochs. In experiment 1, we showed that tasting identical sucrose solutions, but not tasteless water, in the two epochs increased both IEG activity and the degree of overlap between neural ensembles in GC. In experiment 2, odor cues associated with sucrose, but not water, evoked potentiation of IEG activity in GC similar to sucrose itself. Surprisingly, lesions of the basolateral amygdala had minimal effects on associative encoding in GC. Finally, these associatively driven representations of sucrose appeared to be outcome specific, as neural ensembles that were activated by the sucrose-associated cue were also activated by sucrose itself. This degree of overlap between associative and primary taste activity at the ensemble level suggests that GC neurons encode important information about anticipated outcomes. Such representations may provide outcome-specific information for guiding goal-directed behavior.
| S-EPMC2823084 | biostudies-other
Project description:Novel taste memories, critical for animal survival, are consolidated to form long term memories which are dependent on translation regulation in the gustatory cortex We used microarray for identification of genes involved in novel taste learning at two time points- 1 and 3 hours following memory formation for novel taste
2016-03-23 | GSE74546 | GEO
Project description:In the mammalian brain, the insula is the primary cortical substrate involved in the perception of taste. Recent imaging studies in rodents have identified a "gustotopic" organization in the insula, whereby distinct insula regions are selectively responsive to one of the five basic tastes. However, numerous studies in monkeys have reported that gustatory cortical neurons are broadly-tuned to multiple tastes, and tastes are not represented in discrete spatial locations. Neuroimaging studies in humans have thus far been unable to discern between these two models, though this may be because of the relatively low spatial resolution used in taste studies to date. In the present study, we examined the spatial representation of taste within the human brain using ultra-high resolution functional magnetic resonance imaging (MRI) at high magnetic field strength (7-tesla). During scanning, male and female participants tasted sweet, salty, sour, and tasteless liquids, delivered via a custom-built MRI-compatible tastant-delivery system. Our univariate analyses revealed that all tastes (vs tasteless) activated primary taste cortex within the bilateral dorsal mid-insula, but no brain region exhibited a consistent preference for any individual taste. However, our multivariate searchlight analyses were able to reliably decode the identity of distinct tastes within those mid-insula regions, as well as brain regions involved in affect and reward, such as the striatum, orbitofrontal cortex, and amygdala. These results suggest that taste quality is not represented topographically, but by a distributed population code, both within primary taste cortex as well as regions involved in processing the hedonic and aversive properties of taste.SIGNIFICANCE STATEMENT The insula is the primary cortical substrate involved in taste perception, yet some question remains as to whether this region represents distinct tastes topographically or via a population code. Using high field (7-tesla), high-resolution functional magnetic resonance imaging in humans, we examined the representation of different tastes delivered during scanning. All tastes activated primary taste cortex within the bilateral mid-insula, but no brain region exhibited any consistent taste preference. However, multivariate analyses reliably decoded taste quality within the bilateral mid-insula as well as the striatum, orbitofrontal cortex, and bilateral amygdala. This suggests that taste quality is represented by a spatial population code within regions involved in sensory and appetitive properties of taste.
| S-EPMC6989007 | biostudies-literature
Project description:Events separated in time are associatively learned in trace conditioning, recruiting more neuronal circuits and molecular mechanisms than in delay conditioning. However, it remains unknown whether a given sensory memory trace is being maintained as a unitary item to associate. Here, we used conditioned taste aversion learning in the rat model, wherein animals associate a novel taste with visceral nausea, and demonstrate that there are two parallel memory traces of a novel taste: a short-duration robust trace, lasting approximately 3?hr, and a parallel long-duration weak one, lasting up to 8?hr, and dependent on the strong trace for its formation. Moreover, only the early robust trace is maintained by a NMDAR-dependent CaMKII- AMPAR pathway in the insular cortex. These findings suggest that a memory trace undergoes rapid modifications, and that the mechanisms underlying trace associative learning differ when items in the memory are experienced at different time points.
| S-EPMC4703067 | biostudies-literature
Project description:Novel taste memories, critical for animal survival, are consolidated to form long term memories which are dependent on translation regulation in the gustatory cortex (GC) hours following acquisition. However, the role of transcription regulation in the process is unknown.Here, we report that transcription in the GC is necessary for taste learning in rats, and that drinking and its consequences, as well as the novel taste experience, affect transcription in the GC during taste memory consolidation. We show differential effects of learning on temporal dynamics in set of genes in the GC, including Arc/Arg3.1, known to regulate the homeostasis of excitatory synapses.We demonstrate that in taste learning, transcription programs were activated following the physiological responses (i.e., fluid consumption following a water restriction regime, reward, arousal of the animal, etc.) and the specific information about a given taste (i.e., taste novelty). Moreover, the cortical differential prolonged kinetics of mRNA following novel versus familiar taste learning may represent additional novelty related molecular response, where not only the total amount, but also the temporal dynamics of transcription is modulated by sensory experience of novel information.
| S-EPMC4746785 | biostudies-literature