Taste-Specific Neuronal Ensembles in the Gustatory Cortex of Awake Rats

Katz, Donald B.; Simon, S. A.; Nicolelis, Miguel A. L.

doi:10.1523/jneurosci.22-05-01850.2002

Cited by 92 publications

(65 citation statements)

References 47 publications

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“…Despite numerous reports of taste-specific discharge patterns in peripheral gustatory afferents (Ogawa et al, 1973(Ogawa et al, , 1974Nagai and Ueda, 1981;Dethier and Crnjar, 1982;Varkevisser et al, 2001) and central gustatory circuits (Di Lorenzo and Schwartzbaum, 1982;Katz et al, 2002b;Di Lorenzo and Victor, 2003;Verhagen and Scott, 2004), there have been comparatively few attempts to link discharge patterns to taste-guided behavioral responses. One series of experiments by Di Lorenzo and Hecht (1993) and asked whether taste-specific discharge patterns from neurons in the nucleus of the solitary tract (NST; the first synaptic relay for taste in vertebrates) modulate taste-guided licking responses of rats.…”

Section: Discussionmentioning

confidence: 99%

Temporal Coding Mediates Discrimination of “Bitter” Taste Stimuli by an Insect

Glendinning

Davis²,

Rai³

2006

J. Neurosci.

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The mechanisms that mediate discriminative taste processing in insects are poorly understood. We asked whether temporal patterns of discharge from the peripheral taste system of an insect (Manduca sexta caterpillars; Sphingidae) contribute to the discrimination of three "bitter" taste stimuli: salicin, caffeine, and aristolochic acid. The gustatory response to these stimuli is mediated exclusively by three pairs of bitter-sensitive taste cell, which are located in the medial, lateral, and epipharyngeal sensilla. We tested for discrimination by habituating the caterpillars to salicin and then determining whether the habituation generalized to caffeine or aristolochic acid. We ran habituation-generalization tests in caterpillars with their full complement of taste sensilla (i.e., intact) and in caterpillars with ablated lateral sensilla (i.e., lat-ablated). The latter perturbation enabled us to examine discrimination in caterpillars with a modified peripheral taste profile. We found that the intact and lat-ablated caterpillars both generalized the salicin-habituation to caffeine but not aristolochic acid. Next, we determined whether this pattern of stimulus-generalization could be explained by salicin and aristolochic acid generating distinct ensemble, rate, temporal, or spatiotemporal codes. To this end, we recorded excitatory responses from the bitter-sensitive taste cells and then used these responses to formulate predictions about whether the salicin-habituation should generalize to caffeine or aristolochic acid, separately for each coding framework. We found that the pattern of stimulus generalization in both intact and latablated caterpillars could only be predicted by temporal coding. We conclude that temporal codes from the periphery can mediate discriminative taste processing.

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Section: Discussionmentioning

confidence: 99%

Temporal Coding Mediates Discrimination of “Bitter” Taste Stimuli by an Insect

Glendinning

Davis²,

Rai³

2006

J. Neurosci.

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“…For each neuron the number of spikes that occurred in the 2.5 seconds immediately preceding (background activity) and following (evoked activity) each stimulus delivery was initially counted [8,9]. Single-trial spike counts were then grouped according to the tastant delivered, the sequence in which they occurred and the stimulus-delivery protocol employed, thus yielding sets of eight spike counts.…”

Section: Electrophysiological Data Analysismentioning

confidence: 99%

“…In two aspects the stimulus-delivery protocols that we employed in awake and restrained rats contrast with those used in previous studies of GC activity. In those studies food-or water-deprived rats controlled the time of stimulus delivery by bar pressing or freely licking [8,9,14,[21][22][23].…”

Section: Responses To Tastants In Animals Unable To Control the Delivmentioning

confidence: 99%

“…sucrose) and negative (e.g. quinine) tastants that were randomly, but contingently, delivered into the mouth via intra-oral cannulae (IOC) [8,9]. In these experiments, tastants were delivered only after water-deprived and head-restrained animals were sufficiently motivated to press a bar to receive both hedonically positive and negative tastants.…”

Section: Introductionmentioning

confidence: 99%

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Behavioral and neural responses to gustatory stimuli delivered non-contingently through intra-oral cannulas

Soares

Stapleton

Rodríguez

et al. 2007

Physiology & Behavior

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The act of eating requires a decision by an animal to place food in its mouth. The reasons to eat are varied and include hunger as well as the food's expected reward value. Previous studies of tastant processing in the rat primary gustatory cortex (GC) have used either anesthetized or awake behaving preparations that yield somewhat different results. Here we have developed a new preparation in which we explore the influences of intra-oral and non-contingent tastant delivery on rats' behavior and on their GC neural responses. We recorded single unit activity in the rat GC during two sequences of tastant deliveries, PRE and POST, which were separated by a waiting period. Six tastants ranging in hedonic value from sucrose to quinine were delivered in the first two protocols called 4TW and L-S. In the third one, the App L-S protocol, only hedonically positive tastants were used. In the 4TW protocol, tastants were delivered in blocks whereas in the two L-S protocols tastants were randomly interleaved.In the 4TW and L-S protocols the probability of ingesting tastants in the PRE sequence decreased exponentially with the trial number. Moreover, in both protocols this decrease was greater in the POST than in the PRE sequence likely because the subjects learned that unpleasant tastants were to be delivered. In the App L-S protocol the decrease in ingestion was markedly slower than in the other protocols, thus supporting the hypothesis that the decrease in appetitive behavior arises from the noncontingent intra-oral delivery of negatively hedonic tastants like quinine.Although neuronal responses in the three protocols displayed similar variability levels, significant differences existed between the protocols in the way the variability was partitioned between chemosensory and non-chemosensory neurons. While in the 4TW and L-S protocols the former population displayed more changes than the latter, in the App L-S protocol variability was homogeneously distributed between the two populations. We posit that these tuning changes arise,

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“…In fact, the second prediction is that piriform cortical neurons may show spatiotemporal response complexity, given the dynamics of glomerular (Spors et al, 2006) and mitral/ tufted cell (Meredith, 1986;Mazor and Laurent, 2005) odorant responses in the time range of 0.1-1 s. Third, cortical cell activity may not solely be driven by afferent input but may also reflect intracortical cell-cell interactions. Cross-correlation analyses of simultaneously recorded spike trains can be used to identify such interactions (Perkel et al, 1967;Gerstein and Perkel, 1972;Katz et al, 2002). In this series of studies, we sought initial evidence for these three predictions using microelectrode array and paired single-unit recording techniques.…”

Section: Introductionmentioning

confidence: 99%

Spatial and Temporal Distribution of Odorant-Evoked Activity in the Piriform Cortex

Rennaker¹,

Chen²,

Ruyle³

et al. 2007

J. Neurosci.

191

183

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Despite a remarkably precise spatial representation of odorant stimuli in the early stages of olfactory processing, the projections to the olfactory (piriform) cortex are more diffuse and show characteristics of a combinatorial array, with extensive overlap of afferent inputs and widespread intracortical association connections. Furthermore, although there is increasing evidence for the importance of temporal structure in olfactory bulb odorant-evoked output, little is known about how this temporal patterning is translated within cortical neural ensembles. The present study used multichannel electrode arrays and paired single-unit recordings in rat anterior piriform cortex to test several predictions regarding ensemble coding in this system. The results indicate that odorants evoke activity in a spatially scattered ensemble of anterior piriform cortex neurons, and the ensemble activity includes a rich temporal structure. The most pronounced discrimination between different odorants by cortical ensembles occurs during the first inhalation of a 2 s stimulus. The distributed spatial and temporal structure of cortical activity is present at both global and local scales, with neighboring single units contributing to coding of different odorants and active at different phases of the respiratory cycle. Finally, cross-correlogram analyses suggest that cortical unit activity reflects not only afferent input from the olfactory bulb but also intrinsic activity within the intracortical association fiber system. These results provide direct evidence for predictions stemming from anatomical-and theoretical-based models of piriform cortex.

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Taste-Specific Neuronal Ensembles in the Gustatory Cortex of Awake Rats

Cited by 92 publications

References 47 publications

Temporal Coding Mediates Discrimination of “Bitter” Taste Stimuli by an Insect

Temporal Coding Mediates Discrimination of “Bitter” Taste Stimuli by an Insect

Behavioral and neural responses to gustatory stimuli delivered non-contingently through intra-oral cannulas

Spatial and Temporal Distribution of Odorant-Evoked Activity in the Piriform Cortex

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