Gustatory Cortex Neurons Research Articles

Inactivation of Basolateral Amygdala Specifically Eliminates Palatability-Related Information in Cortical Sensory Responses

Evidence indirectly implicates the amygdala as the primary processor of emotional information used by cortex to drive appropriate behavioral responses to stimuli. Taste provides an ideal system with which to test this hypothesis directly, as neurons in both basolateral amygdala (BLA) and gustatory cortex (GC)-anatomically interconnected nodes of the gustatory system-code the emotional valence of taste stimuli (i.e., palatability), in firing rate responses that progress similarly through "epochs." The fact that palatability-related firing appears one epoch earlier in BLA than GC is broadly consistent with the hypothesis that such information may propagate from the former to the latter. Here, we provide evidence supporting this hypothesis, assaying taste responses in small GC single-neuron ensembles before, during, and after temporarily inactivating BLA in awake rats. BLA inactivation (BLAx) changed responses in 98% of taste-responsive GC neurons, altering the entirety of every taste response in many neurons. Most changes involved reductions in firing rate, but regardless of the direction of change, the effect of BLAx was epoch-specific: while firing rates were changed, the taste specificity of responses remained stable; information about taste palatability, however, which normally resides in the "Late" epoch, was reduced in magnitude across the entire GC sample and outright eliminated in most neurons. Only in the specific minority of neurons for which BLAx enhanced responses did palatability specificity survive undiminished. Our data therefore provide direct evidence that BLA is a necessary component of GC gustatory processing, and that cortical palatability processing in particular is, in part, a function of BLA activity.

Distinct neural ensembles in the rat gustatory cortex encode salt and water tastes

The gustatory cortex (GC) is important for perceiving the intensity of tastants but it remains unclear as to how single neurons in the region carry out this function. Previous studies have shown that taste-evoked activity from single neurons in GC can be correlated or anticorrelated with tastant concentration, yet whether one or both neural responses signal intensity is poorly characterized because animals from these studies were not trained to report the intensity of the concentration that they tasted. To address this issue, we designed a two-alternative forced choice (2-AFC) task in which freely licking rats distinguished among concentrations of NaCl and recorded from ensembles of neurons in the GC. We identified three neural ensembles that rapidly (<300 ms or ∼2 licks) processed NaCl concentration. For two ensembles, their NaCl evoked activity was anticorrelated with NaCl concentration but could be further distinguished by their response to water; in one ensemble, water evoked the greatest response while in the other ensemble the lowest tested NaCl concentration evoked the greatest response. However, the concentration sensitive activity from each of these ensembles did not show a strong association with the behaviour of the rat in the 2-AFC task, suggesting a lesser role for signalling tastant intensity. Conversely, for a third neural ensemble, its neural activity was well correlated with increases in NaCl concentration, and this relationship best matched the intensity perceived by the rat. These results suggest that this neuronal ensemble in GC whose activity monotonically increases with concentration plays an important role in signalling the intensity of the taste of NaCl.

Amygdala Stimulation Evokes Time-Varying Synaptic Responses in the Gustatory Cortex of Anesthetized Rats

Gustatory stimuli are characterized by a specific hedonic value; they are either palatable or aversive. Hedonic value, along with other psychological dimensions of tastes, is coded in the time-course of gustatory cortex (GC) neural responses and appears to emerge via top-down modulation by the basolateral amygdala (BLA). While the importance of BLA in modulating gustatory cortical function has been well established, the nature of its input onto GC neurons is largely unknown. Somewhat conflicting results from extracellular recordings point to either excitatory or inhibitory effects. Here, we directly test the hypothesis that BLA can evoke time-varying – excitatory and inhibitory – synaptic responses in GC using in vivo intracellular recording techniques in urethane anesthetized rats. Electrical stimulation of BLA evoked a post-synaptic potential (PSP) in GC neurons that resulted from a combination of short and long latency components: an initial monosynaptic, glutamatergic potential followed by a multisynaptic, GABAergic hyperpolarization. As predicted by the dynamic nature of amygdala evoked potentials, trains of five BLA stimuli at rates that mimic physiological firing rates (5–40 Hz) evoke a combination of excitation and inhibition in GC cells. The magnitude of the different components varies depending on the frequency of stimulation, with summation of excitatory and inhibitory inputs reaching its maximum at higher frequencies. These experiments provide the first description of BLA synaptic inputs to GC and reveal that amygdalar afferents can modulate gustatory cortical network activity and its processing of sensory information via time-varying synaptic dynamics.

Associatively Learned Representations of Taste Outcomes Activate Taste-Encoding Neural Ensembles in Gustatory Cortex

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.

Forebrain neurons that project to the gustatory parabrachial nucleus in rat lack glutamic acid decarboxylase.

Evidence suggests that GABA might mediate the inhibitory influence of centrifugal inputs on taste-evoked responses in the parabrachial nucleus (PBN). Previous studies show that activation of the gustatory cortex (GC), bed nucleus of the stria terminalis (BNST), central nucleus of the amygdala (CeA), and lateral hypothalamus (LH) inhibits PBN taste responses, GABAergic neurons are present in these forebrain regions, and GABA reduces the input resistance of PBN neurons. The present study investigated the expression of glutamic acid decarboxylase immunoreactivity (GAD_67 ir) in GC, BNST, CeA, and LH neurons that project to the PBN in rats. After anesthesia (50 mg/kg ip Nembutal), injections of the retrograde tracer Fluorogold (FG) were made in the physiologically defined gustatory PBN. Brain tissue containing the above forebrain structures was processed and examined for FG and GAD_67 ir. Similar to previous studies, each forebrain site contained retrogradely labeled neurons. Our results suggest further that the major source of input to the PBN taste region is the CeA (608 total cells) followed by GC (257 cells), LH (106 cells), and BNST (92 cells). This suggests a differential contribution to centrifugal control of PBN taste processing. We further show that despite the presence of GAD_67 neurons in each forebrain area, colocalization was extremely rare, occurring only in 3 out of 1,063 FG-labeled cells. If we assume that the influence of centrifugal input is mediated by direct projections to the gustatory region of the PBN, then GABAergic forebrain neurons apparently are not part of this descending pathway.

Ensembles of gustatory cortical neurons anticipate and discriminate between tastants in a single lick

The gustatory cortex (GC) processes chemosensory and somatosensory information and is involved in learning and anticipation. Previously we found that a subpopulation of GC neurons responded to tastants in a single lick (Stapleton et al., 2006). Here we extend this investigation to determine if small ensembles of GC neurons, obtained while rats received blocks of tastants on a fixed ratio schedule (FR5), can discriminate between tastants and their concentrations after a single 50 μL delivery. In the FR5 schedule subjects received tastants every fifth (reinforced) lick and the intervening licks were unreinforced. The ensemble firing patterns were analyzed with a Bayesian generalized linear model whose parameters included the firing rates and temporal patterns of the spike trains. We found that when both the temporal and rate parameters were included, 12 of 13 ensembles correctly identified single tastant deliveries. We also found that the activity during the unreinforced licks contained signals regarding the identity of the upcoming tastant, which suggests that GC neurons contain anticipatory information about the next tastant delivery. To support this finding we performed experiments in which tastant delivery was randomized within each block and found that the neural activity following the unreinforced licks did not predict the upcoming tastant. Collectively, these results suggest that after a single lick ensembles of GC neurons can discriminate between tastants, that they may utilize both temporal and rate information, and when the tastant delivery is repetitive ensembles contain information about the identity of the upcoming tastant delivery.

Differential Spatial Representation of Taste Modalities in the Rat Gustatory Cortex

Discrimination between foods is crucial for the nutrition and survival of animals. Remarkable progress has been made through molecular and genetic manipulations in the understanding of the coding of taste at the receptor level. However, much less is known about the cortical processing of taste sensation and the organizing principles of the gustatory cortex (GC). Using genetic tracing, it has recently been shown that sweet and bitter taste are processed through segregated neuronal circuitries along the gustatory pathway up to the cortical level. This is in disagreement with the evidence that GC neurons recorded in both anesthetized and behaving animals responded to multiple taste modalities (including sweet and bitter). To investigate the functional architecture of the GC in regard to taste modalities, we used in vivo intrinsic optical imaging, a technique that has been successfully applied to explore the organization of other neocortical regions. We found that four of the primary taste modalities (sweet, bitter, salty, and sour) are represented by distinctive spatial patterns but that no region was specific to a single modality. In addition, we found that two tastants of similar hedonic value (pleasant or unpleasant) activated areas with more common regions than two tastants with opposite hedonic value. In summary, we propose that these specific cortical patterns can be used to discriminate among various tastants.

Effects of acetylcholine on coding of taste information in the primary gustatory cortex in rats

Acetylcholine (ACh) receptors are widely distributed throughout the cerebral cortex in rats. Recently, cholinergic innervation of the gustatory cortex (GC) was reported to be involved in certain taste learning in rats. Here, the effects of iontophoretic application of ACh on the response properties of GC neurons were studied in urethane-anesthetized rats. ACh affected spontaneous discharges in a small fraction of taste neurons (11 of 86 neurons tested), but influenced taste responses in 27 of 43 neurons tested. No correlations with ACh susceptibility were noted for spontaneous discharges and taste responses. Among the 27 neurons, ACh facilitated taste responses in 13, inhibited taste responses in 13 and either facilitated or inhibited taste responses depending on the stimuli in 1. Furthermore, ACh affected the responses to best stimuli that produced the largest responses among four basic tastants (best responses) in 7 of 27 taste neurons, to non-best responses in 9, and to both best and non-best responses in 11. ACh mostly inhibited the best responses (13 of 18 neurons). Thus, ACh often decreased the response selectivity to the four basic tastants and changed the response profile. Atropine, a general antagonist of muscarinic receptors, antagonized ACh actions on taste responses or displayed the opposite effects on taste responses to ACh actions in two-thirds of the neurons tested. These findings indicate that ACh mostly modulates taste responses through muscarinic receptors, and suggest that ACh shifts the state of the neuron network in the GC, in terms of the response selectivities and response profiles.

Searching for the bitter truth: Insights into receptors for taste

Searching for the bitter truth: Insights into receptors for taste

Differential Encoding of Behavior and Spatial Context in Deep and Superficial Layers of the Neocortex

Rodent hippocampal activity is correlated with spatial and behavioral context, but how context affects coding in association neocortex is not well understood. The cellular distribution of the neural activity-regulated immediate-early gene Arc was used to monitor the activity history of cells in CA1, and in deep and superficial layers of posterior parietal and gustatory cortices (which encode movement and taste, respectively), during two behavioral epochs in which spatial and behavioral context were independently manipulated while gustatory input was held constant. Under conditions in which the hippocampus strongly differentiated behavioral and spatial contexts, deep parietal and gustatory layers did not discriminate between spatial contexts, whereas superficial layers in both neocortical regions discriminated well. Deep parietal cells discriminated behavioral context, whereas deep gustatory cortex neurons encoded the two conditions identically. Increased context sensitivity of superficial neocortical layers, which receive more hippocampal outflow, may reflect a general principle of neocortical organization for memory retrieval.

Neural signature of taste familiarity in the gustatory cortex of the freely behaving rat.

Ample data indicate that the gustatory cortex (GC) subserves the processing, encoding, and storage of taste information. To further elucidate the neural processes involved, we recorded multi-unit activity in the GC of the freely behaving rat as it became familiar with a novel tastant. Exposure to the tastant was performed over three 40- to 50-min sessions, 24 h apart. In each session, the tastant was presented repeatedly, 1 s at a time, with 10- to 12-s inter-trial intervals. The neural response to the tastant typically lasted 7 s. Our results show that the average neuronal response to the tastant increased as this tastant became familiar, but this increase was detected only during the last 5 s of the response. The increased response was not generalized to another tastant. Furthermore, our analysis suggests that specific neuronal populations subserve the processing of familiarity of specific tastants. The signature of familiarity was not detected in the course of the familiarization session, but only on the subsequent day, suggesting that its development involves slow post-acquisition processes. Our data are in line with the notion that GC neurons process multiple taste attributes, familiarity included, during different temporal phases of their response. The data also suggest that by default the brain considers a taste stimulus as novel, unless proven otherwise.

Dynamic and Multimodal Responses of Gustatory Cortical Neurons in Awake Rats

To investigate the dynamic aspects of gustatory activity, we recorded the responses of small ensembles of cortical neurons to tastants administered to awake rats. Multiple trials of each tastant were delivered during recordings made in oral somatosensory (SI) and gustatory cortex (GC). When integrated tastant responses (firing rates averaged across 2.5 sec) were compared with water responses, 14.4% (13/90) of the GC neurons responded in a taste-specific manner. When time was considered as a source of information, however, the incidence of taste-specific firing increased: as many as 41% (37/90) of the recorded GC neurons exhibited taste-specific patterns of response. For 17% of the neurons identified as responding with taste-specific patterns, the stimulus that caused the most significant response was a function of the time since stimulus delivery. That is, a single neuron might respond most strongly to one tastant in the first 500 msec of a response and then respond most strongly to another tastant later in the response. Further analysis of the time courses of GC and SI cortical neural responses revealed that modulations of GC firing rate arose from three separable processes: early somatosensory input (less than approximately 0.2 sec post-stimulus), later chemosensory input ( approximately 0.2-1 sec), and delayed somatosensory input related to orofacial responses (more than approximately 1.0 sec). These data demonstrate that sensory information is available in the time course of GC responses and suggest the viability of views of gustatory processing that treat the temporal structure of cortical responses as an integral part of the neural code.

Gustatory neural coding in the monkey cortex: the quality of sweetness

1. We analyzed the activity of single neurons in gustatory cortex of alert cynomolgus monkeys in response to the four basic taste stimuli and to a range of chemicals, all of which are predominantly sweet to humans. 2. We recorded taste-evoked responses from a cortical area that measured 4.0 mm in its anteroposterior extent, 5.6 mm dorsoventrally and 2.2 mm mediolaterally. Taste-responsive neurons constituted 4.7% of the 3,066 neurons tested in the course of 66 recording tracks. Nongustatory cells included those responsive to mouth movement (34.1%), tongue touch (1.9%), stimulus approach (0.7%), and tongue extension (0.5%). The functions of 58.2% of the cells we isolated could not be determined. 3. The mean breadth of tuning of these cortical taste neurons was a moderate 0.59 (range 0.00-0.93). 4. There was no evidence that taste cells with similar functional attributes were clustered in the cortex, i.e., there was no apparent topographic organization of taste qualities. 5. A taste space was generated from the correlations among patterns of neural activity evoked by the stimulus array. Within the space, NaCl was most isolated from other stimuli; the profiles elicited by HCl, quinine HCl, and water were all moderately intercorrelated and were clearly distinct from the cluster of sweet stimuli. 6. The 19 sweet chemicals formed a coherent cluster centered on the simple carbohydrates (glucose, fructose, sucrose, maltose) and sorbitol. Nearest this core were calcium cyclamate, aspartame, and cran-raspberry juice. In the next concentric ring were acesulfame potassium, xylose, xylitol, sorbose, polycose, and myoinositol. Increasingly distant from the sugars were sodium saccharin, stevioside, neohesperidin DHC, L-tryptophan and monellin. 7. We compared these results with those of a human psychophysical study of sweet stimuli. Using the position of glucose as a reference, we measured the distances to all other stimuli that were common to the two studies (n = 15). The correlation between the human psychophysical data and those derived from evoked activity in the macaque cortex was +0.82. 8. The high correlation between human psychophysical and macaque electrophysiological data implies that the subtle distinctions among stimuli that are predominantly sweet are quite similar for these two species and reinforces the value of this neural model for human taste perception.

Gustatory neural coding in the monkey cortex: stimulus intensity

1. We analyzed the activity of single neurons in gustatory cortex of alert cynomolgus monkeys in response to a range of stimulus intensities. Chemicals were deionized water, fruit juice, and several concentrations of the four prototypical taste stimuli: 10(-3)-1.0 M glucose, 10(-3)-1.0 M NaCl, 10(-4)-3 x 10(-2) M HCl, and 10(-5)-3 x 10(-3) M quinine HCl. 2. Taste-evoked responses could be recorded from a cortical gustatory area that measured 2.5 mm in its anteroposterior extent, 6.0 mm dorsoventrally, and 3.0 mm mediolaterally. Taste-responsive cells constituted 62 (3.7%) of the 1,661 neurons tested. Nongustatory cells gave responses associated with mouth movement (10.1%), somatosensory stimulation (2.2%), and approach or anticipation (0.9%). 3. Intensity-response functions were determined across 62 gustatory neurons. Neural thresholds for each stimulus quality conformed well to human psychophysical thresholds. Mean discharge rate was a direct function of stimulus concentration for glucose, NaCl, and quinine HCl. The most effective of the basic stimuli was glucose. 4. Power function exponents were calculated from the responses of neural subgroups most responsive to each basic stimulus. Those for glucose, NaCl, and quinine were within the range of psychophysically derived values. Thus the perceived intensity of each basic quality is presumably based on the activity of the appropriate neural subgroup rather than on the mean activity of all taste cells. 5. The mean breadth-of-tuning (entropy) coefficient for 62 gustatory neurons was 0.65 (range, 0.00-0.98). 6. There was no clear evidence of chemotopic organization in the gustatory cortex. 7. An analysis of taste quality indicated that sweet stimuli evoked patterns of activity that were clearly distinct from those of the nonsweet chemicals. Among the latter group, NaCl was differentiable from HCl and quinine HCl, whose patterns were closely related. 8. The response characteristics of cortical taste cells imply gustatory thresholds and intensity-response functions for the nonhuman primate that conform well to those reported in psychophysical studies of humans, reinforcing the value of this neural model for human taste intensity perception.