Gustatory responses of cortical neurons in rats. III. Neural and behavioral measures compared

The responses of 39 cortical neurons to 13 kinds of taste stimuli including the four putative basic taste solutions (sucrose, NaCl, HCl, and quinine HCl) applied to the anterior portion of the tongue were recorded extracellularly in lightly anesthetized rats. The neural responses were analyzed in terms of the four hypotheses of quality coding: across-neuron response pattern, labeled-line, matrix pattern, and across-region response pattern notions. Animals were given a conditioned taste aversion to one of the 11 stimuli by pairing it with a gastrointestinal illness caused by intraperitoneal injection of 0.15 M LiCl. Behavioral taste profiles were constructed for each stimulus from the suppression of rate of drinking, which indicates the extent of generalization of aversion to each of the four basic taste stimuli. Neural taste profiles of each taste stimulus, which indicate the relation of the taste of a stimulus to each taste of the four basic stimuli, differed more or less depending on the kind of quality-coding notions employed. Among the four analyses, across-region correlation coefficients that were derived from an across-region response-pattern theory showed the highest correlation with the behavioral suppression rates. Therefore we conclude that processing of taste information in the cortex involves differences in both response magnitude across neurons and the spatial localization of those neurons. Fluid intake per day of each of the 12 taste solutions was measured by the single-bottle preference method. When the amount of intake was described in terms of an hedonic index (HI), which indicates the hedonic aspect of the taste of each solution, HI's for sucrose, NaCl, HCl, and quinine were 1.17, 0.43, -0.49, and -0.89, respectively. These values represent the degree of deviation of solution intake above (i.e., preferable) or below (aversive) the standard water intake. Then, HI's were calculated for each of the 12 taste stimuli based on the neural taste profiles and actual HI's for each of the four basic taste stimuli. The correlations between the calculated and the actual (or behaviorally obtained) HI's were very high (ranging from 0.832 to 0.941). This result suggests that the hedonic dimension of taste can be matched well by any one of the four proposed hypotheses.     

Studies on gustatory responses of amygdaloid neurons in rats

Summary The responses of 80 amygdaloid neurons to the four basic taste (sucrose, NaCl, HCl and quinine hydrochloride), thermal (5° C, 20° C and 40° C) and tactile (brushing) stimuli applied to the anterior part of the tongue were recorded in anesthetized rats. About 90% of the taste-sensitive amygdaloid neurons responded to thermal and/or tactile stimulations of the tongue as well, and some of them showed convergent responses to tactile stimulation of various parts of the body and to acoustic stimulation. Most (86%) amygdaloid taste-sensitive neurons showed a phasic pattern of excitatory response lasting 1–2 s after onset of stimulation with the broad breadth of tuning to the four taste stimuli. About 35% of the neurons showed monotonic increasing responses with increasing NaCl concentration. The rest of the neurons showed complex intensity-response function. The amygdaloid neurons could be grouped into classes based on their best responsive stimulus, and the response profiles of those neurons showed relative regularity when the four stimuli were hedonically ordered from most to least preferred (i.e., sucrose, NaCl, HCl, quinine). Across-neuron correlations between magnitudes of responses to pairs of the four basic taste stimuli have suggested a tendency that taste information is processed in a hedonic dimension in the amygdala. The neurons in the central (Ce) nucleus showed some differential taste responses from those in other amygdaloid nuclei, i.e., about half of the Ce neurons showed tonic responses, and the across-neuron correlation coefficients in the Ce neurons were much higher than those in the non-Ce neurons.     

Difference in taste quality coding between two cortical taste areas,granular and dysgranular insular areas,in rats

Summary The responses of 84 taste neurons to stimulation of the oral cavity in rats were examined; most taste neurons were found in either a granular insular area (area GI; n = 55) or dysgranular insular area (DI; n = 25), and the others (n = 4) were in an agranular insular area (area AI). The fraction of neurons responding to only one of the four basic stimuli was significantly larger in area GI than in area DI. When neurons were classified by the stimulus which most excited the neuron among the four basic stimuli, every best-stimulus category of neurons was found in both GI and DI areas. Quinine-best and multistimulus-type neurons, whose responses to some non-best stimulus exceeded 90% of the maximum, were more numerous in the cortex than in the thalamocortical relay neurons. When responses were plotted against taste stimuli arranged in the order of sucrose, NaCl, HCl, and quinine along the abscissa (taste coordinate), response profiles of taste neurons often showed two peaks. The double-peaked type of response profiles were found in every best-stimulus category of neurons in both areas; though, a significantly large fraction of quinine-best neurons in area GI were of the double-peaked type. Some taste neurons in area GI (n = 21) and in area DI (n = 7) were inhibited by one to two taste stimuli, particularly by the stimuli present next to the best one along the taste coordinate. In correlation profiles — correlation coefficients between sucrose and NaCl and between HCl and quinine — pairs of stimuli which were located next to each other on the taste coordinate were significantly smaller in area GI than in area DI. It is thus highly probable that area GI plays an important role in fine taste discrimination and area DI in integration of taste information.     

Gustatory responses of cortical neurons in rats. I. Response characteristics

The responses of 111 cortical neurons to the four classical taste stimuli (sucrose, NaCl, HCl, and quinine HCl) applied to the anterior part of the tongue were recorded extracellularly in lightly anesthetized rats. Basic response properties of these cortical taste neurons were analyzed. The location of 88 of 111 neurons were histologically identified. They were distributed from anterodorsal to posteroventral direction in the insular cortex just dorsal to the rhinal sulcus and ventral to the somatic sensory area I. The receptive fields of 17 cortical neurons were examined. Most (94%) of the neurons had a narrow focus on the ipsilateral, contralateral, or bilateral sides of the tongue surface. Half of the foci were surrounded by a less-sensitive receptive field of relatively wide size. No apparent relationship was detected between the location of the cortical neurons and the site or extent of the receptive fields of those neurons, indicating a lack of topographical organization in the cortical gustatory area. The mean rate of the spontaneous discharges was 7.1 impulses/3 s, which is about 3 times larger than that in a first-order taste nerve (chorda tympani). The statistically significant difference of spontaneous discharges among response types of cortical neurons was observed only between the neurons responding in an excitatory manner to only one or two kinds of basic stimuli (6.2 impulses/3 s) and the neurons responding in an inhibitory manner to more than three kinds of taste stimuli (14.2 impulses/3 s). When the net responses (spontaneous rate subtracted) to each of the four tastes were compared with the spontaneous discharges in each neuron, the magnitude of spontaneous discharges was significantly negatively correlated with the net response to sucrose. This fact indicates that a neuron with a larger spontaneous discharge rate has a tendency to respond less to sucrose. Response characteristics of cortical taste neurons were quite distinct from those of the first-order taste neurons in the following respects: 1) a decrease in the average evoked discharge rate, which resulted in a small signal-to-noise ratio; 2) a tendency toward equalization of effectiveness of the four basic taste stimuli; 3) about 27% of the neurons decreased their firing rate during the first 3 s after the onset of taste stimulation; and 4) no clear initial phasic response, with a fluctuation in impulse discharges in some neurons.(ABSTRACT TRUNCATED AT 400 WORDS)     

Responses of neurons in the primate taste cortex to glutamate.

In order to investigate the neural encoding of glutamate in the primate, recordings were made from 190 taste responsive neurons in the primary taste cortex and adjoining orbitofrontal cortex taste area in macaques. Single neurons were found that were tuned to respond best to glutamate (umami taste), just as other cells were found with best responses to glucose (sweet), sodium chloride (salty), HCl (sour), and quinine HCl (bitter). Across the population of neurons, the responsiveness to glutamate was poorly correlated with the responsiveness to NaCl, so that the representation of glutamate was clearly different from that of NaCl. Further, the representation of glutamate was shown to be approximately as different from each of the other four tastants as they are from each other, as shown by multidimensional scaling and cluster analysis. Moreover, it was found that glutamate is approximately as well represented in terms of mean evoked neural activity and the number of cells with best responses to it as the other four stimuli, glucose, NaCl, HCl and quinine. It is concluded that in primate taste cortical areas, glutamate, which produces umami taste in humans, is approximately as well represented as are the tastes produced by: glucose (sweet), NaCl (salty), HCl (sour) and quinine HCl (sour).     

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.     

Gustatory responses of single neurons in the caudolateral orbitofrontal cortex of the macaque monkey

1. In recordings made from 3,120 single neurons, a secondary cortical taste area was found in the caudolateral part of the orbitofrontal cortex of the cynomolgus macaque monkey, Macaca fascicularis. The area is part of the dysgranular field of the orbitofrontal cortex and is situated anterior to the primary cortical taste areas in the frontal opercular and adjoining insular cortices. 2. The responses of 49 single neurons with gustatory responses in the caudolateral orbitofrontal taste cortex were analyzed using the taste stimuli glucose, NaCl, HCl, quinine HCl, water, and blackcurrant juice. 3. A breadth-of-tuning coefficient was calculated for each neuron. This is a metric that can range from 0.0 for a neuron that responds specifically to only one of the four basic taste stimuli to 1.0 for one that responds equally to all four stimuli. The mean coefficient for 49 cells in the caudolateral orbitofrontal cortex was 0.39. This tuning is much sharper than that of neurons in the nucleus of the solitary tract of the monkey, and sharper than that of neurons in the primary frontal opercular and insular taste cortices. 4. A cluster analysis showed that at least seven different groups of neurons were present. For each of the taste stimuli glucose, blackcurrant juice, NaCl, and water, there was one group of neurons that responded much more to that tastant than to the other tastants. The other groups of neurons responded to two or more of these tastants, such as glucose and blackcurrant juice. In this particular region neurons were not found with large responses to HCl or quinine HCl, although such neurons could be present in other parts of the orbitofrontal cortex. 5. On the basis of this and other evidence it is concluded that in the caudolateral orbitofrontal cortex there is a secondary cortical taste area in which the tuning of neurons has become finer than in early areas of taste processing, in which foods, water, and NaCl are strongly represented and where motivation dependence first becomes manifest in the taste system.     

Gustatory responses in the frontal opercular cortex of the alert cynomolgus monkey

The responses of 165 single taste neurons in the anterior operculum of the alert cynomolgus monkey were analyzed. Chemicals were deionized water, blackcurrant juice, and the four basic taste stimuli: glucose, NaCl, HCl, and quinine HCl. Taste-evoked responses could be recorded from an opercular region that measured approximately 4.0 mm in its anteroposterior extent, 2.0 mm mediolaterally, and 3.0 mm dorsoventrally. Within this area, taste-responsive neurons were sparsely distributed such that multiunit activity was rarely encountered and neuronal isolation was readily achieved. Intensity-response functions were determined for nine cells.In each case, the lowest concentration of the dynamic response range conformed well to human electrophysiological and psychophysical thresholds for the basic taste stimuli. There was some evidence of chemotopic organization. Cells that responded best to glucose tended to be distributed toward the anterior operculum, whereas most acid-sensitive neurons were located more posteriorly. The proportion of cells responding best to NaCl peaked in the middle of the area, whereas quinine sensitivity was rather evenly distributed throughout. Opercular neurons in the monkey showed moderate breadth of sensitivity compared with taste cells of other species and at other synaptic levels. A breadth-of-tuning coefficient was calculated for each neuron. This is a metric that can range from 0.0 for a cell that responds specifically to only one of the four basic stimuli to 1.0 for one that responds equally to all four stimuli. The mean coefficient for 165 cells in the operculum was 0.67 (range = 0.12-0.99). Efforts were made to determine whether neurons could be divided into a discrete number of types, as defined by their responsiveness to the stimulus array used here. It was concluded that most taste cells may be assigned to a small number of groups, each of which is statistically independent of the others, but within which the constituent neurons are not identical. An analysis of taste quality indicated that the sweet and salty stimuli evoked patterns of activity that were significantly intercorrelated. Similarly, patterns representing HCl, quinine HCl, and water were related.     

Artificial neural networks estimate the contribution of taste neurons to coding

Taste qualities are believed to be coded in the activity of populations of taste neurons. However, it is not clear whether all neurons are equally responsible for coding. To clarify the point the relative contribution of each taste neuron to coding was assessed by constructing simple three-layer neural networks with input neurons that represent cortical taste neurons of the rat. The networks were trained by the back-propagation learning algorithm to classify the neural response patterns to the basic taste stimuli (sucrose, HCl, quinine-hydrochloride, and NaCl). The networks had four output neurons representing the basic taste qualities, the values of which provide a measure for similarity of test stimuli to the basic taste stimuli. We estimated relative contributions of input neurons to the taste discrimination of the network by examining their significance S(j), which is defined as the sum of the absolute values of the connection weights from the jth input neuron to the hidden layer. When the input neurons with a smaller S(j) (e.g., 15 out of 39 input units) were "pruned" from the trained network, the ability of the network to discriminate the basic taste qualities was not greatly affected. On the other hand, the taste discrimination of the network progressively deteriorated much more rapidly with pruning of input neurons with a larger S(j). These results suggest that cortical taste neurons differentially contribute to the coding of taste qualities. Input neurons with a larger S(j) tended to be with a larger variation of neural discharge rates to the basic taste stimuli. The variation of neural discharges may be important in the coding of taste qualities.     

Coding the sweet taste in the nucleus of the solitary tract: differential roles for anterior tongue and nasoincisor duct gustatory receptors in the rat

1. A variety of chemicals that humans describe as sweet drive neurons in the nucleus of the solitary tract (NST) of the rat more vigorously when applied to the taste receptors associated with the nasoincisor ducts (NID) than when applied to taste receptors on the anterior tongue (AT). 2. The differential effects of sweet stimuli applied to the AT and NID also are evident in the set of across-neuron correlations produced by these stimuli. The psychophysical similarity among the sweet stimuli is better accounted for by responses to stimulation of the NID than by responses to stimulation of the AT (mean correlation between pairs of sweet stimuli = +0.70 for the NID, +0.44 for the AT). 3. Disaccharides or polysaccharides of glucose, i.e., maltose (0.3 M) and Polycose (0.1 M), are poor stimuli on the NID, evoking responses only 17.8 and 26.7% as great as the response elicited by sucrose (0.3 M), an optimal stimulus for this receptor subpopulation. This suggests that Polycose and maltose interact with receptor sites distinct from those with an affinity for sweet stimuli. Polycose and maltose also are ineffective stimuli on the AT, evoking responses only 11.8 and 4.9% as large as the response evoked by an optimal stimulus for this receptor subpopulation, a mixture of electrolytes (0.3 M NaCl, 0.03 M HCl, and 0.01 M quinine HCl). 4. The relative effectiveness of the sweet sugars in driving NST neurons (sucrose greater than fructose greater than glucose) correlates with their order of effectiveness in generating preference behavior in the rat.(ABSTRACT TRUNCATED AT 250 WORDS)     

Gustatory neural coding in the monkey cortex: L-amino acids.

1. Single-neuron activity in the primary gustatory cortex of the alert cynomolgus monkey (Macaca fascicularis) was analyzed in response to a range of taste stimuli. Tastants included the four prototypical stimuli (glucose, NaCl, HCl, and quinine), fruit juice, and 12 amino acids selected for their chemical characteristics, nutritional significance, and biological importance, as well as for the availability of human psychophysical data on their perceived qualities. 2. Taste-evoked responses could be recorded from a cortical area that measured 3.5 mm in its anteroposterior extent, 2.0 mm mediolaterally, and 6.0 mm dorsoventrally. Gustatory cells constituted 4.8% of the 1,129 neurons tested. Nongustatory cells gave responses associated with mouth movements (11.1%), somatosensory stimulation (3.8%), approach or anticipation of the taste stimulus (2.2%), and tongue extension (0.4%). 3. The most effective taste stimuli were those with qualities that humans describe as salty or sweet: NaCl, monosodium glutamate, glucose, proline, glycine, and fruit juice. The least effective tastants were those rated bitter or insipid: tyrosine, tryptophan, phenylalanine, and leucine. Accordingly, 79% of the gustatory neurons responded best to glucose (46%) or NaCl (33%) among the basic stimuli; only 19% responded best to quinine (13%) or HCl (6%). One cell (2%) responded exclusively to fruit juice. 4. Cortical gustatory neurons showed a moderate breadth of sensitivity, with a mean breadth of tuning coefficient of 0.71 across 54 cells. There was no evidence of chemotopic organization in the taste cortex. 5. The taste quality of each stimulus was inferred from the relative similarity of the profiles they evoked. The clearest distinction among stimuli was between those that humans characterize as sweet versus those with other qualities. Several amino acids that have dominant sweet (glycine and proline), salty (arginine and monosodium glutamate), sour (tryptophan), or bitter (phenylalanine) components to humans evoked activity profiles that were associated with those of the appropriate prototypical stimuli. Others (cysteine and lysine) were not closely related to any single prototype. 6. Conclusions based on the responses of cortical cells in the monkey are in close agreement with those that derive from human psychophysical studies of L-amino acids, reinforcing the value of this neural model for human taste perception.     

Gustatory responses in the nucleus tractus solitarius of the alert cynomolgus monkey

Multiunit and single neuron responses to taste stimuli in the nucleus tractus solitarius (NTS) of alert cynomolgus monkeys were analyzed. Intensity-response functions, including neural thresholds to glucose and quinine HCl, agreed well with psychophysical reports, implying that the cynomolgus monkey and human share the same dynamic range of sensitivity to prototypical taste stimuli. The NTS is chemotopically organized: neurons most responsive to HCl are more common in the posterior gustatory area, whereas those most responsive to glucose and NaCl are located in the anterior NTS. Responsiveness to quinine is more widely distributed but tends toward the anterior. Efforts were made to determine if neurons could be divided into a discrete number of types, as determined by their sensitivities to the prototypical stimuli. The clearest distinction was between those that did or did not respond well to HCl. Beyond this, neuronal categories were not obvious. Individual neurons were quite broadly sensitive to our stimulus array, so that, for the typical NTS cell, no one of the four prototypes evoked a majority of the discharges. This extreme breadth of tuning suggests that taste-quality information in the monkey might be incorporated in relative discharge rates across the neuron population. Correlations among patterns of activity to the four prototypical stimuli indicated that only HCl and quinine HCl have closely related taste qualities.     

Gustatory responses of neurons in the nucleus of the solitary tract of behaving rats.

1. The activity of 117 single neurons was recorded in the rostral nucleus of the solitary tract (NST) and tested with each of four standard chemical stimuli [sucrose, NaCl, citric acid, and quinine HCl (QHCl)] and distilled water in awake, behaving rats. In 101 of these neurons, at least one sapid stimulus elicited a significant taste response. The mean spontaneous rate of the taste neurons was 4.1 +/- 5.8 (SD) spike/s. The mean response magnitudes were as follows: sucrose, 10.6 +/- 11.7; NaCl, 8.6 +/- 14.6; citric acid, 6.2 +/- 7.8; and QHCl, 2.4 +/- 6.6 spikes/s. 2. On the basis of their largest response, 42 taste neurons were classified as sucrose-best, 25 as NaCl-best, 30 as citric acid-best, and 4 as QHCl-best. The mean spontaneous rates for these categories were 4.9 +/- 6.2 for sucrose-best cells, 5.8 +/- 7.4 for NaCl-best, 1.6 +/- 2.0 for citric acid-best, and 5.8 +/- 6.0 spikes/s for QHCl-best. The spontaneous rate of the citric acid-best neurons was significantly lower than that of the other categories. 3. At the standard concentrations, 45 taste cells (44.6%) responded significantly to only one of the gustatory stimuli. Of the 30 acid-best neurons, 23 (76.7%) responded only to citric acid. For sucrose-best cells, specific sensitivity was less common (18/42, 42.9%), and for NaCl-best neurons, it was relatively uncommon (3/25, 12%). One of the 4 QHCl-best neurons was specific. In a concentration series, more than one-half of the 19 specific neurons tested responded to only one chemical at any strength. 4. The mean entropy for the excitatory responses of all gustatory neurons was 0.60. Citric acid-best cells showed the least breadth of responsiveness (0.49), sucrose-best cells were somewhat broader (0.56), but NaCl-best and QHCl-best cells were considerably less selective (0.77 and 0.79, respectively). Inhibition was observed infrequently and never reached the criterion for significance. 5. In the hierarchical cluster analysis, the four largest clusters segregated neurons primarily by best-stimulus category. The major exception to this was a group of sucrose-best neurons that also responded to NaCl and were grouped with the NaCl-best neurons. In a two-dimensional space, the specific taste neurons, those that responded to only one of the four standard sapid stimuli, remained in well-separated groups. These specific groups, however, were joined in a ring-like formation by other neurons that responded to more than one of the sapid stimuli.(ABSTRACT TRUNCATED AT 400 WORDS)     

Parabrachial gustatory neural activity during licking by rats.

1. A total of 51 single neurons was recorded from the pontine parabrachial nuclei of three rats being given sapid stimuli either via intraoral infusions or during spontaneous licking behavior. In 46 neurons, sapid stimuli elicited significant taste responses; of these, 28 responded best to NaCl, 15 to sucrose, 2 to citric acid, and 1 to quinine HCl. The remaining five neurons responded significantly only to water. The mean spontaneous rate of taste neurons during the intraoral infusion and licking sessions was 11.1 +/- 1.1 and 10.8 +/- 1.2 (SE) spikes/s, respectively. 2. Of the 39 neurons tested during both licking and intraoral infusions, four responded significantly only to water via either route. The remaining 35 neurons responded significantly to at least some sapid stimuli. The best-stimulus categories remained the same regardless of the route of fluid delivery (24 NaCl best, 10 sucrose best, 1 citric acid best). When the rats were licking the stimuli, nine taste neurons responded significantly to only one sapid chemical [6 Na specific (Ns) and 3 sucrose specific (Ss)] but were more broadly tuned during intraoral infusions. Conversely, three taste neurons that responded specifically during intraoral infusions (3 Na specific) were not as specific when the animal licked the same fluids. 3. Thirty-five taste neurons were tested via both stimulus routes. These data were compared in three ways. First, for each neuron, the responses elicited during licking and intraoral infusions were compared for each of the four standard sapid stimuli. The Pearson correlation coefficients for the 35 taste neurons ranged from 0.9997 to 0.6785, with a mean at 0.953 +/- 0.012 (SE). The second comparison was between stimulus routes across chemicals. With the use of raw responses, the correlation coefficients for NaCl, sucrose, citric acid, and QHCl ranged from 0.925 to 0.778 (t test, P less than 0.0001). With the activity elicited by water subtracted (corrected responses), the correlation coefficients for NaCl, sucrose, citric acid, and QHCl were 0.900, 0.795, 0.369, and 0.211, respectively. The coefficient for QHCl was not significant (t test, P greater than 0.05). Finally, the mean responses to NaCl, sucrose, and citric acid delivered by both routes were compared and found not to differ (paired t test, P greater than 0.05). 4. In separate hierarchical cluster analyses for the licking and infusion data, the largest cluster in each contained all of the Na-best neurons and the next largest, all of the sucrose-best cells.(ABSTRACT TRUNCATED AT 400 WORDS)     

Natural groupings of primate spinothalamic neurons based on cutaneous stimulation. Physiological and anatomical features

1. Two hundred and twenty-one spinothalamic tract (STT) neurons in the lumbar spinal cord of anesthetized monkeys were studied. The majority of the recordings were in laminae IV-VI. Thirteen of these neurons were intracellularly injected with horseradish peroxidase and histologically reconstructed. 2. A standard series of four mechanical cutaneous stimuli, which ranged in intensity from innocuous brushing to tissue-damaging pinching, were used to test the mechanical responsiveness of STT neurons. The mean alterations in discharge rate produced by these test stimuli when delivered to a neuron's excitatory receptive field were used as response measures. 3. Univariate and bivariate analyses of these response measures failed to reveal natural groupings of STT neurons. To assess whether natural groupings dependent upon shared multivariate response patterns were present, a k-means cluster analysis of the responses was performed. 4. Because an assumption about the type of coding used by the STT system had to be made prior to clustering, two independent analyses were performed. One approach assumed a labeled line coding model; response magnitudes were determined within the context of the neuron under study (within-neuron analysis). The other approach assumed a population coding model; response magnitudes were determined within the context of the STT population (across-neuron analysis). 5. The within-neuron analysis suggested that the STT sample could be partitioned into four groups. The smallest group (n = 18, 8%) responded primarily to brushing but often had a convergent nociceptive input; this group was referred to as type I. A second group (n = 31, 14%) had strong responses to low-intensity stimuli, particularly pressure, and modestly larger responses to noxious stimuli; this group was referred to as type II. The clustering in these two groups was relatively weak, reflecting some heterogeneity in response pattern. 6. The largest within-neuron group (n = 108, 49%) was most responsive to noxious stimuli but had a saturating response function; because of their apparent role in coding intermediate intensity stimuli, this group was referred to as type III. The fourth group (n = 64, 29%) responded best to the most intense stimulus used; this group was referred to as type IV. 7. The across-neuron analysis also suggested that the STT sample could be partitioned into four groups. The largest group (n = 122, 55%) had relatively weak responses to all the cutaneous stimuli; this group was referred to as type A. 8. All of the remaining across-neuron groups had mean responses at or above the mean for all cutaneous stimuli.(ABSTRACT TRUNCATED AT 400 WORDS)     

Gustatory neuron types in hamster brain stem

In general, mammalian taste neurons are broadly responsive to stimuli representing different taste qualities. In the hamster, this breadth of tuning increases systematically from peripheral to successively higher brain stem neurons. Some investigators have classified taste-responsive neurons into "best-stimulus" categories on the basis of which of the four basic stimuli (sucrose, NaCl, HCl, or quinine hydrochloride) elicits the maximum response. However, attempts by others to demonstrate the existence of taste neuron types in the chorda tympani nerve and medulla of the rat using hierarchical cluster analysis have not been successful, resulting in the conclusion that there are no neuron types in the rat gustatory system. The present study was designed to look at the question of neuron types in the hamster, a species with a broader range of gustatory sensitivities to anterior tongue stimulation. Responses of 30 neurons in the nucleus tractus solitarius (NTS) and 31 neurons in the parabrachial nuclei (PbN) of the hamster to an array of 18 stimulus compounds were recorded extracellularly. The similarities of the neural response profiles of these cells at each synaptic level were compared using multivariate statistical techniques. The possiblee grouping of cells on the basis of similarities in their response functions was examined with hierarchical cluster analysis, and the relationships among these response functions were examined with multidimensional scaling. The results of the cluster analysis suggested that at both the NTS and PbN, there are three clusters of neural response profiles. These three clusters of response profiles are characterized at both synaptic levels by their predominant sensitivity to 1) sucrose and other sweet-tasting compounds, 2) sodium salts, and 3) nonsodium salts and acids. Representation of these neurons in a two-dimensional space yielded three nonoverlapping groups of cells in both the NTS and PbN, corresponding to the three groups identified by the hierarchical cluster solution. Classification of taste neurons either by their best stimulus or by other criteria has been criticized on the grounds that it may constitute an arbitrary division of a continuous population of neurons. The techniques of numerical taxonomy, which take the cells' variability into account, also result in a grouping of taste cells into classes. These taxonomic classes agree in most instances (80% in NTS and 80.6% in PbN) to a best-stimulus classification. The failure of some investigators to find types of neural response profiles in the rat gustatory system may be the result of species differences in taste sensitivity as well as differences in the statistical procedures employed.     

Gustatory responses of single neurons in the insula of the macaque monkey

1. In recordings made from 2,925 single neurons, a region of primary taste cortex was localized to the rostral and dorsal part of the insula of the cynomolgus macaque monkey, Macaca fascicularis. The area is part of the dysgranular field of the insula and is bordered laterally by the frontal opercular taste cortex. 2. The responses of 65 single neurons with gustatory responses were analyzed in awake macaques with the use of the taste stimuli glucose, NaCl, HCl, quinine HCl (QHCl), water, and black currant juice. 3. Intensity-response functions showed that the lowest concentration in the dynamic part of the range conformed well to human thresholds for the basic taste stimuli. 4. A breadth-of-tuning coefficient was calculated for each neuron. This is a metric that can range from 0.0 for a neuron that responds specifically to only one of the four basic taste stimuli to 1.0 for one that responds equally to all four stimuli. The mean coefficient for 65 cells in the taste insula was 0.56. This tuning is sharper than that of neurons in the nucleus of the solitary tract of the monkey, and similar to that of neurons in the primary frontal opercular taste cortex. 5. A cluster analysis showed that at least six different groups of neurons were present. For each of the taste stimuli, glucose, NaCl, HCl, QHCl, water, and black currant juice, there was one group of neurons that responded much more to that tastant than to the other tastants. Other subgroups of these neurons responded to two or more of these tastants, such as glucose and black currant juice, or NaCl and QHCl. 6. On the basis of this and other evidence, it is concluded that the primary insular taste cortex, in common with the primary frontal opercular taste cortex, represents a stage of information processing in the taste system of the primate at which the tuning of neurons has become sharper than that of neurons in the nucleus of the solitary tract, and is moving toward the fineness achieved in the secondary taste cortex in the caudolateral orbitofrontal taste cortex, where motivation-dependence first becomes manifest in the taste system.     

State-dependent modulation of time-varying gustatory responses

Sensory processing is modulated by attention, which is a function of network states. Here we show that changes in such states do more than a simple gating of stimuli: they actually re-arrange cortical coding space to emphasize emotional valences. We delivered taste stimuli to rats before and after a spontaneous state change ("disengagement") that is associated with a reduction in attention and a concurrent emergence of cortical mu rhythms. The percentage of cortical neurons that responded to tastes, and the average response across neurons, remained stable with disengagement, but the particulars of the responses changed drastically. The distinctiveness of sucrose and quinine-which represent the high and low ends of the palatability spectrum-increased, the distinctiveness of the two aversive tastes (quinine and citric acid) decreased, and the distinctiveness of sucrose and NaCl, which were almost identically palatable to start with, did not change. Overall, then, the changes appeared to be palatability-specific. Two additional findings were consistent with this conclusion: rats' palatability-related behavioral responses to the tastes changed in similar ways with disengagement and disengagement-related neural changes specifically appeared late in the response, when palatability-specific information emerges in cortical responses. These data suggest that neural state changes can change the content of neural codes.     

Gustatory neural coding in the monkey cortex: stimulus quality.

1. Extracellular action potentials were recorded from 50 single neurons in the insular-opercular cortex of two alert cynomolgus monkeys during gustatory stimulation of the tongue and palate. 2. Sixteen stimuli, including salts, sugars, acids, alkaloids, monosodium glutamate, and aspartame, were chosen to represent a wide range of taste qualities. Concentrations were selected to elicit a moderate gustatory response, as determined by reference to previous electrophysiological data or to the human psychophysical literature. 3. The cortical region over which taste-evoked activity could be recorded included the frontal operculum and anterior insula, an area of approximately 75 mm3. Taste-responsive cells constituted 50 (2.7%) of the 1,863 neurons tested. Nongustatory cells responded to mouth movement (20.7%), somatosensory stimulation of the tongue (9.6%), stimulus approach or anticipation (1.7%), and tongue extension (0.6%). The sensitivities of 64.6% of these cortical neurons could not be identified by our stimulation techniques. 4. Taste cells had low spontaneous activity levels (3.7 +/- 3.0 spikes/s, mean +/- SD) and showed little inhibition. They were moderately broadly tuned, with a mean entropy coefficient of 0.76 +/- 0.17. Excitatory responses were typically not robust. 5. Hierarchical cluster analysis was used to determine whether neurons could be divided into discrete types, as defined by their response profiles to the entire stimulus array. There was an apparent division of response profiles into four general categories, with primary sensitivities to sodium (n = 18), glucose (n = 15), quinine (n = 12), and acid (n = 5). However, these categories were not statistically independent. Therefore the notion of functionally distinct neuron types was not supported by an analysis of the distribution of response profiles. It was the case, however, that neurons in the sodium category could be distinguished from other neurons by their relative specificity. 6. The similarity among the taste qualities represented by this stimulus array was assessed by calculating correlations between the activity profiles they elicited from these 50 neurons. The results generally confirmed expectations derived from human psychophysical studies. In a multidimensional representation of stimulus similarity, there were groups that contained acids, sodium salts, and chemicals that humans label bitter and sweet. 7. The small proportion of insular-opercular neurons that are taste sensitive and the low discharge rates that taste stimuli are able to evoke from them suggest a wider role for this cortical area than just gustatory coding.(ABSTRACT TRUNCATED AT 400 WORDS)     

Nerve fibers sensitive to ionic taste stimuli in chorda tympani of the rat

Hypotheses about the peripheral basis for the sense of taste in mammals have been based to a considerable degree on the determined sensibilities of the nerve fibers in the chorda tympani of the rat to chemical stimulation of the anterior tongue. Yet, whether neuron types exist in this nerve, the nature of the basic mechanisms of taste reception that are tapped by this nerve and the form in which information about stimulus quality and intensity is transmitted to the central nervous system by this nerve are, at present, unresolved issues. These issues are addressed in the present study, which is a detailed analysis of the responses of rat chorda tympani nerve fibers that are sensitive to ionic stimuli; solutions applied to the anterior tongue included a range of concentrations of four chemical compounds (sucrose, sodium chloride, hydrochloric acid, and quinine hydrochloride) that represent widely different taste qualities to man or rat. Of the 44 nerve fibers sampled, 40 were stimulated most by one of the two ionic stimuli at test concentrations reported to be equally effective: 21 fibers were most responsive to 0.1 M NaCl and named N units; 19 fibers were most responsive to 0.01 M HCl and named H units. Although many N and H units responded to both HCl and NaCl, the distribution of NaCl-HCl response ratios was bimodal, indicating there are two varieties of units sensitive to ionic taste stimuli in the rat chorda tympani. Sucrose (0.5 M) affected 4 of the nerve fibers and was the most effective stimulus for 3 of them; 0.02 M quinine affected 13 of the fibers but 10 of these were H units. H units were less "specifically tuned" than N units; they were more likely to respond to several of the chemicals. Although the absolute sensitivity to NaCl in N units or to HCl in H units varied more than 10-fold, the relative effects of the four stimuli (response profiles) were generally similar for units of a given type. Exceptions occurred when H unit responses to NaCl or quinine were suppressed by prolonged effects of preceding HCl stimulation. The similarity in response profiles is reflected in high and significant correlations between responses to each pair of effective stimuli across either H or N units.(ABSTRACT TRUNCATED AT 400 WORDS)