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PubMed1990

Corticofugal influence on taste responses in the parabrachial pons of the rat.

Although the anatomy of centrifugal input to gustatory neural structures has been described, little is known of the physiological mechanisms that convey this influence or of their functional significance. As a first step in the investigation of these issues, the effect of a reversible lesion in the gustatory neocortex (GN) on the neural code for taste in the parabrachial nucleus of the pons (PbN) was studied in rats. Electrophysiological responses to taste stimuli bathed over the tongue were recorded from single units in the PbN before, after and following recovery from an infusion of procaine-HCl into the GN. Test stimuli consisted of sapid solutions of NaCl (0.1 M), HCl (0.01 M), sucrose (0.5 M), Na-saccharin (0.004 M) and quinine-HCl (0.01 M). Infusions of procaine into the GN were correlated with both specific and nonspecific effects on the responsivity to gustatory stimuli in the PbN. Specific effects included: (1) changes in the magnitude of response to some tastants, but not others, in a given PbN unit, (2) changes in the across unit patterns produced by sweet stimuli and (3) the appearance of OFF responses in a subset of PbN units. Nonspecific effects were evidenced by changes in the spontaneous rates of activity and by enhancement or suppression of responses across all the tastants tested in a subset of PbN units. Comparison of these results with reports on the effects of decerebration suggests that some of these effects may be accounted for by interruption of the descending input from the GN to the PbN. In addition, the stimulus-specific effects that were noted following procaine infusion into the GN provide support for the suggestion that the GN specifically modifies the electrophysiological patterns that are evoked by salient taste stimuli.

Animals↗
PubMed1999

Taste in the monkey cortex.

The sense of taste in humans differs substantially from that of rodents, from which a preponderance of gustatory electrophysiology derives. To establish a more appropriate neural model for human gustation, we recorded the activity of single neurons in the primary taste cortex in 11 alert cynomolgus macaques. Taste cells composed 6% of all neurons encountered. Another 24% responded during mouth and jaw movements, and 4% were sensitive to tactile stimulation of the mouth. Smaller numbers responded during olfactory or visual stimulation, or when the monkey extended his tongue. Taste cells could be divided into four statistically independent groups, corresponding to those most responsive to glucose (38%), NaCl (34%), quinine (22%), or HCI (5%). The location of a taste cell did not predict its response profile, i.e., there was no clear topographic organization of taste sensitivity. We established neural thresholds and intensity-response functions to the basic stimuli and determined that-with the exception of HCl, to which the macaque is relatively insensitive-they were similar to those reported by human subjects. We then turned to the coding of taste quality, as inferred in macaques from the patterns of neural activity elicited by each of greater than 100 stimuli. The results proved generally faithful to human reports of the perceived qualities of these same tastants. Finally, an investigation of taste mixtures revealed a degree of mixture suppression and interaction among basic qualities similar to those reported by humans. We conclude that the alert macaque offers a reliable neural model for human gustation.

Animals↗
PubMed2001

Neural networks distinguish between taste qualities based on receptor cell population responses.

Response features of taste receptor cell action potentials were examined using an artificial neural network to determine whether they contain information about taste quality. Using the loose patch technique to record from hamster taste buds in vivo we recorded population responses of single fungiform papillae to NaCl (100 mM), sucrose (200 mM) and the synthetic sweetener NC-00274-01 (NC-01) (200 microM). Features of each response describing both burst and inter-burst characteristics were then presented to an artificial neural network for pairwise classification of taste stimuli. Responses to NaCl could be distinguished from those to both NC-01 and sucrose with accuracies of up to 86%. In contrast, pairwise comparisons between sucrose and NC-01 were not successful, scoring at chance (50%). Also, comparisons between two different concentrations of NaCl, 0.01 and 0.005 M, scored at chance. Pairwise comparisons using only those features that relate to the inter-burst behavior of the response (i.e. bursting rate) did not hinder the performance of the neural network as both sweeteners versus NaCl received scores of 75--85%. Comparisons using features corresponding to each individual burst scored poorly, receiving scores only slightly above chance. We then compared the sweeteners with varying concentrations of NaCl (0.1, 0.01, 0.005 and 0.001 M) using only those features corresponding to bursting rate within a 1 s time window. The neural network was capable of distinguishing between NaCl and NC-01 at all concentrations tested; while comparisons between NaCl and sucrose received high scores at all concentrations except 0.001 M. These results show that two different taste qualities can be distinguished from each other based solely on the bursting rates of action potentials in single taste buds and that this distinction is independent of stimulation intensity down to 0.001 M NaCl. These data suggest that action potentials in taste receptor cells may play a role in taste quality coding.

Action Potentials↗
PubMed1998

Behavioral discrimination between quinine and KCl is dependent on input from the seventh cranial nerve: implications for the functional roles of the gustatory nerves in rats.

The rat glossopharyngeal nerve (GL), which innervates posterior tongue taste buds, contains several physiologically defined taste fiber types; at least one type is primarily responsive to certain alkaloids (such as quinine), and another is primarily responsive to acids and salts. In contrast, the chorda tympani (CT), which innervates anterior tongue taste buds, does not appear to contain fibers that differentially respond to quinine relative to salts and acids. It was therefore predicted that GL transection should disrupt behavioral discriminations between quinine and either acids or salts. Water-restricted rats were trained to press one of two levers if a sampled taste stimulus was quinine (0.1-1.0 mM) and the second lever if the sampled stimulus was KCl (0.1-1.0 M). Sham surgery, GL transection, and sublingual and submaxillary salivary gland extirpation were found to have no effect relative to presurgical performance. Both CT transection and combined GL and CT transection caused a substantial and approximately equal decrement in discrimination performance. Removal of the gustatory branches of the seventh cranial nerve [CT and greater superficial petrosal (GSP)] nearly eliminated the discrimination of the taste stimuli, and combined transection of the CT, GL, and GSP unequivocally reduced performance to chance levels. Although these findings were not presaged by the known electrophysiology, they nonetheless compare favorably with other studies reporting little effect of GL transection on behavioral responses to quinine. These results, in the context of other discrimination studies reported in the literature, suggest that, in rats, the neural coding of taste quality depends primarily on the input of the facial nerve.

Alkaloids↗
PubMed2004

Low-dose furosemide modulates taste responses in the nucleus of the solitary tract of the rat.

Taste-evoked neural responses in the nucleus of the solitary tract (NST) are subject to both excitatory and inhibitory modulation by physiological conditions that influence ingestion. Treatments that induce sodium appetite predominantly reduce NST gustatory responsiveness to sapid stimuli. When sodium appetite is aroused with 10 mg of the diuretic furosemide (Furo), however, NST gustatory neurons exhibit an enhanced responsiveness to NaCl. In addition to inducing a sodium appetite, 10 mg Furo supports a conditioned taste aversion (CTA). A lower, 2-mg dose of Furo induces an equivalent sodium appetite, but not a CTA. To determine whether the anomalous electrophysiological results reflected the adverse effects of the 10-mg dose, we replicated the original experiment but instead used 2 mg of Furo. In chronically prepared, lightly anesthetized rats, the responses of 49 single NST neurons to 12 taste stimuli were recorded after subcutaneous injections of either 2 mg Furo or saline. There was no effect of treatment on NST neural responses to the four standard taste stimuli. In the NaCl concentration series, however, 2 mg Furo evoked significantly higher responses to the two highest concentrations of NaCl. There was no effect of treatment in the sucrose concentration series. Thus, unlike other methods that induce a sodium appetite, Furo increases NST neural responsiveness to NaCl. At least as far as the first central relay, sodium appetite apparently does not depend on specific changes in the sensory neural code for taste.

Animals↗
PubMed1982

Coding of gustatory information in the pontine parabrachial nuclei of the rabbit: temporal patterns of neural response.

As an extension of the analysis of magnitude of response to gustatory stimuli in the parabrachial nuclei5, this study sought to determine to what extent time course of neural response coded information about taste quality. A principal components analysis and stepwise discriminant analysis were used to evaluate stimulus-related differences in time course of response. Temporal patterns of response over an 8.192 s period to the 4 basic types of taste stimuli were discriminated from one another at about twice chance level. The discrimination of different qualities of taste by time course exceeded discrimination of different intensities of the stimuli. Analysis of time course restricted to the first 2,048 s of response again revealed significant overall differentiation of the stimuli, but only NaCl and sucrose were individually discriminated. Temporally coded information about gustatory stimuli, particularly in terms of onset characteristics of response, appeared inadequate for perceptual differentiation of taste quality. Such coding might, however, complement an across-neuron spatial pattern code for taste quality in simplifying the decoding of taste input for control of reflexive responses that entail a more inclusive classification of taste stimuli.

Animals↗
PubMed1999

Neural representation of the taste of NaCl and KCl in gustatory neurons of the hamster solitary nucleus.

NaCl and KCl are monovalent salts that can be discriminated behaviorally by hamsters on the basis of their tastes. We examined the effects of the passive Na+ channel blocker amiloride on responses to both of these salts in 34 taste-responsive neurons of the nucleus of the solitary tract (NST) in the hamster. The effects of amiloride were assessed with two different, commonly employed stimulus protocols. Additionally, concentration-response functions for each salt were measured in 37 neurons. Cells were characterized by their best response to (in M) 0. 03 NaCl, 0.1 sucrose, 0.003 HCl, 0.001 quinine hydrochloride, and 0. 1 KCl. In neurons classified as NaCl-best, amiloride reversibly blocked responses to both NaCl and KCl. In neurons classified as HCl-best, amiloride had no effect on either stimulus. In sucrose-best neurons, amiloride blocked the response to NaCl but not KCl. These results support the hypothesis that both salts are transduced by at least two different receptor mechanisms. In the NST, information arising from these different inputs is maintained in discrete populations of neurons. In addition to differences in amiloride sensitivity, the cell types also differed in their responses to the salts across concentration. At midrange salt concentrations, NaCl-best neurons were far more responsive to NaCl than KCl, whereas HCl- and sucrose-best neurons responded equivalently to the two salts at all concentrations. Because NaCl- and HCl-best cells cannot by themselves distinguish NaCl from KCl, it is the relative activity across these cell types that comprises the code for taste discrimination.

Action Potentials↗
PubMedDate not supplied

Gustatory neuron types in the periphery: a functional perspective.

Robert P. Erickson's research and writings formed the intellectual backdrop and guiding force for much of the major research on sensory coding in taste. As articulated best by Erickson, consideration focused on the relative merits of labeled-line and across-fiber pattern theory. The present article focuses primarily on a review of the electrophysiological and behavioral studies on salt taste and salt taste-mediated behavior in rodents. The evidence clearly shows that the peripheral gustatory system consists of a few neuron types/groups with well-defined physiological response characteristics. Electrophysiological studies of the chorda tympani nerve define a physiological group of narrowly tuned neurons selectively responsive to NaCl stimuli. It appears that this is a sodium-sensing module that functions primarily in the detection, recognition, and ingestion of NaCl.

Animals↗
PubMed1979

Sodium deprivation alters neural responses to gustatory stimuli.

The effects of sodium deprivation for 10 d, a period sufficient to induce sodium appetite, on gustatory nerve discharges in rats were determined. Chorda tympani responses to concentration series of sodium chloride, sucrose, hydrochloric acid, and quinine hydrochloride were recorded and analyzed without the experimenter knowing the animal's deprivation condition. After deprivation, both whole nerve and single nerve fiber responses to sodium chloride were smaller; NaCl-best fibers, those more responsive to sodium chloride than to sucrose, hydrochloric acid, or quinine, were most affected. Thresholds had not changed; however, slopes of the stimulus-response functions for sodium chloride were lowered. Comparable changes in responses to the other stimuli did not occur. These results were discussed with respect to a possible relationship between changes in sodium chloride responsivity and changes in sodium intake, differences between methods of inducing sodium appetite, coding of taste quality and intensity, and mechanisms which might effect the responsivity change.

Animals↗
PubMed1981

Stochastic properties of gustatory impulse discharges in rat chorda tympani fibers.

1. The present study was intended to elucidate the role of temporal patterns of impulse discharges of the gustatory primary afferents in the coding of taste qualities by the use of simultaneous analyses of the across-neuron patterning (5) and the temporal patterning of impulses. 2. Impulse discharges of 43 rat chorda tympani fibers elicited by gustatory stimulation (0.1 M NaCl, 0.5 M sucrose, 0.01 N HCl, 0.02 M quinine hydrochloride, 0.3 M KCl, and 0.02 M saccharin sodium) were recorded. The temporal patterns of impulse discharges elicited by these stimuli were statistically analyzed both in an initial dynamic phase and a succeeding stationary phase of responses. In the dynamic phase, the time courses of firing frequency were studied; however, these were not clearly associated with the qualities of taste stimuli. In the stationary phase, the stochastic properties of impulse trains were studied regarding the impulse trains as a stochastic point process (30). In this study, interspike interval histograms (ISI histograms), joint interval histograms, serial correlograms, and autocorrelograms were computed. 3. In general, the distribution patterns of ISI histogram were not absolutely specific to the taste qualities. However, the gamma or the exponential distribution occurred most often with 0.1 M NaCl, and the bimodal or the skewed distribution was dominated with 0.5 M sucrose stimulation among the stimuli tested. The rhythmic discharges did not occur exclusively with the sweet taste stimulation, though they occurred more often with the sweet taste stimulation than with other taste stimulations. The joint interval histogram and the serial correlogram were used to examine the stochastic properties of impulse trains with particular reference to the time dependence in the impulse trains. Generally, the time dependence was not concerned with the taste qualities. 4. The chorda tympani fibers were classified into three types according to the magnitude of responses and the temporal patterns of impulse discharges. The neurons predominantly responsive to NaCl and unresponsive to sucrose were classified as type I neurons. The remaining neurons, which moderately responded to both NaCl and sucrose, were further categorized into type II neurons and type III neurons, depending on their temporal patterns of impulse discharge. The type II neurons tended to show the rhythmic or burstlike firing of impulses in response to more than one kind of taste stimuli. 5. The results showed that the taste quality was represented in the characteristic temporal patterning of impulses as well as in the across-neuron patterning of responses. The possible origin of the temporal discharge pattern and its significance in gustatory information processing were discussed on the basis of the neuron types described above.

Afferent Pathways↗
PubMed2006

Ventral pallidum firing codes hedonic reward: when a bad taste turns good.

The ventral pallidum (VP) is a key structure in brain mesocorticolimbic reward circuits that mediate "liking" reactions to sensory pleasures. Do firing patterns in VP actually code sensory pleasure? Strong evidence for hedonic coding requires showing that neural signals track positive increases in sensory pleasure or even reversals from bad to good. A useful test is the salt alliesthesia of physiological sodium depletion that makes even aversively intense NaCl taste become palatable and "liked." We compared VP neural firing activity in rats during aversive "disliking" reactions elicited by a noxiously intense NaCl taste (triple-seawater 1.5 M concentration) in normal homeostatic state versus in a physiological salt appetite state that made the same NaCl taste palatable and elicit positive "liking" reactions. We also compared firing elicited by palatable sucrose taste, which always elicited "liking" reactions in both states. A dramatic doubling in the amplitude of VP neural firing peaks to NaCl was caused by salt appetite that matched the affective switch from aversive ("disliking") to positive hedonic ("liking") reactions. By contrast, VP neural activity to "liked" sucrose taste was always high and never altered. In summary, VP firing activity selectively tracks the hedonic values of tastes, even across hedonic reversals caused by physiological changes. Our data provide the strongest evidence yet for neural hedonic coding of natural sensory pleasures and suggest, by extension, how abnormalities in VP firing patterns might contribute to clinical hedonic dysfunctions.

Animals↗
PubMed2005

Worldwide haplotype diversity and coding sequence variation at human bitter taste receptor loci.

Bitter taste perception in humans is mediated by receptors encoded by 25 genes that together comprise the TAS2R (or T2R) gene family. The ability to identify the ligand(s) for each of these receptors is dependent on understanding allelic variation in TAS2R genes, which may have a significant effect on ligand recognition. To investigate the extent of coding variation among TAS2R alleles, we performed a comprehensive evaluation of sequence and haplotype variation in the human bitter taste receptor gene repertoire. We found that these genes exhibit substantial coding sequence diversity. In a worldwide population sample of 55 individuals, we found an average of 4.2 variant amino acid positions per gene. In aggregate, the 24 genes analyzed here, along with the phenylthiocarbamide (PTC) receptor gene analyzed previously, specify 151 different protein coding haplotypes. Analyses of the ratio of synonymous and nonsynonymous nucleotide substitutions using the Ka/Ks ratio revealed an excess of amino acid substitutions relative to most other genes examined to date (Ka/Ks = 0.94). In addition, comparisons with more than 1,500 other genes revealed that levels of diversity in the TAS2R genes were significantly greater than expected (pi = 0.11%; p < 0.01), as were levels of differentiation among continental populations (FST = 0.22; p < 0.05). These diversity patterns indicate that unusually high levels of allelic variation are found within TAS2R loci and that human populations differ appreciably with respect to TAS2R allele frequencies. Diversity in the TAS2R genes may be accounted for by natural selection, which may have favored alleles responsive to toxic, bitter compounds found in plants. These findings are consistent with the view that different alleles of the TAS2R genes encode receptors that recognize different ligands, and suggest that the haplotypes we have identified will be important in studies of receptor-ligand recognition.

Alleles↗
PubMed2001

Identification of coding single-nucleotide polymorphisms in human taste receptor genes involving bitter tasting.

T2Rs comprise a G-protein-coupled receptor superfamily that contains functionally defined bitter taste receptors. Here we report the tissue expressions and coding single-nucleotide polymorphisms (cSNPs) in human T2R genes (hT2R3, hT2R4, and hT2R5) on chromosome 7q31. We first demonstrated that hT2R3, hT2R4, and hT2R5 are actually expressed in the circumvallate papillae of the human tongue by reverse transcription-polymerase chain reaction (RT-PCR). We identified six cSNPs within the T2R receptor genes. The hT2R4 and hT2R5 contained four and one cSNPs that cause missense mutations, respectively, while hT2R3 included one silent nucleotide mutation. However, we could not find any nonsense mutations that resulted in a frameshift or a premature stop codon within the open reading frames. Genotype frequencies of each cSNP were in Hardy-Weinberg equilibrium. The identification of nucleotide diversity and amino acid polymorphisms in human T2R receptors could help clarify individual differences in the acceptability and sensitivity to bitter compounds.

Base Sequence↗
PubMed1995

Pruning of rat cortical taste neurons by an artificial neural network model.

1. Taste qualities are believed to be coded in the activity of ensembles 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 needs to be assessed. 2. We constructed simple three-layer neural networks with input units representing 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 units representing the basic taste qualities, the values of which provide a measure for similarity of test stimuli (salts, tartaric acid, and umami substances) to the basic taste stimuli. 3. Trained networks discriminated the response patterns to the test stimuli in a plausible manner in light of previous physiological and psychological experiments. Profiles of output values of the networks paralleled those of across-neuron correlations with respect to the highest or second-highest values in the profiles. 4. We evaluated relative contributions of input units to the taste discrimination of the network by examining their significance Sj, which is defined as the sum of the absolute values of the connection weights from the jth input unit to the hidden layer. When the input units with weaker connection weights (e.g., 15 of 39 input units) were "pruned" from the trained network, the ability of the network to discriminate the basic taste qualities as well as other test stimuli was not greatly affected. On the other hand, the taste discrimination of the network progressively deteriorated much more rapidly with pruning of input units with stronger connection weights. 5. These results suggest that cortical taste neurons differentially contribute to the coding of taste qualities. The pruning technique may enable the evaluation of a given taste neuron in terms of its relative contribution to the coding, with Sj providing a quantitative measure for such evaluation.

Animals↗
PubMed2003

Coding of sweet, bitter, and umami tastes: different receptor cells sharing similar signaling pathways.

Mammals can taste a wide repertoire of chemosensory stimuli. Two unrelated families of receptors (T1Rs and T2Rs) mediate responses to sweet, amino acids, and bitter compounds. Here, we demonstrate that knockouts of TRPM5, a taste TRP ion channel, or PLCbeta2, a phospholipase C selectively expressed in taste tissue, abolish sweet, amino acid, and bitter taste reception, but do not impact sour or salty tastes. Therefore, despite relying on different receptors, sweet, amino acid, and bitter transduction converge on common signaling molecules. Using PLCbeta2 taste-blind animals, we then examined a fundamental question in taste perception: how taste modalities are encoded at the cellular level. Mice engineered to rescue PLCbeta2 function exclusively in bitter-receptor expressing cells respond normally to bitter tastants but do not taste sweet or amino acid stimuli. Thus, bitter is encoded independently of sweet and amino acids, and taste receptor cells are not broadly tuned across these modalities.

Action Potentials↗
PubMed2003

Recovery of amiloride-sensitive neural coding during regeneration of the gustatory nerve: behavioral-neural correlation of salt taste discrimination.

The chorda tympani (CT) nerve innervating the anterior tongue contains two types of NaCl-responsive fibers: one, the N-type, receives input from receptor cells, the NaCl responses of which are strongly inhibited by amiloride, whereas the other, the E-type, receives input from cells poorly sensitive or insensitive to amiloride. To investigate the formation of this differentially responsive neural system, we crushed the mouse CT nerve and examined the subsequent recovery of NaCl responses and amiloride sensitivity of the regenerated nerve and behavioral discrimination between NaCl and KCl. At 2 weeks after the nerve crush, no significant response of the nerve to chemical stimuli was observed. At 3 weeks, responses to salts gradually reappeared. In this period, almost all single fibers responding to NaCl were insensitive to amiloride (E-type). At 4 weeks, some of the single fibers showed amiloride sensitivity (N-type) and behavioral discrimination between NaCl and KCl reappeared. After >or=5 weeks, the number of N-type fibers had reached the control level and became approximately equal to that of E-type fibers. During the course of recovery, N-type and E-type fibers were clearly distinguishable on the basis of their amiloride sensitivities, their KCl/NaCl response ratios, and their concentration-response relationships to NaCl. These results suggest that two salt-responsive systems are independently reformed after the nerve crush. The selective synapse reformation may account for recovery of behavioral discrimination between NaCl and KCl after taste nerve crush and regeneration. It may also explain stable sensory coding for taste quality during the continuous turnover of receptor cells in the healthy animal.

Amiloride↗
PubMed1992

Information processing in mammalian gustatory systems.

The taste system has multiple functions that are carried by three cranial nerves. It is now apparent that these functions cannot be accommodated by a single coding mechanism for taste quality. A current view emphasizes the likely existence of coding channels activated by specific sets of receptors.

Animals↗