Temperature modulates taste responsiveness and stimulates gustatory neurons in the rat geniculate ganglion

In humans, temperature influences taste intensity and quality perception, and thermal stimulation itself may elicit taste sensations. However, peripheral coding mechanisms of taste have generally been examined independently of the influence of temperature. In anesthetized rats, we characterized the single-cell responses of geniculate ganglion neurons to 0.5 M sucrose, 0.1 M NaCl, 0.01 M citric acid, and 0.02 M quinine hydrochloride at a steady, baseline temperature (adapted) of 10, 25, and 40 degrees C; gradual cooling and warming (1 degrees C/s change in water temperature >5 s) from an adapted tongue temperature of 25 degrees C; gradual cooling from an adapted temperature of 40 degrees C; and gradual warming from an adapted temperature of 10 degrees C. Hierarchical cluster analysis of the taste responses at 25 degrees C divided 50 neurons into two major categories of narrowly tuned (Sucrose-specialists, NaCl-specialists) and broadly tuned (NaCl-generalists(I), NaCl- generalists(II), Acid-generalists, and QHCl-generalists) groups. NaCl specialists were excited by cooling from 25 to 10 degrees C and inhibited by warming from 10 to 25 degrees C. Acid-generalists were excited by cooling from 40 to 25 degrees C but not from 25 to 10 degrees C. In general, the taste responses of broadly tuned neurons decreased systematically to all stimuli with decreasing adapted temperatures. The response selectivity of Sucrose-specialists for sucrose and NaCl-specialists for NaCl was unaffected by adapted temperature. However, Sucrose-specialists were unresponsive to sucrose at 10 degrees C, whereas NaCl-specialists responded equally to NaCl at all adapted temperatures. In conclusion, we have shown that temperature modulates taste responsiveness and is itself a stimulus for activation in specific types of peripheral gustatory neurons.     

Development of taste responses in rat nucleus of solitary tract

Extracellular responses from neurons in the nucleus of the solitary tract (NST) were studied in rats aged 5 days to adulthood during chemical stimulation of the tongue with monochloride salts, citric and hydrochloric acids, sucrose, sodium saccharin, and quinine hydrochloride. Multiunit taste responses were recorded in rats at 5-7 days of age and single-unit responses were recorded from 111 neurons in four other age groups of 14-20 days, 25-35 days, 50-60 days, and adult. NST neurons in rats aged 5-7 days consistently responded to relatively high concentrations (0.5 M) of NH4Cl and KCl and to citric and hydrochloric acid. However, they often did not respond to 0.5 M NaCl or to 0.1 M NH4Cl. Single NST neurons in rats aged 14 days and older characteristically responded to all 0.1 and 0.5 M salts and to both acids. At least 75% of neurons also responded to sucrose and sodium saccharin, and 46% responded to all of these stimuli and quinine hydrochloride. After 14 days, no developmental changes occurred in the number of stimuli to which neurons responded. There were substantial developmental alterations in the response magnitudes to some chemical stimuli. Average response frequencies increased after 35 days of age for 0.1 and 0.5 M NaCl, LiCl, KCl, and for sucrose and sodium saccharin. Response frequencies for NH4Cl, citric and hydrochloric acid, and quinine hydrochloride, however, did not change throughout development. The proportion of single NST neurons that responded maximally to specific monochloride salts did not change during development. Most single neurons in all age groups responded equally well to NH4Cl, NaCl, and LiCl. No NST neuron responded maximally to KCl. There were also no developmental differences in response latencies in rats aged 14 days and older. Response frequencies of second-order NST neurons generally reflect changes in responses from the primary afferent, chorda tympani fibers, throughout development; however, the increases in salt response frequencies from NST neurons occur comparatively later in development. Furthermore, at all ages, the taste responses to monochloride salts include higher response frequencies and a general loss in response specificity in NST compared to chorda tympani neurons.(ABSTRACT TRUNCATED AT 400 WORDS)     

Anion size modulates salt taste in rats

The purpose of this study was to investigate the influence of anion size and the contribution of the epithelial sodium channel (ENaC) and the transient receptor potential vanilloid-1 (TRPV1) channel on sodium-taste responses in rat chorda tympani (CT) neurons. We recorded multiunit responses from the severed CT nerve and single-cell responses from intact, narrowly tuned and broadly tuned, salt-sensitive neurons in the geniculate ganglion simultaneously with stimulus-evoked summated potentials to signal when the stimulus contacted the lingual epithelium. Artificial saliva served as the rinse and solvent for all stimuli (0.3 M NH(4)Cl, 0.5 M sucrose, 0.03-0.5 M NaCl, 0.01 M citric acid, 0.02 M quinine hydrochloride, 0.1 M KCl, and 0.03-0.5 M Na-gluconate). We used the pharmacological antagonist benzamil to assess NaCl responses mediated by ENaC, and SB-366791 and cetylpyridinium chloride to assess responses mediated by TRPV1. CT nerve responses were greater to NaCl than Na-gluconate at each concentration; this was attributed mostly to broadly tuned, acid-generalist neurons that responded with higher frequency and shorter latency to NaCl than Na-gluconate. In contrast, narrowly tuned NaCl-specialist neurons responded more similarly to the two salts, but with subtle differences in temporal pattern. Benzamil reduced CT nerve and single-cell responses only of narrowly tuned neurons to NaCl. Surprisingly, SB-366791 and cetylpyridinium chloride were without effect on CT nerve or single-cell NaCl responses. Collectively, our data demonstrate the critical role that apical ENaCs in fungiform papillae play in processing information about sodium by peripheral gustatory neurons; the role of TRPV1 channels is an enigma.     

Development of taste responses in the rat parabrachial nucleus

Extracellular responses from neurons in the parabrachial nuclei (PBN) were studied in rats 4 days old to adulthood during chemical stimulation of the tongue with monochloride salts, citric and hydrochloric acids, sucrose, sodium saccharin, and quinine hydrochloride. Multiunit taste responses were recorded in rats at 4-7 days of age and single-unit responses were recorded from 121 neurons in four other age groups of 14-20 days, 25-35 days, 50-60 days, and adults. PBN neurons in rats 4-7 days old consistently responded to 0.1 M solutions of NH4Cl and NaCl, to 0.5 M solutions of NH4Cl, NaCl, and KCl, and to 1.0 M sucrose, 0.1 M sodium saccharin, 0.1 M citric acid, and 0.1 N HCl. They often did not respond, however, to 0.1 M KCl and 0.01 M quinine hydrochloride. Single PBN neurons in rats 14 days old and older characteristically responded to all stimuli, which consisted of 0.1 and 0.5 M salts, acids, sucrose, sodium saccharin, and quinine hydrochloride. Thus no developmental differences occurred in the number of stimuli to which neurons responded after rats were 14 days old. With the exception of responses to hydrochloric acid, there were significant increases in response frequencies to all stimuli after 14 days of age. Average response frequencies to NH4Cl and citric acid increased after 20 days of age and those to NaCl, LiCl, KCl, sucrose, sodium saccharin, and quinine hydrochloride increased after 35 days of age. Average response frequencies for hydrochloric acid did not alter after 14 days of age. The proportion of single PBN neurons that responded maximally to specific monochloride salts did not change during development. Most single neurons in all age groups responded equally well to NH4Cl, NaCl, and LiCl. No PBN neuron responded maximally to KCl. Developmental differences in response frequencies of third-order gustatory neurons in the PBN generally reflect developmental response changes in first-order neurons of the chorda tympani nerve and second-order neurons of the solitary nucleus. However, unique developmental changes are evident in the PBN. Thus the ontogenetic changes that occur in PBN responses likely relate to modifications of lower-order peripheral and central nervous system afferents and peripheral receptor sensitivities.     

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)     

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.     

Taste-responsive neurons of the glossopharyngeal nerve of the rat

1. Taste sensibilities of neurons in mammalian glossopharyngeal nerves have been inadequately studied, although they innervate the majority of taste buds and may provide unique taste information. 2. Extracellular responses of glossopharyngeal neural units to taste stimuli infused into foliate or vallate papillae were recorded in anesthetized rats. A 0.3-ml/min infusion of stimuli into papillae resulted in short-latency, 5-s nerve-impulse rates that approached 10 times the response rates observed using less invasive means of stimulation. 3. Sucrose, Na saccharin, NaCl, NH4Cl, KCl, HCl, citric acid, acetic acid, MgSO4, and quinine.HCl were effective stimuli for glossopharyngeal neurons at concentrations that have behavioral significance. 4. Response spectra for individual neural units with either foliate or vallate receptive fields fell into three clusters. Forty-six percent were A units that responded most strongly to acids and chloride salts, NH4Cl being the most effective; neither quinine nor sucrose was effective. Twenty-three percent were S units that responded to sugars and saccharin; quinine, salts, and acids were not effective. Thirty-one percent were Q units that responded to quinine; neither NaCl, HCl, nor sucrose was effective stimulus for these fragile units. 5. Glossopharyngeal A neural units were more sensitive to 1 mM HCl than were electrolyte-sensitive H units of the chorda tympani, although both respond generally to salts and acids. Units relatively specific for sodium salts (N units), which are common in the chorda tympani nerve, were not found in the glossopharyngeal nerve, which explains losses in sodium-specific behavior after cutting only the chorda tympani nerve. 6. Q units were the only glossopharyngeal neural units that responded significantly to quinine, and units with similar response spectra do not occur in the chorda tympani nerve. Q units probably mediate aversive reflexes to quinine that are eliminated by cutting only the glossopharyngeal nerve. Glossopharyngeal S neural units were more sensitive to sucrose and are more common than their counterparts in the chorda tympani, although it is not known how they might compare with sugar-sensitive units in the greater superficial petrosal nerve. 7. These data strongly suggest that posterior taste bud fields innervated by the glossopharyngeal nerve are specialized for functions different from those of anterior taste bud fields innervated by the facial nerve.     

Taste quality and intensity: lessons from the Morrison technique

The nontoxic and nonshock Morrison operant technique was used to evaluate taste quality in rat and marmoset: response to a tastant test solution in pursuit of a pellet reward was dependent on making a choice between two bars that had been linked in discrimination training to qualitatively different stimulus pairs (NaCl versus either HCl, QHCl, or NH(4)Cl). The percentage distribution of bar-press responses to test stimuli showed: (1) stability of quality across 0.069-0.3 M NaCl, 0.003-0.1 M HCl, and 0.0001-0.003 M QHCl; (2) for LiCl, a quality change consistent with human reports of a "sour" to "salty" shift; (3) a suggestion that the "salty-like" quality of NH(4)Cl and NaCl are not perceptually equivalent; (4) NaNO(3) shares NaCl-like, QHCl-like, and NH(4)Cl-like components; (5) CaCl(2), KCl, and MgCl(2) share QHCl-like and NH(4)Cl-like components; and (6) responses to HCl and QHCl were not hedonically driven in the rat. Comparison of rank order correlations of single-unit firing rates to the distribution of bar-press responses for the same test stimulus concentration revealed that (7) no single level of the gustatory pathway exclusively accounts for the operant response distribution pattern to either simple or complex tastants, and (8) discriminations between tastants, one of which may be qualitatively complex, are not necessarily mediated only at levels proximal to the solitary nucleus. Thus, the Morrison discrimination technique effectively yields statements about gustatory quality without use of negative reinforcers and largely uninfluenced by tastant hedonics.     

Neural representation of bitter taste in the nucleus of the solitary tract

Based on the molecular findings that many bitter taste receptors (T2Rs) are expressed within the same receptor cells, it has been proposed that bitter taste is encoded by the activation of discrete neural elements. Here we examined how a variety of bitter stimuli are represented by neural activity in central gustatory neurons. Taste responses (spikes/s) evoked by bathing the tongue and palate with intensity-matched concentrations (in M) of 2 sugars (0.32 sucrose and 0.5 D-fructose), ethanol (40%), 4 salts (0.01 NaCl, 0.008 NaNO(3), 0.01 MgCl(2), and 0.05 KCl), 2 acids (0.003 HCl and 0.005 citric acid), and 10 bitter ligands (0.007 quinine-HCl, 0.015 denatonium benzoate, 0.003 l-cysteine, 0.001 nicotine, 0.005 strychnine-HCl, 0.04 tetraethylammonium chloride, 0.03 atropine-SO(4), 0.005 brucine-SO(4), 0.03 papaverine-HCl, and 0.009 sparteine) were recorded from 51 neurons in the nucleus of the solitary tract of anesthetized rats. Cluster analysis was used to categorize neurons into types based on responses to sucrose, NaCl, HCl, and quinine-HCl. Three groupings emerged: type S (responded optimally to sweets), type N (sodium-optimal), and type H/Q (responded robustly to bitters, acids, and salts). Multivariate analyses revealed that across-neuron patterns of response among bitter stimuli were strongly correlated. However, neural type H/Q, which was most responsive to bitter tastants, was not differentially sensitive to bitter stimuli and Na(+) salts, which rats perceive as distinct. Thus central neurons most responsive to bitter substances receive significant input from receptors that mediate other tastes, indicating that bitter stimuli are not represented by activity in specifically tuned neurons.     

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.     

Organization of gustatory sensitivities in hamster superior laryngeal nerve fibers

1. Mammalian taste receptors are distributed within several distinct subpopulations, innervated by branches of cranial nerves VII, IX, and X. Most gustatory electrophysiology has focused on input from the fungiform papillae on the anterior portion of the tongue, carried by the chorda tympani branch of the VIIth nerve. However, laryngeal taste buds in the hamster are as numerous as those in the fungiform papillae. Gustatory fibers in the hamster's chorda tympani and glossopharyngeal nerves have been well characterized. In comparison with these taste fibers, much less is known about the chemical sensitivities of fibers innervating laryngeal taste buds. 2. Action potentials were recorded from 65 individual fibers in the superior laryngeal nerve (SLN) of the hamster. Stimuli were distilled H2O and five concentrations each of sucrose, NaCl, HCl, and quinine hydrochloride (QHCl). All stimuli except the NaCl series were made in physiological saline (0.154 M NaCl) and were delivered from the laryngeal side of the epiglottis via a tracheal cannula. Responses were quantified as the number of impulses in 10 s minus the responses in the preceding 10 s of baseline activity during a rinse with physiological saline. 3. Distilled H2O, HCl, and NaCl were by far the most excitatory stimuli, with mean responses across all cells 5-10 times greater than those evoked by sucrose or QHCl. The order of effectiveness of the strongest concentrations of the stimuli was H2O greater than 0.03 M HCl greater than 1.0 M NaCl much greater than 0.03 M QHCl greater than 1.0 M sucrose. 4. The mean concentration-response function for NaCl was U shaped, with the greatest number of impulses to distilled H2O and 1.0 M NaCl. The responses diminished as the concentrations approached physiological levels (0.154 M NaCl), where there was no response, and increased as NaCl concentration rose above this level. Increasing concentrations of HCl above 0.0003 M elicited increasing responses in these fibers. 5. The mean time course of the responses to distilled H2O and to hypotonic NaCl solutions (0.01 and 0.03 M) peaked in the first few seconds and then declined slowly. This was distinct from the time course of the responses to hypertonic NaCl concentrations (0.3 and 1.0 M), which increased gradually throughout the 10-s response period. Responses to HCl peaked in the initial second and then decayed rapidly to a slowly declining plateau. These distinctively different time courses suggest different receptor mechanisms for water, salt, and acid stimuli. 6. The across-fiber pattern of the responses to hypotonic NaCl solutions correlated strongly to that elicited by distilled H2O.(ABSTRACT TRUNCATED AT 400 WORDS)     

Responses from parabrachial gustatory neurons in behaving rats

1. The responses of a total of 70 single neurons were recorded from the parabrachial nuclei (PBN) in awake rats. In 59 neurons, sapid stimuli (0.5 ml) elicited significant taste responses. Of these 59 neurons, 10 also had significant responses to water. The mean spontaneous rate of the taste neurons was 13.4 +/- 6.9 (SD) spikes/s. Of the remaining 11 neurons, 9 responded significantly only to water; 2 had no significant responses to the standard fluid stimuli. 2. Based on the magnitude of their response to our four standard stimuli, the taste neurons were classified as follows: 42 NaCl-best, 14 sucrose-best, 2 citric acid-best, and 1 QHCl-best. Of these, 25 responded only to one of four sapid stimuli; 20 of these specific cells responded only to NaCl. All the remaining 34 neurons responded to two or more of the four sapid stimuli, with NaCl and sucrose responsiveness dominant. For the 59 taste neurons, the mean entropy for the absolute value of the responses was 0.68; for the excitatory activity alone, it was 0.58. 3. The mean responses to NaCl and sucrose concentration series increased monotonically. Except at the lowest concentration, responses to citric acid also increased monotonically, but with a lower slope. Mean responses to QHCl, however, remained stable or even decreased with increasing concentration. Thus the power functions for the NaCl and sucrose intensity-response series were higher than those of citric acid and QHCl. 4. A hierarchical cluster analysis of 59 parabrachial neurons suggested four different categories: NaCl-best, sucrose-best, citric acid-best, and QHCl-best. These categories were less evident in the two-dimensional space produced by multidimensional analysis, because the positions of NaCl- and sucrose-best neurons formed a continuum in which neural response profiles change successively from sucrose-specific to NaCl-specific. 5. The results were consistent with previous anatomic and neurophysiological data suggesting convergence in the medulla of sensory input from receptors in the nasoincisor ducts (NID) and on the anterior tongue (AT). Taste buds in the NID respond preferentially to sucrose, whereas those on the AT respond more to NaCl.(ABSTRACT TRUNCATED AT 400 WORDS)     

The role of transient receptor potential vanilloid-1 on neural responses to acids by the chorda tympani,glossopharyngeal and superior laryngeal nerves in mice

The transient receptor potential vanilloid-1 (TRPV1) receptor acts as a polymodal nociceptor activated by capsaicin, heat, and acid. TRPV1, which is expressed in sensory neurons innervating the oral cavity, is associated with an oral burning sensation in response to spicy food containing capsaicin. However, little is known about the involvement of TRPV1 in responses to acid stimuli in either the gustatory system or the general somatosensory innervation of the oropharynx. To test this possibility, we recorded electrophysiological responses to several acids (acetic acid, citric acid and HCl) and other taste stimuli from the mouse chorda tympani, glossopharyngeal and superior laryngeal nerves, and compared potential effects of iodo-resiniferatoxin (I-RTX), a potent TRPV1 antagonist, on chemical responses of the three nerves. The results indicated that in the chorda tympani nerve, I-RTX (1–100 nM) did not affect responses to acids, sucrose and quinine HCl, but reduced responses to NaCl (I-RTX at concentrations of 10 and 100 nM) and KCl and NH₄Cl (100 nM). In contrast, in the glossopharyngeal nerve, I-RTX significantly suppressed responses to all acids and salts, but not to sucrose and quinine HCl. Responses to acetic acid were suppressed by I-RTX even at 0.1 nM concentration. The superior laryngeal nerve responded in a concentration-dependent manner to acetic acid, citric acid, HCl, KCl, NH₄Cl and monosodium l-glutamate. The responses to acetic acid, but not to the other stimuli, were significantly inhibited by I-RTX. These results suggested that TRPV1 may be involved in the mechanism for responses to acids presented to the posterior oral cavity and larynx. This high degree of responsiveness to acetic acid may account for the oral burning sensation, known as a flavor characteristic of vinegar.     

Effect of nicotine on chorda tympani responses to salty and sour stimuli

The effect of nicotine on the benzamil (Bz)-insensitive (transient receptor potential vanilloid-1 variant cation channel, TRPV1t) and the Bz-sensitive (epithelial Na(+) channel, ENaC) salt taste receptors and sour taste was investigated by monitoring intracellular Na(+) and H(+) activity (pH(i)) in polarized fungiform taste receptor cells (TRCs) and the chorda tympani (CT) nerve responses to NaCl, KCl, and HCl. CT responses in Sprague-Dawley rats and both wildtype and TRPV1 knockout (KO) mice were recorded in the presence and absence of agonists [resiniferatoxin (RTX) and elevated temperature] and an antagonist (SB-366791) of TRPV1t, the ENaC blocker (Bz), and varying apical pH (pH(o)). At concentrations <0.015 M, nicotine enhanced and at >0.015 M, it inhibited CT responses to KCl and NaCl. Nicotine produced maximum enhancement in the Bz-insensitive NaCl CT response at pH(o) between 6 and 7. RTX and elevated temperature increased the sensitivity of the CT response to nicotine in salt-containing media, and SB-366791 inhibited these effects. TRPV1 KO mice demonstrated no Bz-insensitive CT response to NaCl and no sensitivity to nicotine, RTX, and elevated temperature. We conclude that nicotine modulates salt responses by direct interaction with TRPV1t. At pH(o) >8, the apical membrane permeability of nicotine was increased significantly, resulting in increase in TRC pH(i) and volume, activation of ENaC, and enhancement of the Bz-sensitive NaCl CT response. At pH(o) >8, nicotine also inhibited the phasic component of the HCl CT response. We conclude that the effects of nicotine on ENaC and the phasic HCl CT response arise from increases in TRC pH(i) and volume.     

Central gustatory lesions: I. Preference and taste reactivity tests.

Bilateral electrophysiologically guided lesions were placed in the nucleus of the solitary tract (NST), the parabrachial nucleus (PBN), and the ventral posteromedial thalamic nucleus (VPMpc) of rats, and 15-min intake and taste reactivity (TR) responses elicited by 3 concentrations each of sucrose, NaCl, HCl, and quinine (Q) HCl were subsequently measured. Compared with controls, NST lesions had no significant effects on intake, and rats with PBN lesions consumed significantly more QHCl, sucrose, NaCl, and HCl. Thalamic lesions decreased sucrose intake. Analysis of TR responses showed that the QHCl threshold for aversive responses increased after VPMpc, PBN, and NST lesions. Rats with NST or PBN lesions were unresponsive to increasing sucrose concentration. TR responses elicited by NaCl and HCl were similar across the groups.     

Gastric modulation of gustatory afferent activity

The neural activity evoked by stimulation of the rat's tongue with NaCl, sucrose, HCl, and QHCl was recorded from 25 small populations of second-order gustatory neurons in the nucleus of the solitary tract, both before and after gastric loading. A slowly developing (several minutes) load-induced depression in the response evoked by the taste solutions was noted, with no significant differences seen between loading with air or 0.3 M NaCl. Differences were evident in the magnitude of the decrement for the various stimuli; the order of decrement was sucrose > NaCl > HCl; the response to QHCl showed no clear decrement. The effect of gastric loading, as tested with air loads, is reversible. The magnitude of the load effect was seen to be less with greater levels of food deprivation. The results of this study therefore, demonstrate the existence of gastric effects on the reactivity of second-order gustatory afferents to chemical stimulation of the rat's tongue.     

Operant licking in rabbits for intraoral injection of basic types of tastants

In order to compare and contrast hedonic properties of 0.75 M NaCl and 0.5 M sucrose used in behavioral electrophysiology of taste, tests were carried out of evoked patterns of orolingual response and operant licking on a FR-32 schedule to discrete intraoral injections of these stimuli and other basic types of tastants. In tests of taste reactivity, NaCl and sucrose evoked quantitatively similar numbers of orolingual response in excess of those evoked by water. NaCl was also similar to sucrose in amount of operant licking generated at the outset of the test session. Both of these stimuli were more effective than either 0.02 M HCl, 0.01 M QHCl, or water. The NaCl also did not have the suppressant effect of HCl when alternated with sucrose as the reinforcement for licking. NaCl differed from sucrose in sustaining operant licking. While NaCl would appear to share the same basic hedonic value of sucrose, long-term associative processes pertaining to postingestional consequences of fluid input and short-term sensory processes may act to limit behavioral responsivity for concentrated NaCl. Additional information was obtained on operant licking for sodium saccharin.     

Perceptual characteristics of the amiloride-suppressed sodium chloride taste response in the rat

The contribution of amiloride-sensitive membrane components to the perception of NaCl taste was assessed by using a conditioned taste aversion procedure. Eight independent groups of adult rats were conditioned to avoid either 0.1M NaCl, 0.5M NaCl; 0.1M NH4Cl, or 1.0M sucrose while their tongues were exposed either to water or to the sodium transport blocker amiloride hydrochloride. In contrast to rats exposed to water during conditioning, rats exposed to amiloride were unable to acquire a conditioned taste aversion to 0.1M NaCl. Differences in the acquisition of taste aversions between the amiloride- and nonamiloride-treated groups were not apparent when the conditioned stimulus (CS) was 0.5M NaCl, 0.1M NH4Cl, or 1.0M sucrose. Although the magnitude of the 0.5M NaCl aversion was similar between amiloride- and non-amiloride-treated rats, the perceptual characteristics of the CS differed between groups. Analyses of stimulus generalization gradients revealed that amiloride-treated rats generally avoided all monochloride salts after conditioning to 0.5M NaCl but not nonsodium salts or nonsalt stimuli. In contrast, rats not treated with amiloride only generalized the 0.5M NaCl aversion to sodium salts. No differences in generalization gradients occurred between groups when the CS was 0.1M NH4Cl or 1.0M sucrose. These findings suggest that the "salty" taste of NaCl is primarily related to the amiloride-sensitive portion of the functional taste response in rats. Conversely, the portion of the NaCl response insensitive to amiloride appears to have "sour-salty" perceptual characteristics and does not appear to be perceived as being salty.     

Pontine gustatory activity is altered by electrical stimulation in the central nucleus of the amygdala

Visceral signals and experience modulate the responses of brain stem neurons to gustatory stimuli. Both behavioral and anatomical evidence suggests that this modulation may involve descending input from the forebrain. The present study investigates the centrifugal control of gustatory neural activity in the parabrachial nucleus (PBN). Extracellular responses were recorded from 51 single PBN neurons during application of sucrose, NaCl, NaCl mixed with amiloride, citric acid, and QHCl with or without concurrent electrical stimulation in the ipsilateral central nucleus of the amygdala (CeA). Based on the sapid stimulus that evoked the greatest discharge, 3 neurons were classified as sucrose-best, 32 as NaCl-best, and 16 as citric acid-best. In most of the neurons sampled, response rates to an effective stimulus were either inhibited or unchanged during electrical stimulation of the CeA. Stimulation in the CeA was without effect in two sucrose-best neurons, nine NaCl-best neurons, and one citric acid-best neuron. Suppression was evident in 1 sucrose-best neuron, 18 NaCl-best neurons, and 15 citric acid-best neurons. In NaCl-best neurons inhibited by CeA stimulation, the magnitude of the effect was similar for spontaneous activity and responses to the five taste stimuli. Nonetheless, the inhibitory modulation of gustatory sensitivity increased the relative effectiveness of NaCl resulting in narrower chemical selectivity. For citric acid-best neurons, the magnitude of inhibition produced by CeA activation increased with an increase in stimulus effectiveness. The responses to citric acid were inhibited significantly more than the responses to all other stimuli with the exception of NaCl mixed with amiloride. The overall effect was to change these CA-best neurons to CA/NaCl-best neurons. In a smaller subset of NaCl-best neurons (n = 5), CeA stimulation augmented the responsiveness to NaCl but was without effect on the other stimuli or on baseline activity. It appears that electrical stimulation in the CeA modulates response intensity, as well as the type of gustatory information that is transmitted in a subset of NaCl-best neurons. These findings provide an additional link between the amygdala and the PBN in the control of NaCl intake, modulating the response and the chemical selectivity of an amiloride-sensitive Na+ detecting input pathway.     

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)