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)     

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)     

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.     

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.     

Gustatory neuron types in rat geniculate ganglion

We used extracellular single-cell recording procedures to characterize the chemical and thermal sensitivity of the rat geniculate ganglion to lingual stimulation, and to examine the effects of specific ion transport antagonists on salt transduction mechanisms. Hierarchical cluster analysis of the responses from 73 single neurons to 3 salts (0.075 and 0.3 M NaCl, KCl, and NH(4) Cl), 0.5 M sucrose, 0.01 M HCl, and 0.02 M quinine HCl (QHCl) indicated 3 main groups that responded best to either sucrose, HCl, or NaCl. Eight narrowly tuned neurons were deemed sucrose-specialists and 33 broadly tuned neurons as HCl-generalists. The NaCl group contained three identifiable subclusters: 18 NaCl-specialists, 11 NaCl-generalists, and 3 QHCl-generalists. Sucrose- and NaCl-specialists responded specifically to sucrose and NaCl, respectively. All generalist neurons responded to salt, acid, and alkaloid stimuli to varying degree and order depending on neuron type. Response order was NaCl > HCl = QHCl > sucrose in NaCl-generalists, HCl > NaCl > QHCl > sucrose in HCl-generalists, and QHCl = NaCl = HCl > sucrose in QHCl-generalists. NaCl-specialists responded robustly to low and high NaCl concentrations, but weakly, if at all, to high KCl and NH(4) Cl concentrations after prolonged stimulation. HCl-generalist neurons responded to all three salts, but at twice the rate to NH(4) Cl than to NaCl and KCl. NaCl- and QHCl-generalists responded equally to the three salts. Amiloride and 5-(N,N-dimethyl)-amiloride (DMA), antagonists of Na(+) channels and Na(+)/H(+) exchangers, respectively, inhibited the responses to 0.075 M NaCl only in NaCl-specialist neurons. The K(+) channel antagonist, 4-aminopyridine (4-AP), was without a suppressive effect on salt responses, but, when applied alone in solution, it evoked a response in many HCl-generalists and one QHCl-generalist neuron so tested. Of the 39 neurons tested for their sensitivity to temperature, 23 responded to cooling and chemical stimulation, and 20 of these neurons were HCl-generalists. Moreover, the responses to the four standard stimuli were reduced progressively at lower temperatures in HCl- and QHCl-generalist neurons, but not in NaCl-specialists. Thus sodium channels and Na(+)/H(+) exchangers appear to be expressed exclusively on the membranes of receptor cells that synapse with NaCl-specialist neurons. In addition, cooling sensitivity and taste-temperature interactions appear to be prominent features of broadly tuned neuron groups, particularly HCl-generalists. Taken all together, it appears that lingual taste cells make specific connections with afferent fibers that allow gustatory stimuli to be parceled into different input pathways. In general, these neurons are organized physiologically into specialist and generalist types. The sucrose- and NaCl-specialists alone can provide sufficient information to distinguish sucrose and NaCl from other stimuli, respectively.     

Parabrachial gustatory neural responses to monosodium glutamate ingested by awake rats.

A sample of 41 gustatory neurons isolated in the parabrachial nuclei of awake, behaving rats was tested with sapid solutions of 0.1 M monosodium glutamate (MSG), 0.5 mM of guanosine 5'-monophosphate (GMP), and a mixture of MSG and GMP as well as with 0.3 M sucrose, 0.1 M NaCl, 0.01 M citric acid, and 0.0001 M QHCl. Interneuronal correlation coefficients and factor analysis indicated that both the sodium cation and glutamic anion contributed to the activity elicited by MSG. Guanosine potentiated the responses to MSG, but only in neurons that also responded to sucrose. These results suggest that the gustatory contribution to the flavor denoted by the Japanese word "umami" may be mediated, in part, by neurons that also respond to chemical described by humans as sweet.     

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)     

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.     

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)     

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.     

Modulation of parabrachial taste neurons by electrical and chemical stimulation of the lateral hypothalamus and amygdala

The lateral hypothalamus (LH) and the central nucleus of the amygdala (CeA) exert an influence on ingestive behavior and are reciprocally connected to gustatory and viscerosensory areas, including the nucleus of the solitary tract (NST) and the parabrachial nuclei (PbN). We investigated the effects of LH and CeA stimulation on the activity of 101 taste-responsive neurons in the hamster PbN. Eighty three of these neurons were antidromically activated by stimulation of these sites; 57 were antidromically driven by both. Of these 83 neurons, 21 were also orthodromically activated--8 by the CeA and 3 by the LH. Additional neurons were excited (n = 5) or inhibited (n = 8) by these forebrain nuclei but not antidromically activated. Taste stimuli were: 0.032 M sucrose, 0.032 M sodium chloride (NaCl), 0.032 M quinine hydrochloride (QHCl), and 0.0032 M citric acid. Among the 34 orthodromically activated neurons, more sucrose-best neurons were excited than inhibited, whereas the opposite occurred for citric-acid- and QHCl-best cells. Neurons inhibited by the forebrain responded significantly more strongly to citric acid and QHCl than cells excited by these sites. The effects of electrical stimulation were mimicked by microinjection of DL-homocysteic acid, indicating that cells at these forebrain sites were responsible for these effects. These data demonstrate that many individual PbN gustatory neurons project to both the LH and CeA and that these areas modulate the gustatory activity of a subset of PbN neurons. This neural substrate is likely involved in the modulation of taste activity by physiological and experiential factors.     

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.     

Intake inhibition by NPY: role of appetitive ingestive behavior and aversion

Intraventricular infusion of neuropeptide Y (NPY) decreases the amount female rats ingest during intraoral infusion (consummatory behavior) of a 1-M solution of sucrose at a rate of 0.5 ml/min and simultaneously increases the number of times the rats visit a bottle filled with sucrose (appetitive behavior). In this study, we investigated if the suppression of consummatory behavior was dependent upon the increase of appetitive behavior. The shift from consummatory to appetitive ingestive behavior was attenuated by adding 3-mM quinine HCl (QHCl) to the sucrose solution in the bottle. However, the intraoral intake of the sucrose solution was still decreased in NPY-treated rats. NPY did not modify taste reactivity as measured by aversive responses during continuous intraoral infusion of sucrose or ingestive and aversive responses to brief intraoral infusion of sucrose (0, 0.3 or 1 M) or QHCl (0, 0.3 or 3 mM). NPY stimulated visits to a bottle and intake from the bottle and inhibited sexual behavior in male rats but had no effect on the sexual behavior in the absence of a bottle. The visits and the intake were suppressed, but sexual behavior was not activated by adding QHCl (3 mM) to the solution in the bottle. Obstructing appetitive ingestive behavior, therefore, does not indiscriminately facilitate consummatory behavior. Male rats showed aversive or ingestive behavior and sexual behavior simultaneously during intraoral infusion of QHCl or condensed milk. It is suggested that NPY decreases intraoral intake and increases appetitive ingestive behavior via partially separable mechanisms that are independent of taste aversion.     

Intraoral intake and taste reactivity responses elicited by sucrose and sodium chloride in chronic decerebrate rats

The oral stimulating effects of sucrose and sodium chloride (NaCl) were assessed in chronic decerebrate and pair-fed intact control rats by measuring both oral motor taste-reactivity responses and intraoral intake volume. Taste-reactivity responses were videotaped during the first minute of the intraoral taste infusion. The infusion continued until the taste solution was rejected from the mouth, and the intake volume was computed accordingly. The number of ingestive taste-reactivity responses and the volume of intraoral intake consumed by pair-fed control and decerebrate rats increased with increasing sucrose concentration. Sucrose intake increased as concentration increased to 0.1 M, then plateaued between 0.3, 1.3, and 2.0 M sucrose for both groups. For control rats, intraoral NaCl elicited an inverted U-shaped function for both taste-reactivity responses and intake. Taste-reactivity responses of chronic decerebrate rats varied with NaCl concentration. In contrast to control rats, intake of NaCl did not differ from that of water for decerebrate rats. These data indicate that caudal brain-stem mechanisms are sufficient to control sucrose intake but are not adequate for the concentration dependent intake of NaCl. Second, these data also indicate that it is possible for taste-elicited oral motor responses to be dissociated from intake. The different roles of taste and postingestive factors in sucrose and NaCl intake are discussed.     

Gustatory neural responses to umami stimuli in the parabrachial nucleus of C57BL/6J mice

Umami is considered to be the fifth basic taste quality and is elicited by glutamate. The mouse is an ideal rodent model for the study of this taste quality because of evidence that suggests that this species, like humans, may sense umami-tasting compounds as unique from other basic taste qualities. We performed single-unit recording of taste responses in the parabrachial nucleus (PbN) of anesthetized C57BL/6J mice to investigate the central representation of umami taste. A total of 52 taste-responsive neurons (22 sucrose-best, 19 NaCl-best, 5 citric acid-best, and 6 quinine-best) were recorded from stimulation period with a large panel of basic and umami-tasting stimuli. No neuron responded best to monopotassium glutamate (MPG) or inosine 5'-monophosphate (IMP), suggesting convergence of input in the central nervous system. Synergism induced by an MPG-IMP mixture was observed in all sucrose-best and some NaCl-best neurons that possessed strong sensitivity to sucrose. In more than half of sucrose-best neurons, the MPG-IMP mixture evoked stronger responses than those elicited by their best stimulus. Furthermore, hierarchical cluster analysis and multidimensional analysis indicated close similarity between sucrose and the MPG-IMP mixture. These results strongly suggest the mixture tastes sweet to mice, a conclusion consistent with previous findings that show bidirectional generalization of conditioned taste aversion between sucrose and umami mixtures, and suppression of taste responses to both sucrose and mixtures by the antisweet polypeptide gurmarin in the chorda tympani nerve. The distribution pattern of reconstructed recording sites of specific neuron types suggested chemotopic organization in the PbN.     

Aversive behavior during intraoral intake in male rats

We investigated if the taste of a sucrose solution becomes progressively more aversive during intraoral infusion and if this contributes to the termination of the intake in male rats. The display of aversive behavior, such as gapes and chin rubs, but not headshakes, forelimb flails or orofacial grooming, varied with the concentration of an intraorally infused solution of quinine hydrochloride (QHCl) and increased by the time the rat rejected an intraorally infused 2 M solution of sucrose. Activation of gapes and chin rubs by brief intraoral infusion of QHCl advanced the rejection of the sucrose solution if given late during intraoral infusion, but blockade of gaping by anaesthesization of the oral cavity with Xylocain did not prolong the intake of the sucrose solution. Headshakes and forelimb flails could be elicited by stimulating the head and limbs with sucrose, and gapes and chin rubs were activated by infusion of a 2 M solution of sucrose into the stomach or duodenum but not by infusion of glucose into the jugular or hepatic portal vein. Preventing filling of the gastrointestinal tract during intraoral infusion of sucrose (sham feeding) eliminated the display of gapes and chin rubs. It is suggested that an increase in the aversiveness of the taste of a sucrose solution contributes to the rejection of that solution during intraoral infusion. However, rats can reject a sucrose solution in the absence of any behavioral sign of aversion and none of the so-called "taste-related" aversive behaviors is exclusively dependent upon stimulation of the taste receptors in the oral cavity.     

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.     

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.     

Responses to taste stimulation in the ventroposteromedial nucleus of the thalamus in rats

Extracellular action potentials were recorded from 73 neurons in the parvicellular division of the ventroposteromedial (VPMpc) nucleus of the thalamus of anesthetized Wistar rats during gustatory, thermal, and tactile stimulation of the whole oral cavity. The stimulus array consisted of 16 room-temperature (23 degrees C) sapid stimuli, distilled water at three temperatures (0, 23, and 37 degrees C), and 0.1 M NaCl at three temperatures (0, 23, and 37 degrees C). Among all 151 neurons isolated in VPMpc, 9% responded exclusively to taste, 33% to taste and temperature, none to taste and touch, but 6% to all three modalities. Discharge rates evoked by the basic tastants were 13.8 +/- 1.6 (SD) spikes/s for 0.1 M NaCl, 9.3 +/- 1.4 spikes/s for 0.01 M HCl, 5.1 +/- 0.9 spikes/s for 0.5 M sucrose, and 4.3 +/- 0.6 spikes/s for 0.01 M quinine HCl. Water evoked mean responses at 0, 23, and 37 degrees C of 9.9 +/- 1.5, 0.6 +/- 0.4, and 1.3 +/- 0.9 spikes/s, respectively. The mean firing rate evoked by 37 and 0 degrees C NaCl was 15.0 +/- 2.4 and 17.0 +/- 2.8 spikes/s, respectively. The exponent of the NaCl concentration-response power function was 0.39. Thalamic taste cells were broadly tuned. The mean breadth-of-tuning coefficient for these 73 gustatory cells was 0.79 +/- 0.02. Two cells responded predominantly with inhibition, which accounted for the majority of inhibitory responses. The taste neurons were statistically divisible into three groups: sodium-oriented (n = 40), acid-oriented (n = 12), and sugar-oriented (n = 17). Four additional bitter-oriented neurons were not closely enough related to be defined as a group and were considered outliers. The sodium-oriented group could be divided into three statistically distinct subgroups, differing in the specificity of their responses to NaCl. With respect to polymodal sensitivity, spontaneous rate, evoked response rates, signal-to-noise ratio, proportions of cells responding best to basic tastants, taste neuron groups, taste spaces, and temporal responses, VPMpc neurons have characteristics that are intermediate between those of parabrachial and cortical gustatory neurons.     

Taste reactivity in the hamster

Taste reactivity, which was first described in the rat, consists of ingestive and aversive response components, the latter seen mostly to bitter-tasting stimuli. The present experiment characterized the hamster's taste reactivity to an array of stimuli (sugars: 1 M sucrose, d-fructose and d-glucose; sodium salts: 1 M NaCl, Na2SO4 and NaNO3; acids: 30 mM HCl, tartaric acid and citric acid; bitter-tasting stimuli: 100 mM quinine hydrochloride and nicotine sulfate and 10 mM denatonium benzoate). These 12 stimuli were chosen to represent 3 examples each of stimuli that taste sweet, salty, sour, or bitter to humans; they were presented in random order via an intraoral fistula, one stimulus each day per animal (n = 10). Infusions of 0.6 ml were delivered over a 1-min period from a syringe pump. Orofacial and somatic motor responses were recorded on videotape for later analysis and were also coded online into a computer. Ingestive responses included forward and lateral tongue protrusions and aversive responses included gaping, chin rubbing, forelimb flailing, fluid rejection, increased locomotion, and aversive posturing. Each stimulus group produced a characteristic pattern of these behaviors, with sugars eliciting only ingestive behaviors and the bitter stimuli evoking predominantly aversive responses. Both sodium salts and acids produced ingestive responses, as seen previously in the rat, although these stimuli also elicited aversive behaviors in the hamster, including apes. The patterns of responses were characterized using multivariate procedures; the stimuli fell into distinct groups that were separated primarily along an hedonic dimension.