Neuronal cell types and taste quality coding

Over the past 25 years, there have been two opposing views of how taste information is represented in the activity of gustatory neurons. One view, the across-fiber pattern (AFP) theory, postulates that taste quality is represented by the pattern of activity across the afferent population. Stimuli with similar tastes produce similar patterns of activity. The other view is that activity in a few distinct neuron types codes taste quality in a "labeled-line" fashion. Neurons responding best to sucrose, for example, would represent "sweetness," and those responding best to NaCl would code "saltiness." Some of these neuron types appear to have a biological significance, such as the NaCl-best cells, which receive input about sodium stimuli exclusively from an amiloride-sensitive epithelial ion channel. However, the relatively broad tuning of these neurons makes it unlikely that they are capable of unambiguously coding information about taste quality. Rather, these neuron types play a critical role in establishing unique AFPs that distinguish among taste stimuli. The relative activity across these cell types represent taste quality, much like the patterns of activity across broadly tuned photoreceptors code information about stimulus wavelength.     

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

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

Gustatory and extragustatory functions of mammalian taste receptors

An ever increasing number of reports about taste receptors in non-gustatory tissues suggest that these molecules must have additional functions apart from taste. Of the extraoral tissues expressing taste receptors, the gastrointestinal tract received particular attention since evidence is mounting that tastants after being ingested might exert important regulatory roles in digestive and metabolic processes. At present, the G protein-coupled taste receptors for sweet, umami and bitter stimuli along with taste-related signaling molecules have been investigated in various parts of the alimentary canal. While the mechanism linking the gastrointestinal activity of sweet compounds via the activation of sweet taste receptors to metabolic adjustments has been worked out in some detail, other taste receptor mediated gastrointestinal activities are less well understood. The present article summarizes current knowledge on mammalian G protein-coupled taste receptors as well as various aspects of their proposed role in gastrointestinal tissues.     

NMDA and non-NMDA receptors mediate taste afferent inputs to cortical taste neurons in rats

Two main subclasses of ionotropic receptors for excitatory amino acids (EAAs), N-methyl-d-aspartate (NMDA) receptors and non-NMDA receptors, are involved in neurotransmission in the cortex of mammals. To examine whether EAAs are transmitters at the cortical taste area (CTA) in rats and to elucidate which types of the two ionotropic receptors operate at these synapses, we studied the effects of microiontophoretic administration of EAA antagonists on the responses of 64 taste cortical neurons to four basic taste stimuli in urethane-anesthetized rats. Both d-2-amino-5-phosphonovalerate (APV), a selective antagonist for NMDA receptors, and 6-cyano-7-nitro-quinoxaline-2,3-dione (CNQX), a selective antagonist for non-NMDA receptors, suppressed most of the taste responses. The percentage of neurons suppressed by APV (70.3%) was almost the same as that suppressed by CNQX (64.1%). These suppressive effects were independent of the effects of background discharges during the prestimulus, water-rinsing period. The percentage of neurons suppressed by the antagonists did not differ between any pairs of taste stimuli. The number of neurons possessing both receptors was larger in the granular insular area (area GI), one of the two CTAs, than in the dysgranular insular area (area DI). In addition, taste responses were suppressed by CNQX or by both APV and CNQX in area GI in a significantly larger number of layer V neurons than in area DI. The present results indicate that normal excitatory transmission of taste afferents in the CTA in rats was mediated by both NMDA and non-NMDA receptors. The finding that a large fraction of neurons in the CTA in rats mediated taste information through NMDA receptors in normal transmission might be related to the higher potency of the plasticity observed in the CTA.     

Unilateral nasal obstruction alters sweet taste preference and sweet taste receptors in rat circumvallate papillae

Nasal obstruction causes mouth breathing, and affects the growth and development of craniofacial structures, muscle function in the stomatognathic system, and the taste perceptive system. However, the detailed mechanism underlying the effects of nasal obstruction on taste perception has not been fully elucidated. In this study, we investigated this mechanism using the two-bottle taste preference test, immunohistological analysis, and quantification of the mRNA expression of taste-related molecules in the circumvallate papillae. Neonatal male Wistar rats were divided randomly into control and experimental groups. Rats in the experimental group underwent unilateral nasal obstruction by cauterization of the external nostril at the age of 8 days. Arterial oxygen saturation (SpO₂) was recorded in awake rats using collar clip sensors. Taste preference for five basic taste solutions was evaluated. Immunohistochemical analysis and quantitative real-time polymerase chain reaction (RT-PCR) were conducted to evaluate the expressions of taste-related molecules in the taste cells of the circumvallate papillae. Body weights were similar between the two groups throughout the experimental period. The SpO₂ in the 7- to 12-week-old rats in the experimental group was significantly lower than that in the age-matched rats in the control group. In the two-bottle taste preference test, the sensitivities to sweet taste decreased in the experimental group. The mRNA expression of T1R2, T1R3, α-gustducin, and PLCβ2 was significantly lower in the experimental group than in the control group as determined by quantitative RT-PCR, and the immunohistochemical staining for α-gustducin and PLCβ2 was less prominent. These findings suggest that nasal obstruction may affect sweet taste perception via the reduced expression of taste-related molecules in the taste cells in rat circumvallate papillae.     

Interactions between taste receptors in the frog tongue

Summary Receptors sensitive to stimulation with dilute CaCl₂ solutions and located in different fungiform papillae of the frog tongue are cross-connected via branches of the glossopharyngeal nerve fibers to form chemical sensory units comprising on average about 3 papillae; often one or more papillae were found to be common to different units.The receptor response observed when single papillae were individually stimulated increased, when the strength of the stimulus was raised, at a much lower rate than that obtained by stimulating the whole tongue surface. This proves that the antidromic impulses travelling in the cross-connections linking different papillae result in an evident depression of the receptor response to CaCl₂.The possible functional significance of mutual interaction between the receptors in the frog tongue is discussed.This study was supported by grants from the Consiglio Nazionale delle Ricerche (Impresa di Elettrofisiologia) of Rome, Italy.     

Relationship among reproductive variables,sucrose taste reactivity and feeding behavior in humans

Magnitude-estimation of sucrose pleasantness and sweetness, and feeding behavior, were investigated in female and male college students. The subjects were individually tested five times over a five-week period. Female test intervals were scheduled to include the menses, pre-ovulatory, and luteal phases of the menstrual cycle. The data were analyzed by gender, length of menses, and phase of the menstrual cycle. The results of these analyses were consistent for both the sucrose taste reactivity tests and feeding tests. Male and long-menses females exhibited similar response patterns; and their pattern was significantly different from that of the short-menses females. The mean log pleasantness ratings of the males and long-menses females were significantly smaller than those of the short-menses females. Furthermore, both long-menses females and males behaved similarly in a time-limited surreptitious feeding test. They consumed significantly more food than did short-menses females. Phase of the menstrual cycle did not alter pleasantness response patterns, but there was one phase effect in the feeding tests. Luteal phase intake of short-menses females was elevated relative to that of the menses phase. These findings demonstrate that reproductive variables participate in the control of human regulatory behaviors.     

Modification of the gerbil's taste behavior by the sucrose taste antagonist p-nitrophenyl alpha-D-glucopyranoside

Since the gerbil's chorda tympani nerve response to sucrose is antagonized by p-nitrophenyl alpha-D-glucopyransoide (PNP-Glu), the present taste aversion behavioral experiments sought to determine whether the gerbil's behavioral gustatory responses could be modified by adding PNP-Glu to taste solutions. Results demonstrated that the gerbil's aversion to sucrose was affected by the addition of PNP-Glu, but that the avoidance was overcome by the addition of high enough concentrations of the antagonist. When mixtures of sucrose and quinine were tested, the gerbil's sucrose aversion was unaffected, nor was any change noted in the taste behavior of gerbils trained to avoid 0.1 M sodium chloride after the addition of PNP-Glu.     

From synapse to behavior: rapid modulation of defined neuronal types with engineered GABAA receptors

In mammals, identifying the contribution of specific neurons or networks to behavior is a key challenge. Here we describe an approach that facilitates this process by enabling the rapid modulation of synaptic inhibition in defined cell populations. Binding of zolpidem, a systemically active allosteric modulator that enhances the function of the GABAA receptor, requires a phenylalanine residue (Phe77) in the gamma2 subunit. Mice in which this residue is changed to isoleucine are insensitive to zolpidem. By Cre recombinase-induced swapping of the gamma2 subunit (that is, exchanging Ile77 for Phe77), zolpidem sensitivity can be restored to GABAA receptors in chosen cell types. We demonstrate the power of this method in the cerebellum, where zolpidem rapidly induces significant motor deficits when Purkinje cells are made uniquely sensitive to its action. This combined molecular and pharmacological technique has demonstrable advantages over targeted cell ablation and will be invaluable for investigating many neuronal circuits.     

Role of catecholamines in efferent regulation of taste receptors

The action of efferent stimulation on unit activity of the taste receptors of the frog tongue was studied. A deficiency of catecholamines following reserpine administration or perfusion of the lingual vessels with adrenoblocking agents (inderal, dibenamine) prevents centrifugal inhibition, whereas perfusion with an adrenomimetic (adrenalin) potentiates this effect. These effects of adrenergic substances were also observed in animals after bilateral extirpation of the first ganglion of the sympathetic chain. It is concluded that catecholamines present in the papillae are essential for central inhibitory effects on activity of the taste receptor apparatus.Laboratory of Experimental and Clinical Physiology of Sense Organs, Institute of Normal and Pathological Physiology, Academy of Medical Sciences of the USSR, Moscow. (Presented by Academician of the Academy of Medical Sciences of the USSR A. M. Chernukh.) Translated from Byulleten' Éksperimental'noi Biologii i Meditsiny, Vol. 79, No. 5, pp. 8–11, May, 1975.     

Preference behavior and taste nerve responses in D-penicillamine treated rats

Preferences for NaCl, sucrose, HCl and quinine were examined in rats fed a diet containing D-penicillamine (D-pen), and compared with those of normal control rats. Preferences for NaCl and sucrose were reduced by administration of D-pen, and returned to normal upon cessation of D-pen administration. Change in preferences for NaCl and sucrose depended on the amount as well as the duration of D-pen administration. Preferences for HCl and quinine were unaffected by D-pen. No significant difference in the threshold and magnitude of the chorda tympani nerve responses to the taste stimuli was found between D-pen treated and normal rats. Concentrations of electrolytes in serum and saliva were scarcely changed by D-pen administration, but the amount of serum copper was markedly reduced. Effect of D-pen on sensitivity of taste receptors and role of copper ions in regulating fluid intake are discussed.     

Immunohistochemical detection of neurotrophin-3 and -4, and their receptors in mouse taste bud cells

Neurotrophin-3 (NT3) and neurotrophin-4 (NT4) affect the survival and maintenance of central and peripheral neurons. Using an immunohistochemical method, we examined whether the taste bud cells in the circumvallate papillae of normal mice expressed NT3, NT4, and their respective receptors TrkC and TrkB, and if so, what type of cells in the taste buds expressed them. Double immunostaining for either of them and PGP 9.5, NCAM, or gustducin was used to determine which cell types expressed which neurotrophins and receptors. Normal taste bud cells expressed NT3, NT4, and the TrkB receptor, but not TrkC. The percentage of NT3-immunoreactive cells among all taste bud cells was 89.0%, that of NT4-immunoreactive cells, 58.6%, and that of TrkB-immunoreactive cells, 80.8%. Almost none of the NT4-immunoreactive cells were reactive with anti-PGP 9.5 or the anti-NCAM antibody, but they could be stained with anti-gustducin, revealing that NT4-immunoreactive cells were contained only in the type-II--and possibly type-I--cell population. On the other hand, NT3-, and TrkB-immunoreactive cells included type-III cells, together with type-II, -I, and basal cells, because they were positive for PGP 9.5 and gustducin. We conclude that NT4 may exert trophic actions on all types of taste bud cells by binding to their TrkB receptors, and NT3 may also have a similar, though negligible role.     

The range of taste quality of sodium salts

Thirteen sodium salts as well as sucrose (sweet), citric acid, (sour), and quinine HCl (bitter) standards were arranged in a three-dimensional space by the multidimensional scaling procedure, ALSCAL. The arrangements for salts equated in perceived intensity to 0.15 M NaCl, as well as salts presented at 0.2 M Na⁺, regardless of perceived intensities, revealed that the anion contributes significantly to the overall taste quality of sodium salts. The arrangements were quite stable over the 12 subjects tested. In addition, the anion can reduce the salty aspects of the sensation of sodium salts. The taste range of sodium salts equated for temperature, texture, and viscosity extends beyond the closed system defined by the four so-called primary tastes: salty, sweet, sour, and bitter.     

Reflex reaction of the taste receptors of the tongue to direct stimulation of thegastric receptors

Summary In man, signals from the gastric receptors acting through the central nervous system play an important part in regulating the reaction of the gustatory receptor apparatus. A considerable reduction in the sensitivity of taste receptors tested on the tongue was caused by food introduced directly into the stomach through a fistula, so that to by-pass them.Presented by Active Member AMN SSSR V. V. Parin Translated from Byulleten' Éksperimental'noi Biologii i Meditsiny, Vol. 53, No. 1, pp. 12–14, January, 1962