Temperature dependence of human taste responses

Human taste thresholds for NaCl, HCl, Dulcin and QSO₄ were determined at 17, 22, 27, 32, 37, and 42°C using the psychophysical method of forced choice. The thresholds for all four compounds were lowest between 22° and 32° and rose above and below this temperature range. The results favored a physical-chemical basis for the transduction process over an enzymatic explanation. The effect of temperature on the intensity of suprathreshold solutions of QHCl was tested by varying the adapting and stimulus temperatures of solutions presented to one side of the tongue in a matching procedure with a standard on the other side. The temperature effect was found to be independent of the adapting temperature and the standard concentration, and to depend only on the stimulus temperature.     

Behavioral and neural responses to gustatory stimuli delivered non-contingently through intra-oral cannulas

The act of eating requires a decision by an animal to place food in its mouth. The reasons to eat are varied and include hunger as well as the food's expected reward value. Previous studies of tastant processing in the rat primary gustatory cortex (GC) have used either anesthetized or awake behaving preparations that yield somewhat different results. Here we have developed a new preparation in which we explore the influences of intra-oral and non-contingent tastant delivery on rats' behavior and on their GC neural responses. We recorded single-unit activity in the rat GC during two sequences of tastant deliveries, PRE and POST, which were separated by a waiting period. Six tastants ranging in hedonic value from sucrose to quinine were delivered in the first two protocols called 4TW and L-S. In the third one, the App L-S protocol, only hedonically positive tastants were used. In the 4TW protocol, tastants were delivered in blocks whereas in the two L-S protocols tastants were randomly interleaved. In the 4TW and L-S protocols the probability of ingesting tastants in the PRE sequence decreased exponentially with the trial number. Moreover, in both protocols this decrease was greater in the POST than in the PRE sequence likely because the subjects learned that unpleasant tastants were to be delivered. In the App L-S protocol the decrease in ingestion was markedly slower than in the other protocols, thus supporting the hypothesis that the decrease in appetitive behavior arises from the non-contingent intra-oral delivery of hedonically negative tastants like quinine. Although neuronal responses in the three protocols displayed similar variability levels, significant differences existed between the protocols in the way the variability was partitioned between chemosensory and non-chemosensory neurons. While in the 4TW and L-S protocols the former population displayed more changes than the latter, in the App L-S protocol variability was homogeneously distributed between the two populations. We posit that these tuning changes arise, at least in part, from compounds released upon ingestion, and also from differences in areas of the oral cavity that are bathed as the animals ingest or reject the tastants.     

Ingestion affected by the oral environment: the role of gustatory adaptation on taste reactivity in the rat

Three experiments were performed to determine (1) the time course of changes in ingestive behavior associated with oral infusion of taste substances, and (2) the possible role of changes in the tonic chorda tympani response in the behavioral effect of oral infusion. Experiments 1 and 2 examined 2 different procedures with a variety of sapid solutions to detect alterations in ingestion following oral adaptation. Decrements in Na-saccharin licking were found over a 2-hr period of continuous Na-saccharin stimulation suggesting that gustatory adaptation in the rat extends over a considerable time period and that the effect of the infusion was to alter the incentive motivation properties of the sapid substance. Experiment 3 sought an altered tonic responsivity of the chorda tympani nerve which might correlate with the decrement in ingestion seen in Experiment 2. No evidence of a neural decrement over a 2-hr time was found and it was concluded that central processes were probably involved in the behavioral adaptation found in the second experiment.     

Responsiveness of dog thalamic neurons to taste stimulation of various tongue regions

Receptive fields of single thalamic taste neurons in dogs were studied by examining responses to stimuli representing the four basic taste qualities applied to five different regions on the tongue surface. Twenty single thalamic units responded to taste stimulation of the tongue ipsilateral to the recording site were classified into three types according to characteristics of their receptive fields. In 11 out of 20 units, the location and the size of the receptive field and the most sensitive region in the receptive field did not vary among their effective taste stimuli (type A units). In 5 units, the location and the size of the receptive field varied with taste stimulus, although the most sensitive region was common to the stimuli (type B units). In the remaining 4 units, the most sensitive region varied with taste stimulus (type C units).     

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.     

Behavioral and neural gustatory responses in rabbit

To provide more information on a potentially valuable preparation for studies in taste and appetite, we have examined the taste preferences (and aversions) and chorda tympani sensitivity of the rabbit. Adult male New Zealand rabbits were given a two-bottle preference test between water and various molar concentrations of NaCl, KCl, sucrose, sodium saccharin, quinine hydrochloride and HCl. The rabbits exhibited the expected preferences for sucrose and aversions for quinine and HCl. Unexpectedly, however, the rabbits exhibited only a mild preference for NaCl, a stronger preference for KCl, and an aversion to sodium saccharin. Multiunit discharges of the chorda tympani nerve to the same taste stimuli indicated that the anterior tongue receptors are acutely sensitive to KCl, NaCl and quinine, but not to sucrose, HCl and saccharin. The chorda tympani was more responsive to KCl than to NaCl. Dilute concentrations of both NaCl and sodium saccharin elicited a two-component response consisting of an immediate excitatory phase followed by a tonic inhibitory phase. This complex response pattern of the whole nerve to NaCl and sodium saccharin is discussed in relation to the impulse frequencies in hypothesized water-sensitive and salt-sensitive fibers. Both the behavioral and neural data are discussed in relation to similar data obtained in rat and hamster.     

The cathodal OFF response of electric taste in rats

Summary The cathodal OFF response in electric taste, the production of a taste sensation at the break of a microampere cathodal current passed through the tongue, was studied electrophysiologically in the rat chorda tympani nerve. Previous work in electric taste has centered on ON responses to both anodal and cathodal currents. The cathodal OFF response, like ON responses, increased with increasing current intensity until a saturated response level was achieved. Unlike previously reported ON responses, the OFF response did not show a sensitivity to the ionic composition of the fluid bathing the tongue making this the first electrophysiological report of ion insensitivity in electric taste. The cathodal OFF response was sensitive to the duration of the current pulse preceding it. Longer pulses produced larger OFF responses, until with very long pulses (seconds) a saturated response level was achieved. The half maximal response occurred at 12.5 ms. These results have been interpreted to mean that the cathodal OFF response has an origin other than the microvillus membrane, the site most often implied for ON responses, due largely to its ion insensitivity. A probable location may reside with ion channels transversing the basal membrane which are transiently excited at the break of the current resulting in excitation at the receptor-afferent synapse.     

Dietary sodium deprivation reduces gustatory neural responses of the parabrachial nucleus in rats

Acute sodium depletion induced by furosemide reduces gustatory responses of parabrachial nucleus (PBN) neurons to 0.3-0.5M NaCl in rats. However, in the rat nucleus of the solitary tract (NST), where taste-responsive cells project to the PBN, acute sodium depletion and dietary sodium deprivation elicit different response profiles to lingual NaCl stimulation. To examine the effect of dietary sodium deprivation on the responses of PBN gustatory neurons, we observed the taste responses of the PBN neurons to the four taste qualities and serial concentrations of NaCl in 15-day dietary sodium-deprived and control rats. The results showed that sodium deprivation reduced the responses of PBN taste neurons to 0.1-1.0M NaCl, but not to other tastants. Based on the analyses classified by best-stimulus categories, the number of NaCl-best neurons decreased from 68% to 45% following dietary sodium deprivation, and the responses of the NaCl-best neurons to 0.03-1.0M NaCl were significantly inhibited. Multidimensional scaling illustrated that sodium deprivation increased the similarity of the response profiles of the NaCl-best neurons. These findings suggest that dietary sodium deprivation might modulate sodium intake via increasing aversive threshold for salt rather enhancing salt discrimination.     

Receptive field properties of thalamo-cortical taste relay neurons in the parvicellular part of the posteromedial ventral nucleus in rats

Summary Twenty-five taste and 35 mechanoreceptive neurons were recorded from the parvicellular part of the posteromedial ventral nucleus (VPMpc) in rats. Among them, 14 (56%) of the taste and 7 (18.4%) of the mechanoreceptive neurons were antidromically activated from the cortical taste area (CTA) with a latency of 1–4 ms and identified as thalamocortical (TC) relay neurons. No significant differences were evident in the receptive field properties or in the location in the VPMpc between the TC and non-TC neuron groups. Two classes of TC neurons were recognized: one class consisted of neurons which were most excited by NaCl among the four basic taste stimuli with receptive fields (RFs) confined to a part of the oral cavity, e.g. the anterior tongue, and the other class contained neurons which were most excited by sucrose or HCl, with RFs over a wide area of the oral cavity. Both the TC and non-TC neurons showed similar effects of CTA stimulation: post-stimulus time histograms revealed a long lasting inhibition followed by a rebound facilitation of spontaneous discharge.     

The neuropeptides CCK and NPY and the changing view of cell-to-cell communication in the taste bud

The evolving view of the taste bud increasingly suggests that it operates as a complex signal processing unit. A number of neurotransmitters and neuropeptides and their corresponding receptors are now known to be expressed in subsets of taste receptor cells in the mammalian bud. These expression patterns set up hard-wired cell-to-cell communication pathways whose exact physiological roles still remain obscure. As occurs in other cellular systems, it is likely that neuropeptides are co-expressed with neurotransmitters and function as neuromodulators. Several neuropeptides have been identified in taste receptor cells including cholecystokinin (CCK), neuropeptide Y (NPY), vasoactive intestinal peptide (VIP), and glucagon-like peptide 1 (GLP-1). Of these, CCK and NPY are the best studied. These two peptides are co-expressed in the same presynaptic cells; however, their postsynaptic actions are both divergent and antagonistic. CCK and its receptor, the CCK-1 subtype, are expressed in the same subset of taste receptor cells and the autocrine activation of these cells produces a number of excitatory physiological actions. Further, most of these cells are responsive to bitter stimuli. On the other hand, NPY and its receptor, the NPY-1 subtype, are expressed in different cells. NPY, acting in a paracrine fashion on NPY-1 receptors, results in inhibitory actions on the cell. Preliminary evidence suggests the NPY-1 receptor expressing cell co-expresses T1R3, a member of the T1R family of G-protein coupled receptors thought to be important in detection of sweet and umami stimuli. Thus the neuropeptide expressing cells co-express CCK, NPY, and CCK-1 receptor. Neuropeptides released from these cells during bitter stimulation may work in concert to both modulate the excitation of bitter-sensitive taste receptor cells while concurrently inhibiting sweet-sensitive cells. This modulatory process is similar to the phenomenon of lateral inhibition that occurs in other sensory systems.     

Neural and behavioral responses to taste stimuli in the mouse

Neural responses to lingual stimulations with varying kinds of chemicals were recorded from the chorda tympani nerve of the ddy mouse and preferences for NaCl, sucrose and Na saccharin were measured using the two bottle-choice technique. Sucrose, Na saccharin, HCl, and quinine produced large neural responses compared with that for NaCl. Divalent salts also elicited larger responses than NaCl response. The effectiveness of cations was in the order of $\text{Sr>Mg=Ca>Li?Na?NH}{}_4\text{>K}$. Neural response magnitudes for Na salts with varying anions decrease with the relative hydrated size of anions. Mice highly preferred sucrose and Na saccharin but showed a poor preference for NaCl. Similarity in the gustatory responses between mice and hamsters as well as macaque monkeys, and difference between mice and rats are pointed out.     

Adrenalectomy reduces peripheral neural responses to gustatory stimuli in the rat

In the rat, sodium need leads to an increase in sodium intake, which depends on salt taste sensitivity. The adrenalectomized rat, because of excessive body sodium loss, has been an important animal model for studying the physiological mechanisms underlying salt ingestion. In order to investigate the mediation by peripheral taste responsivity of changes in salt intake, multiunit responses of the chorda tympani nerve to various concentrations of sodium chloride, potassium chloride, lithium chloride, hydrochloric acid, and quinine hydrochloride were recorded from adrenalectomized and control rats. In order to control for a generalized decrease in sensory sensitivity, recordings from the auriculotemporal nerve to tactile stimulation of the pinna were also performed. There were no group differences in amplitude of the integrated neural responses to tactile stimulation. The largest decrease in gustatory responsivity occurred for suprathreshold concentrations of sodium chloride and lithium chloride. The data are discussed with reference to possible mechanisms underlying this neural alteration and to the role that reductions in salt taste responsivity play in mediating increases in salt intake.     

Effects of acetylcholine on coding of taste information in the primary gustatory cortex in rats

Acetylcholine (ACh) receptors are widely distributed throughout the cerebral cortex in rats. Recently, cholinergic innervation of the gustatory cortex (GC) was reported to be involved in certain taste learning in rats. Here, the effects of iontophoretic application of ACh on the response properties of GC neurons were studied in urethane-anesthetized rats. ACh affected spontaneous discharges in a small fraction of taste neurons (11 of 86 neurons tested), but influenced taste responses in 27 of 43 neurons tested. No correlations with ACh susceptibility were noted for spontaneous discharges and taste responses. Among the 27 neurons, ACh facilitated taste responses in 13, inhibited taste responses in 13 and either facilitated or inhibited taste responses depending on the stimuli in 1. Furthermore, ACh affected the responses to best stimuli that produced the largest responses among four basic tastants (best responses) in 7 of 27 taste neurons, to non-best responses in 9, and to both best and non-best responses in 11. ACh mostly inhibited the best responses (13 of 18 neurons). Thus, ACh often decreased the response selectivity to the four basic tastants and changed the response profile. Atropine, a general antagonist of muscarinic receptors, antagonized ACh actions on taste responses or displayed the opposite effects on taste responses to ACh actions in two-thirds of the neurons tested. These findings indicate that ACh mostly modulates taste responses through muscarinic receptors, and suggest that ACh shifts the state of the neuron network in the GC, in terms of the response selectivities and response profiles.     

Sodium chloride detection threshold in the rat determined using a simple operant taste discrimination task

A method for training rats to lick at high rates for a water reinforcer after presentation of one tastant and to inhibit or decrease response rate to avoid a time-out punisher after presentation of another tastant is described and evaluated. The method produced rapid acquisition of simple discrimination and detection tasks, The absolute mean detection threshold for sodium chloride in three rats was 0.0038% (0.0031%–0.0043%). The operant conditioning technique is simple, efficient, and should prove useful for psychophysical and physiological studies of gustation.     

Enhanced short-latency responses in the ventral posterior medial (VPM) thalamic nucleus following whisker trimming in the adult rat

This study examined the effects of whisker trimming on the functional organization of the adult somatosensory thalamus. In vivo extracellular unit recordings were made on ventral posterior medial (VPM) thalamic neurons in urethane anaesthetised adult rats. Neuronal response properties to controlled whisker deflection were recorded in untrimmed control animals and in animals where one row of whiskers had been trimmed for a median of 18 days. Trimming significantly increased short-latency responses to stimulation of the centre receptive field whisker (mean increase of 36%, p<.001). Longer latency responses to surround receptive field whiskers were unaffected. Spontaneous firing was significantly decreased in trimmed animals. A condition-test paradigm indicated that thalamic inhibition was reduced following whisker trimming, although this effect failed to reach statistical significance. These results demonstrate a capacity of the adult somatosensory thalamus to undergo functional reorganization in response to non-traumatic and innocuous whisker trimming.     

GABAergic projections from the thalamic reticular nucleus to the anteroventral and anterodorsal thalamic nuclei of the rat

We have studied GABAergic projections from the thalamic reticular nucleus to the anterior thalamic nuclei of the rat by combining retrograde labelling with horseradish peroxidase and GABA-immunohistochentistry. Small iontophoretic injections of the tracer into subnuclei of the anterior thalamic nuclear complex resulted in retrograde labelling of cells in the rostrodorsal pole of the ipsilateral thalamic reticular nucleus. All of these cells were also GABA-positive. The projections were topographically organized. Neurons located in the most dorsal part of the rostral reticular nucleus projected to the dorsal half of both the posterior subdivision and the medial subdivision of the anteroventral thalamic nucleus, and to the rostral portion of the anterodorsal thalamic nucleus. Immediately ventral to this group of neurons, but still within the dorsal portion of the reticular nucleus, a second group of neurons, extending from the dorsolateral to the dorsomedial edge of the nucleus, projected to the ventral parts of the posterior and medial subdivisions of the anteroventral nucleus. Following injection of tracer into the dorsal part of the rostral anteroventral nucleus, retrograde labelled GABA-containing cell bodies were also found in the ipsilateral anterodorsal nucleus.     

Leminscal and extralemniscal thalamic lesions and tactile discrimination in the rat

Summary Rats with lesions centered in the ventrobasal nuclear complex, the parafascicular-centrum median complex, or the posterior nuclear group were compared to each other and to control groups with and without thalamic damage on a battery of five two-choice tactile discriminations. Almost all animals mastered the first four discriminations, although many rats with lesions did not learn the discrimination with the least difference between positive and negative stimuli. Statistical analyses revealed differences in the raw scores and in the frequency of deviant scores between animals with lesions of the ventrobasal complex and controls, as well as between rats with parafascicular damage and controls. Animals with damage in the posterior nuclear group also showed some deficits on the problems. Histological analyses revealed possible differences in lesion size and locus for ventrobasal and parafascicular animals that did and did not master the series of tactile discriminations. Results are interpreted in terms of the roles of lemniscal and extralemniscal systems in somatic sensation and performance.This investigation was supported by National Science Foundation Grant GB-12374 and by Biomedical Sciences Support Grant FR-07 054 from the General Research Support Branch, Division of Research Resources, Bureau of Health Professions, Education and Manpower Training, National Institute of Health.     

Muscarinic action of acetylcholine in the rat ventromedial thalamic nucleus

Summary Several lines of evidence suggest a role for ACh in the mediation of cerebello-thalamic transmission. The physiological, pharmacological and biochemical experiments described were designed to test this hypothesis for the rat cerebello-thalamic pathway. Unilateral electrolytic lesions of the superior cerebellar peduncle resulted in modest falls of CAT from both ventromedial thalamic nuclei (contralateral 35%, ipsilateral 15%). Iontophoretic application of ACh to relay cells evokes three types of response (i) excitation (ii) inhibition (iii) polyphasic combinations of (i) and (ii). The type of response evoked was directly related to the firing pattern of the cell. Thus, for example, excitatory responses were never recorded during high-frequency bursting but were easily evoked following a switch to tonic, single-spike activity. All responses to ACh and synaptic responses to cerebellar stimulation were sensitive to muscarinic but not to nicotinic cholinergic antagonists. The nicotinic antagonist mecamylamine was a potent blocker of excitant amino acid responses but had no effect on cerebellarevoked synaptic responses. Cholinergic and anticholinergic agents had a profound action on relay cell firing pattern. ACh promoted single-spike activity whereas atropine promoted high-frequency bursting. The actions of ACh are discussed with reference to recently discovered voltage-sensitive ionic conductances. Because of the modulatory action of ACh on relay cell firing pattern and excitability no firm conclusion can be reached concerning the hypothesis under test here. We tentatively suggest a dual role for ACh as both neurotransmitter and neuromodulator.     

Electrophysiological actions of quinine on voltage-dependent currents in dissociated rat taste cells

 How taste receptor cells participate in encoding disparate compounds into distinct taste qualities represents a fundamental problem in the study of gustatory transduction mechanisms. Quinine is the most common stimulus employed to represent bitterness yet its electrophysiological consequences on voltage-dependent ion channels in the taste receptor cell have not been elucidated in detail. This study examines such effects on taste receptor cells dissociated from the foliate and circumvallate papillae of the rat. Outward potassium currents, which include transient, sustained and calcium-activated components, were reversibly inhibited by bath application of quinine, with an IC₅₀ of 5.1×10^–6 M. The time course of the current traces, along with voltage shifts in normalized conductance and inactivation curves, suggests that multiple mechanisms of inhibition may be occurring. Inwardly rectifying potassium currents were unaffected. Sodium currents, to somewhat higher concentrations of quinine (IC₅₀ = 6.4×10^–5 M), were also reduced in magnitude without noticeable effects on activation or reversal potential but with a shift in inactivation. Calcium currents, visualized with barium as a charge carrier, were enhanced in magnitude by the presence of low concentrations of quinine (10^–5 M) but were suppressed by higher concentrations (10^–4 M). Quinine broadened the waveform of the gustatory action potential and increased the input resistance. These data serve as genesis to future investigations of the signal transduction mechanism of quinine on voltage-dependent currents. Received: 18 November 1996 / Received after revision: 25 February 1997 / Accepted: 5 March 1997