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1.  Water as an Independent Taste Modality 
To qualify as a “basic” taste quality or modality, defined as a group of chemicals that taste alike, three empirical benchmarks have commonly been used. The first is that a candidate group of tastants must have a dedicated transduction mechanism in the peripheral nervous system. The second is that the tastants evoke physiological responses in dedicated afferent taste nerves innervating the oropharyngeal cavity. Last, the taste stimuli evoke activity in central gustatory neurons, some of which may respond only to that group of tastants. Here we argue that water may also be an independent taste modality. This argument is based on the identification of a water dedicated transduction mechanism in the peripheral nervous system, water responsive fibers of the peripheral taste nerves and the observation of water responsive neurons in all gustatory regions within the central nervous system. We have described electrophysiological responses from single neurons in nucleus of the solitary tract (NTS) and parabrachial nucleus of the pons, respectively the first two central relay nuclei in the rodent brainstem, to water presented as a taste stimulus in anesthetized rats. Responses to water were in some cases as robust as responses to other taste qualities and sometimes occurred in the absence of responses to other tastants. Both excitatory and inhibitory responses were observed. Also, the temporal features of the water response resembled those of other taste responses. We argue that water may constitute an independent taste modality that is processed by dedicated neural channels at all levels of the gustatory neuraxis. Water-dedicated neurons in the brainstem may constitute key elements in the regulatory system for fluid in the body, i.e., thirst, and as part of the swallowing reflex circuitry.
PMCID: PMC2967336  PMID: 21048894
taste; gustatory; water; nucleus of the solitary tract; parabrachial nucleus of the pons
2.  Neural Coding Mechanisms for Flow Rate in Taste-Responsive Cells in the Nucleus of the Solitary Tract of the Rat 
Journal of neurophysiology  2006;97(2):1857-1861.
When a taste stimulus enters the mouth, intentional movement of the stimulus within the oropharyngeal cavity affects the rate at which taste receptors are exposed to the stimulus and may ultimately affect taste perception. Early studies have shown that stimulus flow rate, the experimental equivalent of the effects of these investigative movements, modulates the portion of the peripheral nerve response that occurs when behavioral assessments of tastants are made. The present experiment studied the neural coding mechanisms for flow rate in the nucleus of the solitary tract (NTS), the first central relay in the taste pathway. Responses to NaCl (0.1 M) presented at high (5 ml/s) and low (3 ml/s) flow rates, sucrose (0.5 M), quinine HCl (0.01 M), and HCl (0.01 M) were recorded extracellularly from single NTS units in multiple replications. Information conveyed by evoked responses was analyzed with a family of metrics that quantify the similarity of two spike trains in terms of spike count and spike timing. Information about flow rate was conveyed by spike timing and spike count in approximately equal proportions of units (each ∼1/3), whereas information about taste quality was conveyed by spike timing in about half of the units. Different subsets of units contributed information for discrimination of flow rate and taste quality.
PMCID: PMC2659613  PMID: 17182909
3.  Quality time: Representation of a multidimensional sensory domain through temporal coding 
Receptive fields of sensory neurons in the brain are usually restricted to a portion of the entire stimulus domain. At all levels of the gustatory neuraxis, however, there are many cells that are broadly tuned, i.e., they respond well to each of the basic taste qualities (sweet, sour, salty and bitter). Although it might seem that this broad tuning precludes a major role for these cells in representing taste space, here we show the opposite – namely, that the tastant-specific temporal aspects (firing rate envelope and spike timing) of their responses enable each cell to represent the entire stimulus domain. Specifically, we recorded the response patterns of cells in the nucleus of the solitary tract (NTS) to representatives of four basic taste qualities and their binary mixtures. We analyzed the temporal aspects of these responses, and used their similarities and differences to construct the taste space represented by each neuron. We found that for the more broadly tuned neurons in the NTS, the taste space is a systematic representation of the entire taste domain. That is, the taste space of these broadly tuned neurons is three-dimensional, with basic taste qualities widely separated and binary mixtures placed close to their components. Further, the way that taste quality is represented by the firing rate envelope is consistent across the population of cells. Thus, the temporal characteristics of responses in the population of NTS neurons, especially those that are more broadly tuned, produce a comprehensive and logical representation of the taste world.
PMCID: PMC2766857  PMID: 19625513
taste; nucleus of the solitary tract; temporal coding; gustation; electrophysiology; rat
4.  A Test for Measuring Gustatory Function 
The Laryngoscope  2008;118(8):1411-1416.
The purpose of this study is to determine the usefulness of edible taste strips for measuring human gustatory function.
Research Design
The physical properties of edible taste strips were examined in order to determine their potential for delivering threshold and suprathreshold amounts of taste stimuli to the oral cavity. Taste strips were then assayed by fluorescence to analyze the uniformity and distribution of bitter tastant in the strips. Finally, taste recognition thresholds for sweet taste were examined in order to determine whether or not taste strips would produce recognition thresholds that were equal to or better than those obtained from aqueous tests.
Edible strips were prepared from pullulan-hydroxypropyl methylcellulose solutions that were dried to a thin film. The maximal amount of a tastant that could be incorporated in a 2.54 × 2.54 cm taste strip was identified by including representative taste stimuli for each class of tastant (sweet, sour, salty, bitter, and umami) during strip formation. Distribution of the bitter tastant quinine hydrochloride in taste strips was assayed by fluorescence emission spectroscopy. The efficacy of taste strips for evaluating human gustatory function was examined by using a single series ascending method of limits protocol. Sucrose taste recognition threshold data from edible strips was then compared to results that were obtained from a standard “sip and spit” recognition threshold test.
Edible films that formed from a pullulan-hydroxypropyl methylcellulose polymer mixture can be used to prepare clear, thin strips that have essentially no background taste and leave no physical presence after release of tastant. Edible taste strips could uniformly incorporate up to five percent of their composition as tastant. Taste recognition thresholds for sweet taste were over one order of magnitude lower with edible taste strips when compared to an aqueous taste test.
Edible taste strips are a highly sensitive method for examining taste recognition thresholds in humans. This new means of presenting taste stimuli should have widespread applications for examining human taste function in the lab, in the clinic, or at remote locations.
PMCID: PMC2823587  PMID: 18528309
gustation; taste test; pullulan; hydroxypropyl methylcellulose; sweet taste
5.  Taste Coding in the Nucleus of the Solitary Tract of the Awake, Freely Licking Rat 
It is becoming increasingly clear that the brain processes sensory stimuli differently according to whether they are passively or actively acquired, and these differences can be seen early in the sensory pathway. In the nucleus of the solitary tract (NTS), the first relay in the central gustatory neuraxis, a rich variety of sensory inputs generated by active licking converge. Here we show that taste responses in the NTS reflect these interactions. Experiments consisted of recordings of taste-related activity in the NTS of awake rats as they freely licked exemplars of the five basic taste qualities (sweet, sour, salty, bitter, umami). Nearly all taste-responsive cells were broadly tuned across taste qualities. A subset responded to taste with long latencies (>1.0 s), suggesting the activation of extra-oral chemoreceptors. Analyses of the temporal characteristics of taste responses showed that spike timing conveyed significantly more information than spike count alone in almost half of NTS cells, as in anesthetized rats, but with less information per cell. In addition to taste-responsive cells, the NTS contains cells that synchronize with licks. Since the lick pattern per se can convey information, these cells may collaborate with taste-responsive cells to identify taste quality. Other cells become silent during licking. These latter “anti-lick” cells show a surge in firing rate predicting the beginning and signaling the end of a lick bout. Collectively, the data reveal a complex array of cell types in the NTS, only a portion of which include taste-responsive cells, which work together to acquire sensory information.
PMCID: PMC3427930  PMID: 22855799
6.  Information Processing in the Parabrachial Nucleus of the Pons 
As the second synapse in the central gustatory pathway of the rodent, the parabrachial nucleus of the pons (PbN) receives information about taste stimuli directly from the nucleus of the solitary tract (NTS). Data show that NTS cells amplify taste responses before transmitting taste-related signals to the PbN. NTS cells of varied response profiles send converging input to PbN cells, though input from NTS cells with similar profiles is more effective at driving PbN responses. PbN cells follow NTS input for the first 3 s of taste stimulation for NaCl, HCl, and quinine, but are driven in cyclic bursts throughout the response interval for sucrose. Analyses of the temporal characteristics of NTS and PbN responses show that both structures use temporal coding with equal effectiveness to identify taste quality. Thus, the NTS input to the PbN is comprehensive, in that PbN cells receive NTS input that could support broad sensitivity, systematic, in that the time course of PbN firing patterns depend reliably on the tastant, and efficient, in that information from the NTS is preserved as it is communicated across structures. Comparisons of NTS and PbN taste responses in rats form the basis for our speculation that in primates, where the central gustatory pathway does not synapse in the PbN, the function of the PbN in taste processing may have been incorporated into that of the NTS.
PMCID: PMC3759149  PMID: 19686160
taste; parabrachial pons; temporal coding
7.  The Cells and Logic for Mammalian Sour Taste detection 
Nature  2006;442(7105):934-938.
Mammals taste many compounds yet use a sensory palette consisting of only five basic taste modalities: sweet, bitter, sour, salty, and umami (the taste of monosodium glutamate)1,2. While this repertoire may appear modest, it provides animals with critical information about the nature and quality of food. Sour taste detection functions as an important sensory input to warn against the ingestion of acidic (e.g. spoiled or unripe) food sources1–3. We have used a combination of bioinformatics, genetic, and functional studies to identify PKD2L1, a polycystic kidney disease-like ion channel4, as a candidate mammalian sour taste sensor. In the tongue, PKD2L1 is expressed in a subset of taste receptor cells (TRCs) distinct from those responsible for sweet, bitter and umami taste. To examine the role of PKD2L1-expressing taste cells in vivo, we engineered mice with targeted genetic ablations of selected populations of TRCs. Animals lacking PKD2L1-cells are completely devoid of taste responses to sour stimuli. Notably, responses to all other tastants remained unaffected, proving that the segregation of taste qualities even extends to ionic stimuli. Our results now establish independent cellular substrates for four of the five basic taste modalities, and support a comprehensive labeled-line mode of taste coding at the periphery5–10. Interestingly, PKD2L1 is also expressed in specific neurons surrounding the central canal of the spinal cord. Here we demonstrate that these PKD2L1-expressing neurons send projections to the central canal, and selectively trigger action potentials in response to decreases in extracellular pH. We propose that these cells correspond to the long sought components of the cerebrospinal fluid chemosensory system11. Taken together, our results suggest a common basis for acid sensing in disparately different physiological settings.
PMCID: PMC1571047  PMID: 16929298
8.  Gustatory stimuli representing different perceptual qualities elicit distinct patterns of neuropeptide secretion from taste buds 
Taste stimuli that evoke different perceptual qualities (e.g., sweet, umami, bitter, sour, salty) are detected by dedicated subpopulations of taste bud cells that employ distinct combinations of sensory receptors and transduction molecules. Here, we report that taste stimuli also elicit unique patterns of neuropeptide secretion from taste buds that are correlated with those perceptual qualities. We measured tastant-dependent secretion of glucagon-like peptide-1 (GLP-1), glucagon and neuropeptide Y (NPY) from circumvallate papillae of Tas1r3+/+, +/− and −/− mice. Isolated tongue epithelia were mounted in modified Ussing chambers, permitting apical stimulation of taste buds; secreted peptides were collected from the basal side and measured by specific ELISAs. Appetitive stimuli (sweet: glucose, sucralose; umami: monosodium glutamate; polysaccharide: Polycose) elicited GLP-1 and NPY secretion and inhibited basal glucagon secretion. Sweet and umami stimuli were ineffective in Tas1r3−/− mice, indicating an obligatory role for the T1R3 subunit common to the sweet and umami taste receptors. Polycose responses were unaffected by T1R3 deletion, consistent with the presence of a distinct polysaccharide taste receptor. The effects of sweet stimuli on peptide secretion also required the closing of ATP-sensitive K+ (KATP) channels, as the KATP channel activator diazoxide inhibited the effects of glucose and sucralose on both GLP-1 and glucagon release. Both sour citric acid and salty NaCl increased NPY secretion but had no effects on GLP-1 or glucagon. Bitter denatonium showed no effects on these peptides. Together, these results suggest that taste stimuli of different perceptual qualities elicit unique patterns of neuropeptide secretion from taste buds.
PMCID: PMC3687534  PMID: 23616560
9.  Two types of inhibitory influences target different groups of taste-responsive cells in the nucleus of the solitary tract of the rat 
Brain research  2009;1275:24-32.
Electrical stimulation of the chorda tympani nerve (CT; innervating taste buds on the rostral tongue) is known to initiate recurrent inhibition in cells in the nucleus of the solitary tract (NTS, the first central relay in the gustatory system). Here, we explored the relationship between inhibitory circuits and the breadth of tuning of taste-responsive NTS neurons. Initially, NTS cells with evoked responses to electrical stimulation of the CT (0.1 ms pulses; 1 Hz) were tested with each of four tastants (0.1 M NaCl, 0.01 M HCl, 0.01 M quinine and 0.5 M sucrose) in separate trials. Next, the CT was electrically stimulated using a paired-pulse (10-2000 ms interpulse interval; blocks of 100 trials) paradigm. Forty-five (30 taste-responsive) of 51 cells with CT-evoked responses (36 taste-responsive) were tested with paired pulses. The majority (34; 75.6%) showed paired-pulse attenuation, defined as fewer evoked spikes in response to the second (test) pulse compared with the first (conditioning) pulse. A bimodal distribution of the peak of paired-pulse attenuation was found with modes at 10 ms and 50 ms in separate groups of cells. Cells with early peak attenuation showed short CT-evoked response latencies and large responses to relatively few taste stimuli. Conversely, cells with late peak attenuation showed long CT-evoked response latencies and small taste responses with less selectivity. Results suggest that the breadth of tuning of an NTS cell may result from the combination of the sensitivities of peripheral nerve inputs and the recurrent influences generated by the circuitry of the NTS.
PMCID: PMC2699607  PMID: 19371730
taste; gustation; chorda tympani nerve; nucleus of the solitary tract; electrical stimulation; inhibition
10.  Temporal Characteristics of Gustatory Responses in Rat Parabrachial Neurons Vary by Stimulus and Chemosensitive Neuron Type 
PLoS ONE  2013;8(10):e76828.
It has been demonstrated that temporal features of spike trains can increase the amount of information available for gustatory processing. However, the nature of these temporal characteristics and their relationship to different taste qualities and neuron types are not well-defined. The present study analyzed the time course of taste responses from parabrachial (PBN) neurons elicited by multiple applications of “sweet” (sucrose), “salty” (NaCl), “sour” (citric acid), and “bitter” (quinine and cycloheximide) stimuli in an acute preparation. Time course varied significantly by taste stimulus and best-stimulus classification. Across neurons, the ensemble code for the three electrolytes was similar initially but quinine diverged from NaCl and acid during the second 500ms of stimulation and all four qualities became distinct just after 1s. This temporal evolution was reflected in significantly broader tuning during the initial response. Metric space analyses of quality discrimination by individual neurons showed that increases in information (H) afforded by temporal factors was usually explained by differences in rate envelope, which had a greater impact during the initial 2s (22.5% increase in H) compared to the later response (9.5%). Moreover, timing had a differential impact according to cell type, with between-quality discrimination in neurons activated maximally by NaCl or citric acid most affected. Timing was also found to dramatically improve within-quality discrimination (80% increase in H) in neurons that responded optimally to bitter stimuli (B-best). Spikes from B-best neurons were also more likely to occur in bursts. These findings suggest that among PBN taste neurons, time-dependent increases in mutual information can arise from stimulus- and neuron-specific differences in response envelope during the initial dynamic period. A stable rate code predominates in later epochs.
PMCID: PMC3790754  PMID: 24124597
11.  Processing of Hedonic and Chemosensory Features of Taste in Medial Prefrontal and Insular Networks 
The Journal of Neuroscience  2013;33(48):18966-18978.
Most of the research on cortical processing of taste has focused on either the primary gustatory cortex (GC) or the orbitofrontal cortex (OFC). However, these are not the only areas involved in taste processing. Gustatory information can also reach another frontal region, the medial prefrontal cortex (mPFC), via direct projections from GC. mPFC has been studied extensively in relation to its role in controlling goal-directed action and reward-guided behaviors, yet very little is known about its involvement in taste coding. The experiments presented here address this important point and test whether neurons in mPFC can significantly process the physiochemical and hedonic dimensions of taste. Spiking responses to intraorally delivered tastants were recorded from rats implanted with bundles of electrodes in mPFC and GC. Analysis of single-neuron and ensemble activity revealed similarities and differences between the two areas. Neurons in mPFC can encode the chemosensory identity of gustatory stimuli. However, responses in mPFC are sparser, more narrowly tuned, and have a later onset than in GC. Although taste quality is more robustly represented in GC, taste palatability is coded equally well in the two areas. Additional analysis of responses in neurons processing the hedonic value of taste revealed differences between the two areas in temporal dynamics and sensitivities to palatability. These results add mPFC to the network of areas involved in processing gustatory stimuli and demonstrate significant differences in taste-coding between GC and mPFC.
PMCID: PMC3841457  PMID: 24285901
12.  Sour Taste Responses in Mice Lacking PKD Channels 
PLoS ONE  2011;6(5):e20007.
The polycystic kidney disease-like ion channel PKD2L1 and its associated partner PKD1L3 are potential candidates for sour taste receptors. PKD2L1 is expressed in type III taste cells that respond to sour stimuli and genetic elimination of cells expressing PKD2L1 substantially reduces chorda tympani nerve responses to sour taste stimuli. However, the contribution of PKD2L1 and PKD1L3 to sour taste responses remains unclear.
Methodology/Principal Findings
We made mice lacking PKD2L1 and/or PKD1L3 gene and investigated whole nerve responses to taste stimuli in the chorda tympani or the glossopharyngeal nerve and taste responses in type III taste cells. In mice lacking PKD2L1 gene, chorda tympani nerve responses to sour, but not sweet, salty, bitter, and umami tastants were reduced by 25–45% compared with those in wild type mice. In contrast, chorda tympani nerve responses in PKD1L3 knock-out mice and glossopharyngeal nerve responses in single- and double-knock-out mice were similar to those in wild type mice. Sour taste responses of type III fungiform taste cells (GAD67-expressing taste cells) were also reduced by 25–45% by elimination of PKD2L1.
These findings suggest that PKD2L1 partly contributes to sour taste responses in mice and that receptors other than PKDs would be involved in sour detection.
PMCID: PMC3098277  PMID: 21625513
13.  Thalamic contribution to cortical processing of taste and expectation 
Taste related information reaches the gustatory cortex (GC) through two routes: a thalamic and a limbic pathway. While evidence is accumulating on limbic-cortical interactions in taste, very little information is available on the function of the gustatory thalamus in shaping GC activity. Here we rely on behavioral electrophysiological techniques to study taste-evoked activity in GC before and after inactivation of the parvicellular portion of the ventroposteromedial nucleus of thalamus (VPMpc; i.e. the gustatory thalamus). Gustatory stimuli were presented to rats either alone or preceded by an anticipatory cue. The reliance on two different behavioral contexts allowed us to investigate how the VPMpc mediates GC responses to uncued tastants, cued tastants and anticipatory cues. Inactivation of the thalamus resulted in a dramatic reduction of taste processing in GC. However, responses to anticipatory cues were unaffected by this manipulation. The use of a cue-taste association paradigm also allowed for the identification of two subpopulations of taste specific neurons: those that responded to gustatory stimulation and to the cue (i.e. cue-and-taste) and those that responded to tastants only (i.e. taste-only). Analyses of these two populations revealed differences in response dynamics and connectivity with the VPMpc.
The results provide novel evidence for the role of VPMpc in shaping GC activity and demonstrate a previously unknown association between responsiveness to behavioral events, temporal dynamics and thalamic connectivity in GC.
PMCID: PMC3711560  PMID: 23365221
14.  The effect of barium on perceptions of taste intensity and palatability 
Dysphagia  2013;29(1):96-108.
Barium may affect the perception of taste intensity and palatability. Such differences are important considerations in the selection of dysphagia assessment strategies and interpretation of results.
Eighty healthy women grouped by age (younger, older) and genetic taste status (supertaster, non-taster) rated intensity and palatability for seven tastants prepared in deionized water with and without 40% w/v barium: non-carbonated and carbonated water, diluted ethanol, and high concentrations of citric acid (sour), sodium chloride (salty), caffeine (bitter) and sucrose (sweet). Mixed model analyses explored the effects of barium, taster status, and age on perceived taste intensity and acceptability of stimuli.
Barium was associated with lower taste intensity ratings for sweet, salty, and bitter tastants, higher taste intensity in carbonated water, and lower palatability in water, sweet, sour, and carbonated water. Older subjects reported lower palatability (all barium samples, sour) and higher taste intensity scores (ethanol, sweet, sour) compared to younger subjects. Supertasters reported higher taste intensity (ethanol, sweet, sour, salty, bitter) and lower palatability (ethanol, salty, bitter) than non-tasters. Refusal rates were highest for younger subjects and supertasters, and for barium (regardless of tastant), bitter, and ethanol.
Barium suppressed the perceived intensity of some tastes and reduced palatability. These effects are more pronounced in older subjects and supertasters, but younger supertasters are least likely to tolerate trials of barium and strong tastant solutions.
PMCID: PMC4313733  PMID: 24037100
Dysphagia; Taste; Mixture Suppression; Barium; Palatability; Deglutition; Deglutition Disorders
The gustatory nerves of mice lacking P2X2 and P2X3 purinergic receptor subunits (P2X-dblKO) are unresponsive to taste stimulation (Finger et al., 2005). Surprisingly, P2X-dblKO mice show residual behavioral responses to concentrated tastants, presumably via post-ingestive detection. Therefore, the current study tested whether post-ingestive signaling is functional in P2X-dblKO mice and if so, whether it activates the primary viscerosensory nucleus of the medulla, the nucleus of the solitary tract (nTS). Like WT animals, P2X-dblKO mice learned to prefer a flavor paired with 150 mM monosodium glutamate (MSG) over a flavor paired with water. This preference shows that, even in the absence of taste sensory input, post-ingestive cues are detected and associated with a flavor in P2X-dblKO mice. MSG-evoked neuronal activation in the nTS was measured by expression of the immediate early gene c-Fos (c-Fos-like immunoreactivity; Fos-LI). In rostral, gustatory nTS, P2X-dblKO animals, unlike WT animals, showed no taste quality-specific labeling of neurons. Further, MSG-evoked Fos-LI was significantly less in P2X-dblKO mice compared to WT animals. In contrast, in more posterior, viscerosensory nTS, MSG-induced Fos-LI was similar in WT and P2X-dblKO mice. Together, these results suggest that P2X-dblKO mice can form preferences based on post-ingestive cues and that post-ingestive detection of MSG does not rely on the same purinergic signaling that is crucial for taste.
PMCID: PMC3131261  PMID: 21697361
taste; feeding; post-ingestive; MSG; c-Fos; nucleus of the solitary tract; P2X; purinergic signaling
16.  Ensembles of Gustatory Cortical Neurons Anticipate and Discriminate Between Tastants in a Single Lick 
Frontiers in Neuroscience  2007;1(1):161-174.
The gustatory cortex (GC) processes chemosensory and somatosensory information and is involved in learning and anticipation. Previously we found that a subpopulation of GC neurons responded to tastants in a single lick (Stapleton et al., 2006). Here we extend this investigation to determine if small ensembles of GC neurons, obtained while rats received blocks of tastants on a fixed ratio schedule (FR5), can discriminate between tastants and their concentrations after a single 50 μL delivery. In the FR5 schedule subjects received tastants every fifth (reinforced) lick and the intervening licks were unreinforced. The ensemble firing patterns were analyzed with a Bayesian generalized linear model whose parameters included the firing rates and temporal patterns of the spike trains. We found that when both the temporal and rate parameters were included, 12 of 13 ensembles correctly identified single tastant deliveries. We also found that the activity during the unreinforced licks contained signals regarding the identity of the upcoming tastant, which suggests that GC neurons contain anticipatory information about the next tastant delivery. To support this finding we performed experiments in which tastant delivery was randomized within each block and found that the neural activity following the unreinforced licks did not predict the upcoming tastant. Collectively, these results suggest that after a single lick ensembles of GC neurons can discriminate between tastants, that they may utilize both temporal and rate information, and when the tastant delivery is repetitive ensembles contain information about the identity of the upcoming tastant delivery.
PMCID: PMC2570088  PMID: 18982126
Bayesian generalized linear model; gustatory cortex; neural ensembles; fixed ratio schedule; multi-electrode neurophysiology; rate and temporal coding; gustation, licking
17.  Taste Enhancement by Pulsatile Stimulation Is Receptor Based But Independent of Receptor Type 
Chemosensory Perception  2012;5(2):179-187.
Effects of subjects’ taste sensitivity (expressed as taste detection threshold), tastant quality and taste transduction mechanism on pulsation-induced taste enhancement were tested. Taste intensities of pulsatile MSG and NaCl stimuli at pulsation periods below, at and above individual taste fusion periods (TFP in seconds) were compared to taste intensities of a continuous reference of the same net tastant concentration and quality. In line with results previously reported for sucrose, pulsation-induced taste enhancement peaked around TFP for both MSG and NaCl and did not require perception of tastant pulsation. TFP and pulsation effects were independent of the taste transduction mechanism (G-protein-coupled receptor for MSG versus ion-channel for NaCl). The absence of a relation between TFP and taste sensitivity suggests that temporal gustatory resolution and taste sensitivity are not necessarily influenced by the same factors. The results support earlier findings that early stages of taste transduction are involved in pulsation-induced taste enhancement. Pulsation-induced taste enhancement is determined by the pulsation rate (i.e. TFP) which is longer for MSG than NaCl. This is probably due to the tastant-specific interaction with the receptor rather than the taste transduction mechanism (G-protein-coupled receptor versus ion-channel) involved.
PMCID: PMC3343238  PMID: 22611466
Pulsatile stimulation; Taste enhancement; Taste fusion period; Taste receptor; Gustometer; Chemistry; Neurosciences; Chemistry/Food Science, general; Food Science
18.  Relationships among Taste Qualities Assessed with Response-Context Effects 
Chemical Senses  2011;36(7):581-587.
Psychophysical judgments often depend on stimulus context. For example, sugar solutions are judged sweeter when a tasteless fruity aroma has been added. Response context also matters; adding a fruity aroma to sugar increases the rated sweetness when only sweetness is considered but not when fruitiness is judged as well. The interaction between stimulus context and response context has been explored more extensively in taste–odor mixtures than in taste–taste mixtures. To address this issue, subjects in the current study rated the sourness of citric acid mixed with quinine (bitter), sodium chloride (salty), and cyclamate (sweet) (stimulus context). In one condition, subjects rated sourness alone. In another, subjects rated both sourness and the other salient quality (bitterness, saltiness, or sweetness) (response context). Sourness ratings were most sensitive to response context for sour–salty mixtures (i.e., ratings of sourness alone exceeded ratings of sourness made simultaneously with saltiness) and least sensitive to context for the sour–sweet mixtures (sourness ratings made under the 2 conditions were essentially identical). Response-context effects for the sour–bitter mixture were nominally intermediate. The magnitudes of these context effects were related to judgments of qualitative similarity between citric acid and the other stimuli, consistent with prior findings. These types of context effects are relevant to the study of taste–taste mixture interactions and should provide insight into the perceptual similarities among the taste qualities.
PMCID: PMC3155392  PMID: 21441368
gustatory; psychophysics; similarity
19.  A High Throughput In Vivo Assay for Taste Quality and Palatability 
PLoS ONE  2013;8(8):e72391.
Taste quality and palatability are two of the most important properties measured in the evaluation of taste stimuli. Human panels can report both aspects, but are of limited experimental flexibility and throughput capacity. Relatively efficient animal models for taste evaluation have been developed, but each of them is designed to measure either taste quality or palatability as independent experimental endpoints. We present here a new apparatus and method for high throughput quantification of both taste quality and palatability using rats in an operant taste discrimination paradigm. Cohorts of four rats were trained in a modified operant chamber to sample taste stimuli by licking solutions from a 96-well plate that moved in a randomized pattern beneath the chamber floor. As a rat’s tongue entered the well it disrupted a laser beam projecting across the top of the 96-well plate, consequently producing two retractable levers that operated a pellet dispenser. The taste of sucrose was associated with food reinforcement by presses on a sucrose-designated lever, whereas the taste of water and other basic tastes were associated with the alternative lever. Each disruption of the laser was counted as a lick. Using this procedure, rats were trained to discriminate 100 mM sucrose from water, quinine, citric acid, and NaCl with 90-100% accuracy. Palatability was determined by the number of licks per trial and, due to intermediate rates of licking for water, was quantifiable along the entire spectrum of appetitiveness to aversiveness. All 96 samples were evaluated within 90 minute test sessions with no evidence of desensitization or fatigue. The technology is capable of generating multiple concentration–response functions within a single session, is suitable for in vivo primary screening of tastant libraries, and potentially can be used to evaluate stimuli for any taste system.
PMCID: PMC3741146  PMID: 23951319
20.  Time to taste 
Fly  2010;4(4):283-287.
Circadian clocks keep time in the digestive, circulatory, reproductive, excretory and nervous systems even in absence of external cues. Central oscillators in the brain control locomotor activity of organisms ranging from fruit flies to man, but the functions of the clocks in peripheral nervous system are not well understood. The presence of autonomous peripheral oscillators in the major taste organ of drosophila, the proboscis, prompted us to test whether gustatory responses are under control of the circadian clock. We find that synchronous rhythms in physiological and behavioral responses to attractive and aversive tastants are driven by oscillators in gustatory receptor neurons (GRNs); primary sensory neurons that carry taste information from the proboscis to the brain. During the middle of the night, high levels of G protein-coupled receptor kinase 2 (GPRK2) in the GRNs suppresses tastant-evoked responses. Flies with disrupted gustatory clocks are hyperphagic and hyperactive, recapitulating behaviors typically seen under the stress of starvation. Temporal plasticity in innate behaviors should offer adaptive advantages to flies. In this Extra View article we discuss how oscillators inside GRNs regulate responsiveness to tastants and influence feeding, metabolism and general activity.
PMCID: PMC3174479  PMID: 20798595
circadian clock; chemosensory; GPRK2; GRN; taste; gustatory system; feeding
21.  Regulation of gustatory physiology and appetitive behavior by the circadian clock in Drosophila melanogaster 
Current biology : CB  2010;20(4):300-309.
Circadian regulation of chemosensory processes is common in animals, but little is known about how circadian clocks control chemosensory systems or the consequences of rhythms in chemosensory system function. Taste is a major chemosensory gate used to decide whether or not an animal will eat, and the main taste organ in Drosophila, the proboscis, harbors autonomous circadian oscillators. Here we examine gustatory physiology, tastant-evoked appetitive behavior, and food ingestion to understand clock-dependent regulation of the Drosophila gustatory system.
Here we report that single-unit responses from labellar gustatory receptor neurons (GRNs) to attractive and aversive tastants show diurnal and circadian rhythms in spike amplitude, frequency and duration across different classes of gustatory sensilla. Rhythms in electrophysiological responses parallel behavioral rhythms in proboscis extension reflex (PrER). Molecular oscillators in GRNs are necessary and sufficient for rhythms in gustatory responses, and drive rhythms in G protein coupled receptor kinase 2 (GPRK2) expression that mediate rhythms in taste-sensitivity. Eliminating clock function in certain GRNs increases feeding and locomotor activity, mimicking a starvation response.
Circadian clocks in GRNs control neuronal output and drive behavioral rhythms in taste responses that peak at a time of day when feeding is maximal in flies. Our results argue that oscillations in GPRK2 levels drive rhythms in gustatory physiology and behavior, and that GRN clocks repress feeding. The similarity in gustatory system organization and feeding behavior in flies and mammals, and diurnal changes in taste sensitivity in humans, suggest that our results are relevant to the situation in humans.
PMCID: PMC4234688  PMID: 20153192
22.  Breadth of Tuning and Taste Coding in Mammalian Taste Buds 
A longstanding question in taste research concerns taste coding and, in particular, how broadly are individual taste bud cells tuned to taste qualities (sweet, bitter, umami, salty, and sour). Taste bud cells express G-protein-coupled receptors for sweet, bitter, or umami tastes but not in combination. However, responses to multiple taste qualities have been recorded in individual taste cells. We and others have shown previously there are two classes of taste bud cells directly involved in gustatory signaling: “receptor” (type II) cells that detect and transduce sweet, bitter, and umami compounds, and “presynaptic” (type III) cells. We hypothesize that receptor cells transmit their signals to presynaptic cells. This communication between taste cells could represent a potential convergence of taste information in the taste bud, resulting in taste cells that would respond broadly to multiple taste stimuli. We tested this hypothesis using calcium imaging in a lingual slice preparation. Here, we show that receptor cells are indeed narrowly tuned: 82% responded to only one taste stimulus. In contrast, presynaptic cells are broadly tuned: 83% responded to two or more different taste qualities. Receptor cells responded to bitter, sweet, or umami stimuli but rarely to sour or salty stimuli. Presynaptic cells responded to all taste qualities, including sour and salty. These data further elaborate functional differences between receptor cells and presynaptic cells, provide strong evidence for communication within the taste bud, and resolve the paradox of broad taste cell tuning despite mutually exclusive receptor expression.
PMCID: PMC3717408  PMID: 17913917
taste bud; cell type; taste processing; presynaptic cell; receptor cell; coding
23.  Sarco/Endoplasmic Reticulum Ca2+-ATPases (SERCA) Contribute to GPCR-Mediated Taste Perception 
PLoS ONE  2011;6(8):e23165.
The sense of taste is important for providing animals with valuable information about the qualities of food, such as nutritional or harmful nature. Mammals, including humans, can recognize at least five primary taste qualities: sweet, umami (savory), bitter, sour, and salty. Recent studies have identified molecules and mechanisms underlying the initial steps of tastant-triggered molecular events in taste bud cells, particularly the requirement of increased cytosolic free Ca2+ concentration ([Ca2+]c) for normal taste signal transduction and transmission. Little, however, is known about the mechanisms controlling the removal of elevated [Ca2+]c from the cytosol of taste receptor cells (TRCs) and how the disruption of these mechanisms affects taste perception. To investigate the molecular mechanism of Ca2+ clearance in TRCs, we sought the molecules involved in [Ca2+]c regulation using a single-taste-cell transcriptome approach. We found that Serca3, a member of the sarco/endoplasmic reticulum Ca2+-ATPase (SERCA) family that sequesters cytosolic Ca2+ into endoplasmic reticulum, is exclusively expressed in sweet/umami/bitter TRCs, which rely on intracellular Ca2+ release for signaling. Serca3-knockout (KO) mice displayed significantly increased aversive behavioral responses and greater gustatory nerve responses to bitter taste substances but not to sweet or umami taste substances. Further studies showed that Serca2 was mainly expressed in the T1R3-expressing sweet and umami TRCs, suggesting that the loss of function of Serca3 was possibly compensated by Serca2 in these TRCs in the mutant mice. Our data demonstrate that the SERCA family members play an important role in the Ca2+ clearance in TRCs and that mutation of these proteins may alter bitter and perhaps sweet and umami taste perception.
PMCID: PMC3149081  PMID: 21829714
24.  Not so fast: taste stimulus coding time in the rat revisited 
Behavioral and electrophysiological studies suggest that rats can identify a taste stimulus with a single lick, in <200 ms. However, the conditions under which these conclusions were drawn varied widely across experiments. We designed a series of experiments to assess the effects of the number of licks of a tastant that are available, tastant concentration and prior learning experience on the speed with which a tastant can modify behavior. To accomplish this we tested exemplars of four basic taste qualities (quinine, 0.1 mM; NaCl, 100 mM; saccharin, 4 mM, or sucrose, 100 mM; citric acid, 10 mM) in rats that were conditioned to avoid quinine. Taste stimuli were available for one, two, or three licks on separate days. All tastants were presented in a randomized order interspersed with water rinse licks presented on a variable ratio schedule. A tastant-specific significant increase in the proportion of long pauses in licking following quinine presentation was defined as evidence of “behavioral identification.” Rats with aversion training given three licks of all taste stimuli paused significantly more often after quinine by the fourth interlick interval, ~580 ms. Control rats showed no evidence of quinine (0.1 mM) identification. When rats in all conditioning groups were tested with a high concentration of quinine (10 mM), a single lick was sufficient to produce significant pausing after quinine, but not until the fourth interlick interval, i.e., ~580 ms. Testing rats with only two tastants rather than four in a session had no effect on the speed of quinine identification. Present data confirm that a single lick is sufficient for rats to identify a taste stimulus, but that additional licks occur before evidence of identification is apparent. Furthermore, learning, tastant concentration and motivation to drink can all modify the speed of behavioral identification.
PMCID: PMC3364696  PMID: 22666196
taste; identification; behavior; conditioned taste aversion; rat
25.  When a good taste turns bad: Neural mechanisms underlying the emergence of negative affect and associated natural reward devaluation by cocaine 
Neuropharmacology  2013;76(0 0):360-369.
An important feature of cocaine addiction in humans is the emergence of negative affect (e.g., dysphoria, irritability, anhedonia), postulated to play a key role in craving and relapse. Indeed, the DSM-IV recognizes that social, occupational and/or recreational activities become reduced as a consequence of repeated drug use where previously rewarding experiences (e.g., food, job, family) become devalued as the addict continues to seek and use drug despite serious negative consequences. Here, research in the Carelli laboratory is reviewed that examined neurobiological mechanisms that may underlie these processes using a novel animal model. Oromotor responses (taste reactivity) were examined as rats learned that intraoral infusion of a sweet (e.g., saccharin) predicts impending but delayed access to cocaine self-administration. We showed that rats exhibit aversive taste reactivity (i.e., gapes/rejection responses) during infusion of the sweet paired with impending cocaine, similar to aversive responses observed during infusion of quinine, a bitter tastant. Critically, the expression of this pronounced aversion to the sweet predicted the subsequent motivation to self-administer cocaine. Electrophysiology studies show that this shift in palatability corresponds to an alteration in nucleus accumbens (NAc) cell firing; neurons that previously responded with inhibition during infusion of the palatable sweet shifted to excitatory activity during infusion of the cocaine-devalued tastant. This excitatory response profile is typically observed during infusion of quinine, indicating that the once palatable sweet becomes aversive following its association with impending but delayed cocaine, and NAc neurons encode this aversive state. We also review electrochemical studies showing a shift (from increase to decrease) in rapid NAc dopamine release during infusion of the cocaine-paired tastant as the aversive state developed, again, resulting in responses similar to quinine infusion. Collectively, our findings suggest that cocaine-conditioned cues elicit a cocaine-need state that is aversive, is encoded by a distinct subset of NAc neurons and rapid dopamine signaling, and promotes cocaine-seeking behavior. Finally, we present data showing that experimentally induced abstinence (30 days) exacerbates this natural reward devaluation by cocaine, and this effect is correlated with a greater motivation to lever press during extinction. Dissecting the neural mechanisms underlying these detrimental consequences of addiction is critical since it may lead to novel treatments that ameliorate negative affective states associated with drug use and decrease the drive (craving) for the drug.
PMCID: PMC4160877  PMID: 23639430

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