Volume 8 Supplement 3
The neural processing of taste
© Lemon and Katz; licensee BioMed Central Ltd. 2007
Published: 18 September 2007
Although there have been many recent advances in the field of gustatory neurobiology, our knowledge of how the nervous system is organized to process information about taste is still far from complete. Many studies on this topic have focused on understanding how gustatory neural circuits are spatially organized to represent information about taste quality (e.g., "sweet", "salty", "bitter", etc.). Arguments pertaining to this issue have largely centered on whether taste is carried by dedicated neural channels or a pattern of activity across a neural population. But there is now mounting evidence that the timing of neural events may also importantly contribute to the representation of taste. In this review, we attempt to summarize recent findings in the field that pertain to these issues. Both space and time are variables likely related to the mechanism of the gustatory neural code: information about taste appears to reside in spatial and temporal patterns of activation in gustatory neurons. What is more, the organization of the taste network in the brain would suggest that the parameters of space and time extend to the neural processing of gustatory information on a much grander scale.
In general, there are two models of spatial coding that have been proposed to account for the neural representation of taste information. One viewpoint, known as "labeled-line" theory, proposes that neurons encode taste in a binary fashion: when cells are active (i.e., turned "on") they signal the presence of a particular stimulus feature, in this case a single taste quality [1, 2]. When these same neurons are quiescent or "off", a stimulus that evokes this particular quality is absent. Thus, the activation of a cell serves one and only one purpose under the auspices of labeled-line theory. In contrast to this view, some have argued that taste is carried by a pattern of activity across a population of neurons [3, 4]. In "across-neuron pattern" theory, individual neurons contribute to the representation of multiple stimulus qualities and quality information is signaled by the response of a neuronal population.
Although the coding debate has largely waffled between whether taste uses lines or patterns, traditional spatial coding models overlook information dependencies that could be present in the timing of action potentials or in time-dependent interactions among gustatory neurons. Yet the very nature of the organization of taste circuits in the central nervous system (CNS) as interactive networks arranged in series, in parallel and recurrently would impose temporal structure on the activities of neurons in any given taste nucleus or region. Such structure could serve various functions in the processing of taste, such as to evolve spatial representations about taste stimuli through time as related to various external and organismal variables. Here, we summarize recent developments that shed new light on how the parameters of space and time may contribute to the neural processing of taste information.
Spatial processing: taste receptors and the brain
In some respects, a labeled-line mechanism is likely the least complex form of spatial coding that a sensory neural circuit could adopt. Interest in a line code as a plausible explanation of the operation of circuits for taste has been invigorated by the results of recent molecular and genomic studies of taste receptors. These investigations have identified two families of G-protein-coupled receptors, known as the T1r and T2r receptors, involved in the transduction of different taste stimuli. Members of the T1r class combine form heterodimeric, functional receptors that sense palatable taste stimuli. Specifically, the T1r3/T1r2 receptor recognizes some ligands described as sweet-tasting by humans whereas the T1r3/T1r1 receptor is involved in the detection of amino acid stimuli [5, 6]. On the other hand, receptors of the T2r family are implicated for the detection of unpalatable, bitter-tasting ligands [7, 8]. These receptors for sweet, umami and bitter stimuli have been found to be expressed in non-overlapping subsets of taste bud cells (TBCs) in oral epithelia, which has been interpreted as evidence of cellular specificity to a single stimulus quality [9–11]. Mice engineered to express receptors for a tasteless compound in TBCs that normally harbor T1r sweet or T2r bitter receptors display corresponding preference or aversion of this ligand [12, 13]. Moreover, the expression of bitter receptors in T1r "sweet" TBCs results in behavioral attraction towards bitter ligands . Some have argued that these findings indicate that individual TBCs respond to stimuli of only a single taste quality class and that information about a given quality is carried along one of a few dedicated, labeled neural channels [9, 12–14].
Although the non-overlapping expression patterns of T1r and T2r receptors have been touted as evidence for labeled-line coding, other data paint a different picture of taste processing in the periphery. Functional studies using patch clamp electrophysiology and calcium imaging techniques have shown that many TBCs are broadly sensitive to stimuli of different taste qualities, with some TBCs responding to both sweet and bitter stimuli [15–17]. What is more, there is evidence for multiple receptors for sweet and umami stimuli [18, 19], which tempers conclusions about the peripheral processing of these tastants drawn from studies of single kinds of receptors. Psychophysical studies have found no difference in detection thresholds for sucrose or monosodium glutamate between mice genetically engineered to lack the T1r3 receptor and wild-type controls , suggesting that T1r3-independent receptors are importantly involved in the detection of sweet and umami stimuli. Finally, there is now evidence suggesting that taste cells exchange information with neighboring cells within a bud and that there are separate populations of cells for sensing taste stimuli and communicating with afferent nerves [21–23]. This raises the possibility that information from taste receptor cells with different tuning properties could converge onto common cells in the taste bud for transmittal to the brain . Processing within taste buds could potentially muddle the interpretation of receptor gene expression data as showing dedicated "lines" for taste qualities. Further studies of routes of communication within taste buds will shed light on the intricacies of interactions among TBCs.
How are central neural circuits for taste organized to encode information about stimulus quality? Pursuing an answer to this question has been complicated by the pervasive multisensitive nature of central gustatory neurons. That is, numerous investigations have shown that central networks for taste are composed of categories of neurons that are generally broadly responsive to stimuli of different taste qualities. At odds with the line hypothesis drawn from studies of the expression patterns of T1r and T2r receptors, several studies have indicated that categories of central gustatory neurons that are strongly responsive to sweet or bitter stimuli are not specifically-tuned to only these kinds of tastants, displaying robust sensitivity to stimuli such as sodium salts (i.e., "salty") and acidic ("sour") solutions [24–27]. A neurophysiological study of how neurons in the nucleus of the solitary tract (NST) process bitter taste information conveyed by the VIIth nerve, which provides input critical for behavioral taste discriminations , found that the category of neuron that responded most strongly to bitter tastants, such as quinine, denatonium benzoate and papaverine, responded just as well to moderate concentrations of the sodium salts NaCl and NaNO3 . From the perspective of a labeled-line code, that NaCl drives these bitter most-responsive neurons just as effectively as a many strongly bitter stimuli, such as quinine, would predict that NaCl should elicit a prominent "bitter" sensation that is common to quinine. However, rats do not behaviorally generalize between the tastes of NaCl and quinine in conditioning paradigms [29, 30], suggesting that these stimuli are perceived by rodents as independent. In addition, rats prefer moderate concentrations of NaCl whereas they clearly avoid suprathreshold concentrations of quinine . Yet if we attend solely to the output of bitter most-responsive neurons, which according to the line hypothesis should allow us to detect bitter tastes, we would not be able to tell whether NaCl or quinine was present on gustatory epithelia. A more recent study of the NST reported the presence of cells selective for bitter tastants . But the majority of the bitter-sensitive neurons described in  were shown to receive taste input from the IXth nerve, which is thought to contribute more to oromotor reflexes than to taste quality identification [28, 33]. Clearly it becomes difficult to reconcile the neural representation of the qualitative identity of bitter tastants by considering only those neurons that respond most effectively to such stimuli.
That neuron categories or "types" are multisensitive suggests that the output of any single neuron class alone can only provide equivocal information about taste quality [34, 35], which has implications for how central gustatory circuits could be organized to represent information about tastants. But before going further it is important to carefully consider what analyses of neuron types can actually tell us about neural information processing. It has been commonplace in gustatory neurophysiological studies to use as the unit of analysis the neuron type, which reflects the pooled response of neurons of a common category. These categories are typically defined by grouping cells on the basis of their best stimulus or through multivariate procedures that cluster neurons based on similarities among their response profiles to a set of stimuli. Analyses in which neuron type is a primary factor seemingly assume that it is the pooled response of a group of neurons that the brain would make due with in order to decipher stimulus input. But how would the brain pool the activities of neurons of a common type? Would the brain need to attend to all cells of the group or only a subset? Moreover, does the pooling scheme used by the brain adhere to experimenter-imposed categorizations of neurons? Or does the brain simply "readout" the activities of gustatory neurons on an individual basis? Of course, there are no clear answers to any of these questions. How the brain would pool the activities of gustatory neurons in the NST, for example, would likely be dependent on the specifics of synaptic connections between these cells and follower neurons in the parabrachial nucleus, a topic which is not well understood. Further, the average response of a neuron type could potentially under- or overestimate the tuning properties of individual cells. Thus, evaluating the coding performance of gustatory neurons is likely best indexed through understanding the information-handling limits of the individual cells themselves, which would also bear on the stimulus detection performance that could be achieved through pooling their activities in some way. Defining these limits requires knowledge of how reliably individual gustatory neurons respond to stimuli over time and across trials, a topic that has received only scant attention in the literature (but see ).
Just as important as within-neuron response variability, one must consider the length of time over which taste responses are measured. Many studies of taste processing have quantified the activities of gustatory neurons based on spike counts measured over 5 or 10 second stimulus-response windows. Yet it is important to acknowledge that this period is exceedingly long relative to amount of time that it takes the nervous system to arrive at a perceptual judgment about taste stimulus quality. Behavioral studies using conditioned avoidance procedures have shown that rats can recognize and respond to taste stimuli in less than 1 second following contact [37–39]. What this means is that necessary and sufficient information about stimulus quality is embedded in the spiking activities of gustatory neurons during the first few hundred milliseconds of evoked activity. This brief window containing critical information about stimulus identity may correspond to only a few or several action potentials maximum in many gustatory neurons when they are under taste drive.
Although intriguing, the model presented in  (Figure 2) presents a description of how a spatial neural representation could potentially work in taste. The model shows that information about tastant identity could be extracted by a hypothetical reader that compares NST neurons under a theoretical framework. But it is, of course, unknown whether or not the nervous system would adopt a similar algorithm to register tastant identity. Understanding exactly how taste neurons are being "readout" by the brain will require knowledge of the architecture of networks linking these cells to downstream neurons and nuclei and the information transfer functions used in these circuits. The specifics here remain to be worked out.
Time and interactive processing in taste
Historically, most models of gustatory coding have not attended to information that could be carried by dependencies on the timing of neural events. In fact, strict across-neuron pattern and labeled-line models assume that time matters very little in "gustatory coding." Evidence supporting this assumption is actually scanty, however. The use of 5–10 sec firing rate averages has, for the most part, been adopted by necessity rather than design, as taste neurons are often only held through single presentations of individual stimuli. While some studies report correlations between overall firing rates and taste-related behaviors among the members of large stimulus batteries, these correlations are moderate at best and describe only broad similarities between tastes . Furthermore, the oft-cited fact that rodents can, under some circumstances, demonstrate recognition of a taste in ~200 msec [39, 42] fails to serve as a strong indictment against temporal coding for at least 2 reasons: 1) this result causes equal problems for all current coding schemes – given that taste information arrives at the NST relatively slowly  and that taste responses are relatively low-firing-rate phenomena, neurons only have an opportunity to fire a few spikes in the first 200 msec that a taste is on the animal's tongue – a paucity of information for the purposes of reliable recognition of an activated neuron or spatial pattern; and 2) many taste-related behaviors occur only on a time-scale an order of magnitude higher than that described in the above-mentioned studies  – the code produced depends on the attentional state of the animal , along with many other task-specific variables.
There are several reasons to consider time in gustatory coding, meanwhile, above and beyond the fact that different taste behaviors require differing amounts of stimulus processing time. First, networks in the NST [46, 47] and beyond, including larger networks of feed-forward and feedback connections [48–51], almost ensure that taste processing and coding will be modulated through time as neurons receive asynchronous input from multiple sources (this topic will be returned to shortly). In addition, it is likely that taste coding has a temporal aspect because most other sensory responses have been shown to do so [52–54].
What little evidence has been collected thus far suggests that gustatory neurons do respond to tastes with time-varying patterns of activity, at both the brainstem  and cortical [55, 56] levels. To some extent this result is obtained because the collection of multiple trials of data, which is required for complex analysis, reveals subtle, phasic, and multi-phasic responses that are missed in overall rate analyses of single trial datasets. Such datasets also reveal that response profiles determined from experiments in which each taste was delivered only once or twice are frequently overly influenced by trial-to-trial variability in responsiveness , for which CNS neurons are notorious. Thus, reliance on large, tonic responses causes researchers to mischaracterize taste coding both in what is observed and in what is missed.
Adherents to spatial coding hypotheses deem the subtler, time-varying modulations observed in taste responses to be either "noise" or "unimportant." Such conclusions, however, are contradicted by at least two types of studies: those demonstrating that temporal codes carry specific, useful information, and those showing that animals can make taste judgments based solely on temporal codes.
As to the first of these types of studies, taste codes recorded from awake animals do not simply vary through time – they appear to "multiplex" information [55, 57], as has also been shown for both visual  and olfactory responses . That is, early portions of the taste responses, at least in cortex, convey information about taste quality, whereas later portions convey information about taste palatability. More recent data suggest that changes in these "late phase" responses are specifically related to changes in taste palatability, measured in terms of orofacial behaviors . This serves as evidence that taste temporal coding may reflect the processing that the taste receives as the animal decides what it thinks of the taste.
Furthermore, examinations of ensemble responses reveal that what appears in single neuron records to be random trial-to-trial variability is in fact coherent at the population level. When spikes and firing rate changes in cortical neurons are related to spikes and changes in other, simultaneously recorded neurons (instead of to the onset of a stimulus), they can be seen to be progressing through taste-specific series of states that "evolve" at different rates on different trials . The state sequence provides significantly better information about the taste delivered in a particular trial than do methods based on overall rates (or even time-varying PSTHs). This and the previous study suggest that the temporal codes are important to understanding the processing of tastes. While it is clear that gapes and licks can be produced by brainstem central pattern generator (CPG) circuits, lesion studies show that a large network of forebrain regions – prefrontal cortex, amygdala, and hypothalamus, at least – is responsible for making decisions about palatability [61–63], and thus for deciding which brainstem patterns are produced in the intact animal; as an analogy think of the control of walking, which can be done by spinalized mammals and yet intrinsically involves cerebellar and cortical control mechanisms .
But of course absolute proof requires experiments showing that temporal codes are used, not simply that they can be used. Two recent studies are exciting in this regard. In one, researchers electrically stimulated the NTS of rats, using a temporal pattern of spikes that had been previously recorded in response to a taste, as those rats drank water. The rats responded to the water as if it was bitter when a quinine pattern of stimulation was delivered . Furthermore, a conditioned aversion to sucrose generalized to water consumed simultaneously with sucrose pattern delivery, but not to the delivery of other taste patterns. These data provide compelling evidence that rats use temporal codes for taste.
Manduca caterpillars also appear to make use of temporal information when identifying tastes . These critters have a few transductive elements (sensillae) that respond to a wide array of bitter stimuli; these sensillae respond to aristolochic acid (AA) with an accelerating pattern of spikes, and to caffeine with a decelerating pattern of spikes. When efforts are made to equalize the overall spiking responses to these stimuli (i.e., the spatial codes), the caterpillars still distinguish between AA and salicin (another bitter taste that provokes a decelerating neural response) but not between caffeine and salicin. These data strongly support the value of time in taste.
The activity of neural networks provides a plausible mechanism for most of the temporal coding phenomena described above. Studies that have used multi-electrode recordings to reveal interactions between taste neurons [67–70], and those that have used a combination of stimulation/inactivation and recording to reveal feedback influences on NTS and PbN taste responses [48–51], demonstrate the reality of network processing in taste. Clearly, taste neurons "talk" to each other, and this conversation goes on between varieties of neurons within single brain regions, in convergences of neurons with disparate response patterns on single downstream targets, and in modulation of basic responses by forebrain neurons carrying more highly processed information. It is almost inevitable that neural interactions will cause modulation of taste responses through time.
There is evidence that the "code" for taste in the brain could involve both spatial [71, 72] and temporal aspects of the activities of gustatory neurons. But the parameters of space and time are also critical to gustatory coding on a much larger scale. Taste processing is a network-level event, involving distributed CNS structures that engage one another in time-dependent fashion. It is this interactive processing between the nodes of the taste system that regulates information flow throughout the central gustatory neuraxis, ultimately shaping and evolving the neural "code" for taste relative various parameters of ongoing perceptual and behavioral processing. Understanding such neural interactions could provide a compelling window to the organization of circuits for taste, although our knowledge here is still in its infancy.
Supported by National Institutes of Health grants DC008194 to C.H.L. and DC006666, DC007703 to D.B.K.
This article has been published as part of BMC Neuroscience Volume 8 Supplement 3, 2007: The chemical senses: recent advances and new promises. The full contents of the supplement are available online at http://www.biomedcentral.com/1471-2202/8?issue=S3.
- Pfaffmann C, Frank M, Bartoshuk LM, Snell TC: Coding gustatory information in the squirrel monkey chorda tympani. Progress in Psychobiology and Physiological Psychology. Edited by: Sprague JM, Epstein AN. 1976, New York: Academic Press, 6: 1-27.Google Scholar
- Hellekant G, Ninomiya Y, Danilova V: Taste in chimpanzees. III: labeled-line coding in sweet taste. Physiol Behav. 1998, 65: 191-200. 10.1016/S0031-9384(97)00532-5.View ArticlePubMedGoogle Scholar
- Pfaffmann C: The afferent code for sensory quality. Am Psychol. 1959, 14: 226-232. 10.1037/h0049324.View ArticleGoogle Scholar
- Erickson RP: Sensory neural patterns and gustation. Olfaction and Taste. Edited by: Zotterman Y. 1963, Oxford: Pergamon Press, 1: 205-213.View ArticleGoogle Scholar
- Nelson G, Chandrashekar J, Hoon MA, Feng L, Zhao G, Ryba NJ, Zuker CS: An amino-acid taste receptor. Nature. 2002, 416: 199-202. 10.1038/nature726.View ArticlePubMedGoogle Scholar
- Li X, Staszewski L, Xu H, Durick K, Zoller M, Adler E: Human receptors for sweet and umami taste. Proc Natl Acad Sci USA. 2002, 99: 4692-4696. 10.1073/pnas.072090199.PubMed CentralView ArticlePubMedGoogle Scholar
- Chandrashekar J, Mueller KL, Hoon MA, Adler E, Feng L, Guo W, Zuker CS, Ryba NJ: T2Rs function as bitter taste receptors. Cell. 2000, 100: 703-711. 10.1016/S0092-8674(00)80706-0.View ArticlePubMedGoogle Scholar
- Bufe B, Hofmann T, Krautwurst D, Raguse JD, Meyerhof W: The human TAS2R16 receptor mediates bitter taste in response to beta-glucopyranosides. Nat Genet. 2002, 32: 397-401. 10.1038/ng1014.View ArticlePubMedGoogle Scholar
- Scott K: The sweet and the bitter of mammalian taste. Curr Opin Neurobiol. 2004, 14: 423-427. 10.1016/j.conb.2004.06.003.View ArticlePubMedGoogle Scholar
- Nelson G, Hoon MA, Chandrashekar J, Zhang Y, Ryba NJ, Zuker CS: Mammalian sweet taste receptors. Cell. 2001, 106: 381-390. 10.1016/S0092-8674(01)00451-2.View ArticlePubMedGoogle Scholar
- Adler E, Hoon MA, Mueller KL, Chandrashekar J, Ryba NJP, Zuker CS: A novel family of mammalian taste receptors. Cell. 2000, 100: 693-702. 10.1016/S0092-8674(00)80705-9.View ArticlePubMedGoogle Scholar
- Mueller KL, Hoon MA, Erlenbach I, Chandrashekar J, Zuker CS, Ryba NJ: The receptors and coding logic for bitter taste. Nature. 2005, 434: 225-229. 10.1038/nature03352.View ArticlePubMedGoogle Scholar
- Zhao GQ, Zhang Y, Hoon MA, Chandrashekar J, Erlenbach I, Ryba NJ, Zuker CS: The receptors for mammalian sweet and umami taste. Cell. 2003, 115: 255-266. 10.1016/S0092-8674(03)00844-4.View ArticlePubMedGoogle Scholar
- Zhang Y, Hoon MA, Chandrashekar J, Mueller KL, Cook B, Wu D, Zuker CS, Ryba NJ: Coding of sweet, bitter, and umami tastes: different receptor cells sharing similar signaling pathways. Cell. 2003, 112: 293-301. 10.1016/S0092-8674(03)00071-0.View ArticlePubMedGoogle Scholar
- Sato T, Beidler LM: Broad tuning of rat taste cells to four basic taste stimuli. Chem Senses. 1997, 22: 287-293. 10.1093/chemse/22.3.287.View ArticlePubMedGoogle Scholar
- Gilbertson TA, Boughter JD, Zhang H, Smith DV: Distribution of gustatory sensitivities in rat taste cells: whole-cell responses to apical chemical stimulation. J Neurosci. 2001, 21: 4931-4941.PubMedGoogle Scholar
- Caicedo A, Kim KN, Roper SD: Individual mouse taste cells respond to multiple chemical stimuli. J Physiol. 2002, 544: 501-509. 10.1113/jphysiol.2002.027862.PubMed CentralView ArticlePubMedGoogle Scholar
- Maruyama Y, Pereira E, Margolskee RF, Chaudhari N, Roper SD: Umami responses in mouse taste cells indicate more than one receptor. J Neurosci. 2006, 26: 2227-2234. 10.1523/JNEUROSCI.4329-05.2006.PubMed CentralView ArticlePubMedGoogle Scholar
- Damak S, Rong M, Yasumatsu K, Kokrashvili Z, Varadarajan V, Zou S, Jiang P, Ninomiya Y, Margolskee RF: Detection of sweet and umami taste in the absence of taste receptor T1r3. Science. 2003, 301: 850-853. 10.1126/science.1087155.View ArticlePubMedGoogle Scholar
- Delay ER, Hernandez NP, Bromley K, Margolskee RF: Sucrose and Monosodium Glutamate Taste Thresholds and Discrimination Ability of T1R3 Knockout Mice. Chem Senses. 2006, 31: 351-357. 10.1093/chemse/bjj039.View ArticlePubMedGoogle Scholar
- Zhao FL, Shen T, Kaya N, Lu SG, Cao Y, Herness S: Expression, physiological action, and coexpression patterns of neuropeptide Y in rat taste-bud cells. Proc Natl Acad Sci USA. 2005, 102: 11100-11105. 10.1073/pnas.0501988102.PubMed CentralView ArticlePubMedGoogle Scholar
- Kaya N, Shen T, Lu SG, Zhao FL, Herness S: A paracrine signaling role for serotonin in rat taste buds: expression and localization of serotonin receptor subtypes. Am J Physiol Regul Integr Comp Physiol. 2004, 286: R649-658.View ArticlePubMedGoogle Scholar
- DeFazio RA, Dvoryanchikov G, Maruyama Y, Kim JW, Pereira E, Roper SD, Chaudhari N: Separate populations of receptor cells and presynaptic cells in mouse taste buds. J Neurosci. 2006, 26: 3971-3980. 10.1523/JNEUROSCI.0515-06.2006.PubMed CentralView ArticlePubMedGoogle Scholar
- Verhagen JV, Giza BK, Scott TR: Effect of amiloride on gustatory responses in the ventroposteromedial nucleus of the thalamus in rats. J Neurophysiol. 2005, 93: 157-166. 10.1152/jn.00823.2003.View ArticlePubMedGoogle Scholar
- Di Lorenzo PM, Lemon CH, Reich CG: Dynamic coding of taste stimuli in the brainstem: effects of brief pulses of taste stimuli on subsequent taste responses. J Neurosci. 2003, 23: 8893-8902.PubMedGoogle Scholar
- Lemon CH, Smith DV: Neural representation of bitter taste in the nucleus of the solitary tract. J Neurophysiol. 2005, 94: 3719-3729. 10.1152/jn.00700.2005.View ArticlePubMedGoogle Scholar
- Scott TR, Giza BK: Coding channels in the taste system of the rat. Science. 1990, 249: 1585-1587. 10.1126/science.2171145.View ArticlePubMedGoogle Scholar
- St John SJ, Spector AC: Behavioral discrimination between quinine and KCl is dependent on input from the seventh cranial nerve: implications for the functional roles of the gustatory nerves in rats. J Neurosci. 1998, 18: 4353-4362.PubMedGoogle Scholar
- Morrison GR: Behavioural response patterns to salt stimuli in the rat. Can J Psychology. 1967, 21: 141-152.View ArticleGoogle Scholar
- Nowlis GH, Frank ME, Pfaffmann C: Specificity of acquired aversions to taste qualities in hamsters and rats. J Comp Physiol Psychol. 1980, 94: 932-942. 10.1037/h0077809.View ArticlePubMedGoogle Scholar
- Pfaffmann C: Taste, its sensory and motivating properties. Am Sci. 1964, 52: 187-206.Google Scholar
- Geran LC, Travers SP: Single neurons in the nucleus of the solitary tract respond selectively to bitter taste stimuli. J Neurophysiol. 2006, 96: 2513-2527. 10.1152/jn.00607.2006.View ArticlePubMedGoogle Scholar
- Travers JB, Grill HJ, Norgren R: The effects of glossopharyngeal and chorda tympani nerve cuts on the ingestion and rejection of sapid stimuli: an electromyographic analysis in the rat. Behav Brain Res. 1987, 25: 233-246. 10.1016/0166-4328(87)90071-4.View ArticlePubMedGoogle Scholar
- Smith DV, St John SJ: Neural coding of gustatory information. Curr Opin Neurobiol. 1999, 9: 427-435. 10.1016/S0959-4388(99)80064-6.View ArticlePubMedGoogle Scholar
- Scott TR, Giza BK: Issues of gustatory neural coding: where they stand today. Physiol Behav. 2000, 69: 65-76. 10.1016/S0031-9384(00)00189-X.View ArticlePubMedGoogle Scholar
- Di Lorenzo PM, Victor JD: Taste response variability and temporal coding in the nucleus of the solitary tract of the rat. J Neurophysiol. 2003, 90: 1418-1431. 10.1152/jn.00177.2003.View ArticlePubMedGoogle Scholar
- Scott TR: Behavioral support for a neural taste theory. Physiol Behav. 1974, 12: 413-417. 10.1016/0031-9384(74)90118-8.View ArticlePubMedGoogle Scholar
- Halpern BP: Time as a factor in gustation: temporal patterns of taste stimulation and response. Taste, Olfaction, and the Central Nervous System. Edited by: Pfaff DW. 1985, New York, NY: Rockefeller University Press, 181-209.Google Scholar
- Halpern BP, Tapper DN: Taste stimuli: quality coding time. Science. 1971, 171: 1256-1258. 10.1126/science.171.3977.1256.View ArticlePubMedGoogle Scholar
- Lemon CH, Smith DV: Influence of response variability on the coding performance of central gustatory neurons. J Neurosci. 2006, 26: 7433-7443. 10.1523/JNEUROSCI.0106-06.2006.View ArticlePubMedGoogle Scholar
- Nakamura K, Norgren R: Taste responses of neurons in the nucleus of the solitary tract of awake rats: an extended stimulus array. J Neurophysiol. 1993, 70: 879-891.PubMedGoogle Scholar
- Boughter JD, John SJ, Noel DT, Ndubuizu O, Smith DV: A Brief-access Test for Bitter Taste in Mice. Chem Senses. 2002, 27: 133-142. 10.1093/chemse/27.2.133.View ArticlePubMedGoogle Scholar
- Erickson RP, Di Lorenzo PM, Woodbury MA: Classification of taste responses in brain stem: Membership in fuzzy sets. J Neurophysiol. 1994, 71: 2139-2150.PubMedGoogle Scholar
- Halpern BP: Temporal Characteristics of Human Taste Judgements as Calibrations for Gustatory Event-related Potentials and Gustatory Magnetoencephalographs. Chem Senses. 2005, 30 (Suppl 1): i228-i229. 10.1093/chemse/bjh197.View ArticlePubMedGoogle Scholar
- Fontanini A, Katz DB: State-dependent modulation of time-varying gustatory responses. J Neurophysiol. 2006, 96: 3183-3193. 10.1152/jn.00804.2006.View ArticlePubMedGoogle Scholar
- Bradley RM, Grabauskas G: Neural circuits for taste: excitation, inhibition, and synaptic plasticity in the rostral gustatory zone of the nucleus of the solitary tract. Ann N Y Acad Sci. 1998, 855: 467-474. 10.1111/j.1749-6632.1998.tb10607.x.View ArticlePubMedGoogle Scholar
- Lemon CH, Di Lorenzo PM: Effects of electrical stimulation of the chorda tympani nerve on taste responses in the nucleus of the solitary tract. J Neurophysiol. 2002, 88: 2477-2489. 10.1152/jn.00094.2002.View ArticlePubMedGoogle Scholar
- Li CS, Cho YK, Smith DV: Modulation of parabrachial taste neurons by electrical and chemical stimulation of the lateral hypothalamus and amygdala. J Neurophysiol. 2005, 93: 1183-1196. 10.1152/jn.00828.2004.View ArticlePubMedGoogle Scholar
- Li CS, Cho YK, Smith DV: Taste responses of neurons in the hamster solitary nucleus are modulated by the central nucleus of the amygdala. J Neurophysiol. 2002, 88: 2979-2992. 10.1152/jn.00239.2002.View ArticlePubMedGoogle Scholar
- Lundy RF, Norgren R: Activity in the hypothalamus, amygdala, and cortex generates bilateral and convergent modulation of pontine gustatory neurons. J Neurophysiol. 2004, 91: 1143-1157. 10.1152/jn.00840.2003.View ArticlePubMedGoogle Scholar
- Cho YK, Li CS, Smith DV: Descending influences from the lateral hypothalamus and amygdala converge onto medullary taste neurons. Chem Senses. 2003, 28: 155-171. 10.1093/chemse/28.2.155.View ArticlePubMedGoogle Scholar
- Ghazanfar AA, Nicolelis MAL: The space-time continuum in mammalian sensory pathways. Time and the Brain. Edited by: Sidney MR. 2000, Australia: Harwood Press, 97-130.View ArticleGoogle Scholar
- Laurent G, Stopfer M, Friedrich RW, Rabinovich MI, Volkovskii A, Abarbanel HD: Odor encoding as an active, dynamical process: experiments, computation, and theory. Annu Rev Neurosci. 2001, 24: 263-297. 10.1146/annurev.neuro.24.1.263.View ArticlePubMedGoogle Scholar
- McClurkin JW, Optican LM, Richmond BJ, Gawne TJ: Concurrent processing and complexity of temporally encoded neuronal messages in visual perception. Science. 1991, 253: 675-677. 10.1126/science.1908118.View ArticlePubMedGoogle Scholar
- Katz DB, Simon SA, Nicolelis MA: Dynamic and multimodal responses of gustatory cortical neurons in awake rats. J Neurosci. 2001, 21: 4478-4489.PubMedGoogle Scholar
- Kobayakawa T, Ogawa H, Kaneda H, Ayabe-Kanamura S, Endo H, Saito S: Spatio-temporal analysis of cortical activity evoked by gustatory stimulation in humans. Chemical Senses. 1999, 24: 201-209. 10.1093/chemse/24.2.201.View ArticlePubMedGoogle Scholar
- Katz DB: The many flavors of temporal coding in gustatory cortex. Chem Senses. 2005, 30 (Suppl 1): i80-i81. 10.1093/chemse/bjh123.View ArticlePubMedGoogle Scholar
- Sugase Y, Yamane S, Ueno S, Kawano K: Global and fine information coded by single neurons in the temporal visual cortex. Nature. 1999, 400: 869-873. 10.1038/23703.View ArticlePubMedGoogle Scholar
- Friedrich RW, Habermann CJ, Laurent G: Multiplexing using synchrony in the zebrafish olfactory bulb. Nat Neurosci. 2004, 7: 862-871. 10.1038/nn1292.View ArticlePubMedGoogle Scholar
- Jones LM, Fontanini A, Katz DB: Ensemble responses of gustatory cortical neurons accurately predict tastant identity. Chem Senses. 2006, 31: A115-Google Scholar
- Touzani K, Taghzouti K, Velley L: Increase of the aversive value of taste stimuli following ibotenic acid lesion of the central amygdaloid nucleus in the rat. Behavioural Brain Research. 1997, 88: 133-142. 10.1016/S0166-4328(96)02273-5.View ArticlePubMedGoogle Scholar
- Gutierrez R, Carmena JM, Nicolelis MA, Simon SA: Orbitofrontal ensemble activity monitors licking and distinguishes among natural rewards. J Neurophysiol. 2006, 95: 119-133. 10.1152/jn.00467.2005.View ArticlePubMedGoogle Scholar
- Ferssiwi A, Cardo B, Velley L: Gustatory preference-aversion thresholds are increased by ibotenic acid lesion of the lateral hypothalamus in the rat. Brain Res. 1987, 437: 142-150. 10.1016/0006-8993(87)91535-6.View ArticlePubMedGoogle Scholar
- Orlovsky GN, Deliagina TG, Grillner S: Neuronal control of locomotion from mollusc to man. 1999, Oxford: Oxford University PressView ArticleGoogle Scholar
- Di Lorenzo PM, Hallock RM, Kennedy DP: Temporal coding of sensation: mimicking taste quality with electrical stimulation of the brain. Behav Neurosci. 2003, 117: 1423-1433. 10.1037/0735-7044.117.6.1423.View ArticlePubMedGoogle Scholar
- Glendinning JI, Davis A, Rai M: Temporal coding mediates discrimination of "bitter" taste stimuli by an insect. J Neurosci. 2006, 26: 8900-8. 10.1523/JNEUROSCI.2351-06.2006.View ArticlePubMedGoogle Scholar
- Adachi M, Ohshima T, Yamada S, Satoh T: Cross-correlation analysis of taste neuron pairs in rat solitary tract nucleus. J Neurophysiol. 1989, 62: 501-509.PubMedGoogle Scholar
- Katz D, Simon S, Nicolelis MAL: Taste-specific neuronal ensembles in the gustatory cortex of awake rats. J Neurosci. 2002, 22: 1850-1857.PubMedGoogle Scholar
- Yokota T, Satoh T: Three-dimensional estimation of the distribution and size of putative functional units in rat gustatory cortex as assessed from the inter-neuronal distance between two neurons with correlative activity. Brain Res Bull. 2001, 54: 575-584. 10.1016/S0361-9230(01)00464-6.View ArticlePubMedGoogle Scholar
- Yamada S, Ohshima T, Oda H, Adachi M, Satoh T: Synchronized discharge of taste neurons recorded simultaneously in rat parabrachial nucleus. J Neurophysiol. 1990, 63: 294-302.PubMedGoogle Scholar
- Yoshimura H, Sugai T, Fukuda M, Segami N, Onoda N: Cortical spatial aspects of optical intrinsic signals in response to sucrose and NaCl stimuli. Neuroreport. 2004, 15: 17-20. 10.1097/00001756-200401190-00005.View ArticlePubMedGoogle Scholar
- Accolla R, Bathellier B, Petersen CC, Carleton A: Differential spatial representation of taste modalities in the rat gustatory cortex. J Neurosci. 2007, 27: 1396-1404. 10.1523/JNEUROSCI.5188-06.2007.View ArticlePubMedGoogle Scholar
This article is published under license to BioMed Central Ltd. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.