Review
Coding in the mammalian gustatory system

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To understand gustatory physiology and associated dysfunctions it is important to know how oral taste stimuli are encoded both in the periphery and in taste-related brain centres. The identification of distinct taste receptors, together with electrophysiological recordings and behavioral assessments in response to taste stimuli, suggest that information about distinct taste modalities (e.g. sweet versus bitter) are transmitted from the periphery to the brain via segregated pathways. By contrast, gustatory neurons throughout the brain are more broadly tuned, indicating that ensembles of neurons encode taste qualities. Recent evidence reviewed here suggests that the coding of gustatory stimuli is not immutable, but is dependant on a variety of factors including appetite-regulating molecules and associative learning.

Introduction

The gustatory system, together with the somatosensory system, is involved in analyzing diverse features of food, such as its chemosensory (modality, intensity), orosensory (texture, temperature, pungency) and rewarding properties. Other senses including vision and olfaction also contribute 1, 2 but their modulating roles in food perception are beyond the scope of this review.

The first goal of this review is to elaborate gustatory coding schemes in the periphery and cortical areas. In particular, the review highlights the increasing complexity of the gustatory neural pathway as demonstrated by the finding that cortical areas also contain information about the pleasantness or hedonic value (Glossary) of tastants. The second goal is to show how the gustatory system, at the central level, integrates information from internal signals and changes the tastants’ cortical representation accordingly.

Section snippets

Organizing tastes: from taste buds to cortex

Gustatory processing is first achieved at the level of taste-receptor cells (TRCs) that are assembled into taste buds (TBs) distributed among different papillae of the tongue, palate, larynx, pharynx, and epiglottis. TBs contain about 100 TRCs that protrude through the lingual epithelium into a taste pore (Figure 1a). Upon tastant binding to receptors on microvilli of TRCs, transduction machinery is activated and neurotransmitters are released that cause the excitation of afferent nerve fibres.

Taste coding

There are presently two major hypotheses on how taste information is processed [7]. The first, termed ‘labelled line’ (Glossary), refers to a coding model in which peripheral (or central) neurons that respond the most robustly to a given taste modality carry the totality of the information via segregated pathways. This coding scheme can simply be thought of as a wire extending from the periphery to the higher areas that signals a particular modality (e.g. sucrose). Intensity increases are

Coding at the periphery

Data from studies using a variety of different techniques, including genetic, morphological, and electrophysiological recordings, have shown that several types (and subtypes) of TRCs are present in TB cell types I, II and III [8]. Basal cells are progenitors of TRC cells and are found at the base of TBs 9, 10. Type I cells were initially believed to be supporting (or ‘glial-like’) cells because they express enzymes involved in transmitter uptake and degradation. However, recent studies showed

Coding in the brainstem and thalamus

Before discussing tastant responses in the brainstem and higher brain regions, when considering gustatory coding it is important to mention four factors that can influence the interpretation of experimental results. First, a large majority of the electrophysiological recordings are performed in anesthetized animals. The anaesthetic agent used could limit or modify inputs from other brain areas and hence alter and/or modify the neuron's selectivity to tastants [46]. Second, in nearly all of the

Coding in the primary gustatory cortex (GC)

The GC is a multimodal area that responds to tastants as well as to thermal, mechanical, visceral and nociceptive stimuli 65, 66, 67. Basically, the responses of individual GC neurons to tastants exhibit the same patterns of activity as those described for brainstem and thalamic neurons in that some have been reported to be quite selective to tastants, whereas others are more broadly tuned (Figure 2e). With few exceptions, the GC responses were measured as the average activity over several

Spatial maps of taste modalities in the gustatory cortex

Cells in the mammalian brain that perform a given function, or share common functional properties, are often grouped together anatomically. Striking examples come from the primary visual, auditory and somatosensory neocortices that are organized into spatial maps according to specific features of the sensory stimulus. Following the same organization principles, in the GC one can also expect to find a chemotopic organization, in other words, topographical regions in which neurons respond to a

Taste associative encoding

Having explored GC responses under conditions where the taste stimuli do not have any intrinsic meaning to the animal, other than their inherent hedonic value, we now review what happens when the response to a tastant is associated with a salient event. If taste processing were immutable, it follows that the behavioral response should be invariant. However, in a conditioned taste aversion (CTA, Glossary) paradigm, electrophysiological studies in rats found that some units change their response

The frontal cortex and reward

The OFC is often called the secondary taste cortex because it has direct projections from the GC. The functions of many OFC neurons are involved in decision making, predicting reward, and also encoding the reward value 83, 84. The OFC receives convergent gustatory, somatosensory, visual and olfactory inputs, and consequently many OFC neurons exhibit multisensory responses that can be important in consolidating the flavor of food. One physiologically interesting gustatory property of the OFC

Conclusion

This review provides evidence that gustatory processing in the periphery uses a labelled-line scheme, whereas gustatory processing within the CNS is contained in a multisensory, distributed, feed-forward and backward, plastic network that includes reward, and whose responses can depend on the animal's internal state. That is, the processing of information regarding what is ingested must be continually updated and taken into account because internal states associated with malaise or satiety can

Acknowledgements

We apologize to colleagues whose studies have not been cited in this review due to space constraints. A.C. was supported by the University of Geneva, the Swiss National Science Foundation, the European Research Council (contract number ERC-2009-StG-243344-NEUROCHEMS), the European Molecular Biology Organization (Young Investigator program) and the European Commission Coordinated Action ENINET (contract number LSHM-CT-2005-19063). S.A.S. was supported by National Institutes of Health grant

References (98)

  • P.M. Di Lorenzo

    The neural code for taste in the brain stem: response profiles

    Physiol. Behav.

    (2000)
  • R.M. Hallock et al.

    Temporal coding in the gustatory system

    Neurosci. Biobehav. Rev.

    (2006)
  • B.P. Halpern

    Constraints imposed on taste physiology by human taste reaction time data

    Neurosci. Biobehav. Rev.

    (1986)
  • M.A. Schoenfeld

    Functional magnetic resonance tomography correlates of taste perception in the human primary taste cortex

    Neuroscience

    (2004)
  • D.B. Katz

    Gustatory processing is dynamic and distributed

    Curr. Opin. Neurobiol.

    (2002)
  • D.M. Small

    Dissociation of neural representation of intensity and affective valuation in human gustation

    Neuron

    (2003)
  • Y. Yasoshima et al.

    Short-term and long-term excitability changes of the insular cortical neurons after the acquisition of taste aversion learning in behaving rats

    Neuroscience

    (1998)
  • E.T. Rolls et al.

    The orbitofrontal cortex and beyond: from affect to decision-making

    Prog. Neurobiol.

    (2008)
  • E.T. Rolls

    Sensory-specific and motivation-specific satiety for the sight and taste of food and water in man

    Physiol. Behav.

    (1983)
  • I.E. de Araujo

    Neural ensemble coding of satiety states

    Neuron

    (2006)
  • B. Bathellier

    Dynamic ensemble odor coding in the mammalian olfactory bulb: sensory information at different timescales

    Neuron

    (2008)
  • R.P. Erickson

    The evolution of neural coding ideas in the chemical senses

    Physiol. Behav.

    (2000)
  • B. Bathellier

    Wavelet-based multi-resolution statistics for optical imaging signals: application to automated detection of odour activated glomeruli in the mouse olfactory bulb

    Neuroimage

    (2007)
  • P. Dalton

    The merging of the senses: integration of subthreshold taste and smell

    Nat. Neurosci.

    (2000)
  • F.N. Zaidi

    Types of taste circuits synaptically linked to a few geniculate ganglion neurons

    J. Comp. Neurol.

    (2008)
  • A.C. Spector et al.

    The representation of taste quality in the mammalian nervous system

    Behav. Cogn. Neurosci. Rev.

    (2005)
  • D. Ongur et al.

    The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans

    Cereb. Cortex

    (2000)
  • J.C. Kinnamon et al.

    Ultrastructure of taste buds

  • T.E. Finger

    Cell types and lineages in taste buds

    Chem. Senses

    (2005)
  • T. Okubo

    Cell lineage mapping of taste bud cells and keratinocytes in the mouse tongue and soft palate

    Stem Cells

    (2009)
  • N. Shigemura

    Amiloride-sensitive NaCl taste responses are associated with genetic variation of ENaC alpha-subunit in mice

    Am. J. Physiol. Regul. Integr. Comp. Physiol.

    (2008)
  • A. Vandenbeuch

    Amiloride-sensitive channels in type I fungiform taste cells in mouse

    BMC Neurosci.

    (2008)
  • J. Chandrashekar

    The cells and peripheral representation of sodium taste in mice

    Nature

    (2010)
  • J. Chandrashekar

    The receptors and cells for mammalian taste

    Nature

    (2006)
  • C.A. Perez

    A transient receptor potential channel expressed in taste receptor cells

    Nat. Neurosci.

    (2002)
  • A.L. Huang

    The cells and logic for mammalian sour taste detection

    Nature

    (2006)
  • J. Chandrashekar

    The taste of carbonation

    Science

    (2009)
  • V. Lyall

    Decrease in rat taste receptor cell intracellular pH is the proximate stimulus in sour taste transduction

    Am. J. Physiol. Cell Physiol.

    (2001)
  • K.L. Mueller

    The receptors and coding logic for bitter taste

    Nature

    (2005)
  • T.A. Gilbertson

    Distribution of gustatory sensitivities in rat taste cells: whole-cell responses to apical chemical stimulation

    J. Neurosci.

    (2001)
  • C.E. Riera

    Sensory attributes of complex tasting divalent salts are mediated by TRPM5 and TRPV1 channels

    J. Neurosci.

    (2009)
  • K.J. Watson

    Expression of aquaporin water channels in rat taste buds

    Chem. Senses

    (2007)
  • P. Cameron

    The molecular basis for water taste in Drosophila

    Nature

    (2010)
  • D. Gaillard

    The gustatory pathway is involved in CD36-mediated orosensory perception of long-chain fatty acids in the mouse

    FASEB J.

    (2008)
  • A.J. Oliveira-Maia

    Nicotine activates TRPM5-dependent and independent taste pathways

    Proc. Natl. Acad. Sci. U. S. A.

    (2009)
  • V. Lyall

    The mammalian amiloride-insensitive non-specific salt taste receptor is a vanilloid receptor-1 variant

    J. Physiol.

    (2004)
  • T.R. Clapp

    Mouse taste cells with G protein-coupled taste receptors lack voltage-gated calcium channels and SNAP-25

    BMC Biol.

    (2006)
  • Y.J. Huang

    The role of pannexin 1 hemichannels in ATP release and cell–cell communication in mouse taste buds

    Proc. Natl. Acad. Sci. U. S. A.

    (2007)
  • R.A. Romanov

    Voltage dependence of ATP secretion in mammalian taste cells

    J. Gen. Physiol.

    (2008)
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