Review
Gustatory processing is dynamic and distributed

https://doi.org/10.1016/S0959-4388(02)00341-0Get rights and content

Abstract

The process of gustatory coding consists of neural responses that provide information about the quantity and quality of food, its generalized sensation, its hedonic value, and whether it should be swallowed. Many of the models presently used to analyze gustatory signals are static in that they use the average neural firing rate as a measure of activity and are unimodal in the sense they are thought to only involve chemosensory information. We have recently elaborated upon a dynamic model of gustatory coding that involves interactions between neurons in single as well as in spatially separate, gustatory and somatosensory regions. We propose that the specifics of gustatory responses grow not only out of information ascending from taste receptor cells, but also from the cycling of information around a massively interconnected system.

Introduction

The gustatory system has evolved to detect and discriminate between foods, to select nutritious diets, and to initiate, sustain and terminate ingestion [1]. These processes evolve over several seconds and involve the integration of multiple sources of information. In this review, we discuss the neural system that underlies taste behaviors, focusing particularly on the time-varying nature of taste neural responses and the neural interactions that may give rise to such time-varying responses. First, we explain how the convergence of distributed pathways throughout the gustatory neural circuitry leads to dynamic responses. Next, we show that the currently debated static models of taste coding cannot account for the dynamic and interactive aspects of gustatory neural processing. Finally, we present recent data confirming that gustation is dynamic and distributed, and argue that these data require a more general systemic theory of gustatory coding.

Section snippets

Functional anatomy of the gustatory system

Fig. 1a shows a schematic diagram of the principle gustatory pathways 2., 3.. Transduction of chemical information occurs in the oral cavity when chemicals make contact with taste receptor cells 4••., 5••.. Primary gustatory neurons course within the CNS cranial nerves VII, IX and X [6] to the nucleus of the solitary tract (NST), which in turn transmits information to the parabrachial nuclei of the pons (PbN). From the brainstem, taste information is transmitted to the thalamocortical system,

Currently debated models of taste coding are static and noninteractive

The long-standing debate over the nature of gustatory neural coding has primarily addressed the question ‘Are taste stimuli coded by labeled lines (LL), by across-fiber patterns (AFP), or by some combination of the two?’ Discussions of these models focus on whether dedicated sets of neurons signal the presence of a particular taste component, or whether tastes are represented in the ‘landscape’ of responses across an entire neural population (see [3]). Both of these models have admirably

Time-varying gustatory responses

Dynamic properties have recently been recognized in the responses of neurons in several sensory systems, including some, such as gustation, in which responses had previously been described in terms of a single value 17••., 18., 19.. The investigation of the role of time in gustatory responses dates back to the recognition that the firing rates of primary gustatory neurons peak and then decrease as the system adapts to prolonged application of gustatory stimuli 20., 21., 22.. By the early 1980s,

Interactions in gustatory responses: I. Within-area interactions

Over the past decade, interactive processing within neural populations (typically measured as peaks in cross-correlograms or cross-spectra for pairs of neurons) has received serious consideration as a potential mechanism of neural coding. Much of the attention paid to interactive neural processing has been directed towards the search for functionally significant patterns of ‘synchrony’, that is the near-simultaneous (timescale of 1–10 ms) firing of individual action potentials between neurons.

Interactions in gustatory responses: II. Between-region interactions

In addition to interactions within single areas, interactions between regions also modulate taste responses (see also [39]). Indeed, recent evidence showed that feedback connections between GC and NST modulate NST activity via both excitatory pathways and GABAergic synapses [40•]. Fig. 4c shows an example of a GC–NST interaction. It is clear that cortical activation (electrical stimulation) may excite or inhibit NST activity, and that infusion of bicuculline in the NST blocks the inhibitory

Interactions in gustatory responses: III. Input from other systems

Early electrophysiological studies reported converging projections from gustatory and lingual somatosensory origins in several relays of the gustatory pathway, especially at the cortical level, where somatosensory and taste responses are found in intermingled cells or even within the same cells 2., 42., 43.. In this regard, it may not be so surprising to learn that mechanically stimulating the tongue can produce ‘taste phantoms’ [44] and that temperature changes on the tongue can induce or

Conclusions

We have attempted to justify the reasons for moving beyond static and unimodal models of gustatory coding towards models in which processing occurs in time, is multimodal and involves interactions between neurons in the same and in spatially separate gustatory regions. We propose that the specifics of gustatory responses grow not only out of information ascending from taste receptor cells but rather from the cycling of information around a massively interconnected system.

Acknowledgements

We are grateful to Robert Erickson for many fruitful discussions of data and theory. We also acknowledge support from NIH grants DC-00403 (DBK), DC-01065 (SAS), and DE-11121 (MALN), and by Philip Morris Incorporated.

References and recommended reading

Papers of particular interest, published within the annual period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

References (52)

  • M. Bazhenov et al.

    Model of cellular and network mechanisms for odor-evoked temporal patterning in the locust antennal lobe

    Neuron

    (2001)
  • M. Bazhenov et al.

    Model of transient oscillatory synchronization in the locust antennal lobe

    Neuron

    (2001)
  • H. Ogawa et al.

    GABAergic inhibition and modifications of taste responses in the cortical taste area in rats

    Neurosci Res

    (1998)
  • P.M. Di Lorenzo et al.

    Transfer of information about taste from the nucleus of the solitary tract to the parabrachial nucleus of the pons

    Brain Res

    (1997)
  • D.V. Smith et al.

    GABA-mediated corticofugal inhibition of taste-responsive neurons in the nucleus of the solitary tract

    Brain Res

    (2000)
  • T. Yamamoto et al.

    Cortical neurons responding to tactile, thermal and taste stimulations of the rat's tongue

    Brain Res

    (1981)
  • J. Todrank et al.

    A taste illusion: taste sensation localized by touch

    Physiol Behav

    (1991)
  • 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)
  • J.F. Glenn et al.

    Gastric modulation of gustatory afferent activity

    Physiol Behav

    (1976)
  • V.G. Dethier

    A comparative role of taste in food intake: a comparative view

  • T.A. Gilbertson et al.

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

    J Neurosci

    (2001)
  • M.C. Whitehead et al.

    Anatomy of the gustatory system in the hamster: central projections of the chorda tympani and the lingual nerve

    J Comp Neurol

    (1983)
  • E.M. Barnett et al.

    Anterograde tracing of trigeminal afferent pathways from the murine tooth pulp to cortex using herpes simplex virus type 1

    J Neurosci

    (1995)
  • G. Laurent

    A systems perspective on early olfactory coding

    Science

    (1999)
  • A.A. Ghazanfar et al.

    The structure and function of dynamic cortical and thalamic receptive fields

    Cereb Cortex

    (2001)
  • D.L. Ringach et al.

    Dynamics of orientation tuning in macaque primary visual cortex

    Nature

    (1997)
  • Cited by (101)

    • 3.14 - Taste Pathways, Representation and Processing in the Brain

      2020, The Senses: A Comprehensive Reference: Volume 1-7, Second Edition
    • Central taste anatomy and physiology

      2019, Handbook of Clinical Neurology
      Citation Excerpt :

      According to the most extreme view of the labeled-line theory, the same coding strategy applies from the tongue to the cortex (Chen et al., 2011). A second theory, historically rooted in the across-neuron pattern theory (Erickson, 1963), postulates that taste qualities are encoded by the combined and dynamic activity of large ensembles of neurons (Katz et al., 2002). Each taste quality can engage the same group of neurons but evokes different patterns of activity.

    View all citing articles on Scopus
    View full text