ReviewGustatory processing is dynamic and distributed
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
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