Trends in Neurosciences
ReviewCoding in the mammalian gustatory system
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
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