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The neural mechanisms of gustation: a distributed processing code

Nature Reviews Neuroscience volume 7, pages 890–901 (2006)Cite this article

Abstract

Whenever food is placed in the mouth, taste receptors are stimulated. Simultaneously, different types of sensory fibre that monitor several food attributes such as texture, temperature and odour are activated. Here, we evaluate taste and oral somatosensory peripheral transduction mechanisms as well as the multi-sensory integrative functions of the central pathways that support the complex sensations that we usually associate with gustation. On the basis of recent experimental data, we argue that these brain circuits make use of distributed ensemble codes that represent the sensory and post-ingestive properties of tastants.

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Figure 1: Schematic diagram of a taste bud, taste receptor cell and associated neurons.
Figure 2: Salt intake is explained by input from both gustatory and trigeminal nerves.
Figure 3: Anatomical overview of the central taste pathways.
Figure 4: Ensemble activity of OFC neurons discriminates and anticipates natural rewards.
Figure 5: Taste processing in the gustatory cortex is fast.
Figure 6: Functional MRI shows multimodal integration in the human taste cortex.
Figure 7: Coding of satiety states by neuronal ensembles in the rat forebrain.

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Acknowledgements

This work was supported in part by grants from the National Institutes of Health, from Philip Morris Inc. USA and Philip Morris International.

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Authors and Affiliations

  1. Departments of Neurobiology and Anesthesiology,

    Sidney A. Simon

  2. Duke University, Durham, 27710, North Carolina, USA

    Sidney A. Simon

  3. Department of Neurobiology and the Center for Neuroengineering,

    Ivan E. de Araujo

  4. Duke University, Durham, 27710, North Carolina, USA

    Ivan E. de Araujo

  5. Department of Neurobiology,

    Ranier Gutierrez

  6. Duke University, Durham, 27710, North Carolina, USA

    Ranier Gutierrez

  7. the Departments of Neurobiology, Biomedical Engineering and Psychological and Brain Science, Duke University, Durham, 27710, North Carolina, USA

    Miguel A. L. Nicolelis

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  1. Sidney A. Simon
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  4. Miguel A. L. Nicolelis
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Glossary

Amiloride

A potassium-sparing diuretic that inhibits epithelial sodium channels (ENaCs) in the kidney and in taste receptor cells.

Carbonic anhydrase

Family of zinc-containing enzymes that catalyse the rapid interconversion of carbon dioxide and water into protons and bicarbonate ions.

Cholecystokinin

(CCK). A peptide hormone secreted from the mucosal epithelial cells in the small intestine (duodenum) that causes the release of digestive enzymes from the pancreas. Peripheral and central administration of CCK reduces appetite.

Chorda tympani nerve

Branch of cranial nerve VII that innervates the front two-thirds of the tongue and carries taste information to the brain.

Conditioned taste aversion

(CTA). This is a one-trial form of learning that occurs when a palatable tastant becomes aversive after pairing with gastric malaise.

ENaC/Deg

Epithelial sodium channel (ENaC)/degenerin (Deg) is a superfamily of ion channels involved in epithelial Na+ transport, mechanotransduction and neurotransmission.

Forebrain

The anterior portion of the brain that includes the telencephalon and the diencephalon. It contains the cerebral cortex, the thalamus and the hypothalamus.

Gap junction

A junction between two cells consisting of pores that allow the passage of molecules (up to 1 kDa).

Glossopharyngeal nerve

Cranial nerve IX, receiving sensory fibres from the posterior one-third of the tongue, the tonsils and the pharynx.

Greater superior petrosal nerve

Branch of cranial nerve VII that innervates the back of the tongue and palate.

Gustducin

A G protein that is almost exclusively expressed in taste cells.

Neuropeptide Y

(NPY). A member of the pancreatic polypeptide hormone family, this peptide is produced and released by cell groups located in the hypothalamic arcuate nucleus. Central administration of NPY increases food intake and metabolism.

Purinergic receptors

These receptors are ion channels that are activated by ATP.

Sensory-specific satiety

Term referring to a specific reduction in the reward value of a particular food that has been eaten until satiety.

Superior laryngeal branch

Nerve that arises from the inferior vagal ganglion inferior to the pharyngeal branch of the vagus nerve.

Temporal coding models

These models propose that information on taste identity and quality is encoded in the temporal structure of spike trains.

TRPM5

A cation channel member of the transient receptor potential superfamily (subfamily M, member 5). Regulation of TRPM5 by Ca2+ could mediate transduction in taste receptor cells. It is required for the normal transduction of sweet, bitter and umami tastes.

Umami

A Japanese word used to describe the fifth primary taste. It corresponds to the savoury taste of food as produced, for example, by monosodium glutamate. Umami taste is found in vegetables, fish, meats and cheese.

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Simon, S., de Araujo, I., Gutierrez, R. et al. The neural mechanisms of gustation: a distributed processing code. Nat Rev Neurosci 7, 890–901 (2006). https://doi.org/10.1038/nrn2006

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