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Cover ArticleArticles, Systems/Circuits

Spatiotemporal Coding of Individual Chemicals by the Gustatory System

Sam Reiter, Chelsey Campillo Rodriguez, Kui Sun and Mark Stopfer
Journal of Neuroscience 2 September 2015, 35 (35) 12309-12321; DOI: https://doi.org/10.1523/JNEUROSCI.3802-14.2015
Sam Reiter
1National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland 20892, and
2Department of Neuroscience, Brown University, Providence, Rhode Island 02912
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Chelsey Campillo Rodriguez
1National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland 20892, and
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Kui Sun
1National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland 20892, and
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Mark Stopfer
1National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland 20892, and
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Abstract

Four of the five major sensory systems (vision, olfaction, somatosensation, and audition) are thought to use different but partially overlapping sets of neurons to form unique representations of vast numbers of stimuli. The only exception is gustation, which is thought to represent only small numbers of basic taste categories. However, using new methods for delivering tastant chemicals and making electrophysiological recordings from the tractable gustatory system of the moth Manduca sexta, we found chemical-specific information is as follows: (1) initially encoded in the population of gustatory receptor neurons as broadly distributed spatiotemporal patterns of activity; (2) dramatically integrated and temporally transformed as it propagates to monosynaptically connected second-order neurons; and (3) observed in tastant-specific behavior. Our results are consistent with an emerging view of the gustatory system: rather than constructing basic taste categories, it uses a spatiotemporal population code to generate unique neural representations of individual tastant chemicals.

SIGNIFICANCE STATEMENT Our results provide a new view of taste processing. Using a new, relatively simple model system and a new set of techniques to deliver taste stimuli and to examine gustatory receptor neurons and their immediate followers, we found no evidence for labeled line connectivity, or basic taste categories such as sweet, salty, bitter, and sour. Rather, individual tastant chemicals are represented as patterns of spiking activity distributed across populations of receptor neurons. These representations are transformed substantially as multiple types of receptor neurons converge upon follower neurons, leading to a combinatorial coding format that uniquely, rapidly, and efficiently represents individual taste chemicals. Finally, we found that the information content of these neurons can drive tastant-specific behavior.

  • neural coding
  • taste
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The Journal of Neuroscience: 35 (35)
Journal of Neuroscience
Vol. 35, Issue 35
2 Sep 2015
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Spatiotemporal Coding of Individual Chemicals by the Gustatory System
Sam Reiter, Chelsey Campillo Rodriguez, Kui Sun, Mark Stopfer
Journal of Neuroscience 2 September 2015, 35 (35) 12309-12321; DOI: 10.1523/JNEUROSCI.3802-14.2015

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Spatiotemporal Coding of Individual Chemicals by the Gustatory System
Sam Reiter, Chelsey Campillo Rodriguez, Kui Sun, Mark Stopfer
Journal of Neuroscience 2 September 2015, 35 (35) 12309-12321; DOI: 10.1523/JNEUROSCI.3802-14.2015
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  • neural coding
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