Spatiotemporal Coding of Individual Chemicals by the Gustatory System.
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.


CONCLUSIONS
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.
National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland 20892, and Department of Neuroscience, Brown University, Providence, Rhode Island 02912.
Sam
http://orcid.org/0000-0001-6879-663X
S
Reiter
National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland 20892, and.
Chelsey
C
Campillo Rodriguez
National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland 20892, and.
Kui
http://orcid.org/0000-0002-5430-1664
K
Sun
National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland 20892, and stopferm@mail.nih.gov.
Mark
http://orcid.org/0000-0001-9200-1884
M
Stopfer
D000200:Action Potentials / Q000502:physiology; D000344:Afferent Pathways / Q000502:physiology; D000818:Animals; D002628:Chemoreceptor Cells / Q000502:physiology* / Q000648:ultrastructure; D004305:Dose-Response Relationship, Drug; D004594:Electrophysiology; D005260:Female; D008297:Male; D018402:Manduca; D008855:Microscopy, Electron, Scanning; D011930:Reaction Time / Q000502:physiology; D012679:Sense Organs / Q000166:cytology*; D012965:Sodium Chloride / Q000494:pharmacology; D013268:Stimulation, Chemical; D013395:Sucrose / Q000494:pharmacology; D013569:Synapses / Q000502:physiology* / Q000648:ultrastructure; D013649:Taste / Q000502:physiology*; D013997:Time Factors
D012965:Sodium Chloride; D013395:Sucrose
neural coding; taste