Coding of gustatory information by single cells in the nucleus of the solitary tract of the awake, voluntarily licking rat

An increasing body of experimental evidence shows that forebrain taste responses in awake animals are processed over long periods of time (>1 sec) in spatially and temporally dynamic networks spanning multiple brain regions. However, very little is known about the taste responses of awake, voluntarily consuming animals in the nucleus of the solitary tract (NTS), which houses the obligatory first synapse of the ascending gustatory pathway in the central nervous system and is reciprocally connected with several higher gustatory nuclei. To investigate taste coding in unanesthetized animals, we chronically implanted microelectrodes into the NTS of male, Sprague -Dawley rats and recorded electrophysiological single-cell responses as animals sampled exemplars of the five basic taste qualities (sweet, sour, salty, bitter and umami) and distilled water. Animals were free to move about during testing sessions and all stimuli were delivered when the animal voluntarily licked a sip tube. Responses to between 39 and 175 presentations of each taste quality over a single lick, as well as between 4 and 39 blocks of consecutive deliveries of each taste quality, were recorded in 47 isolated taste-responsive units. Nearly all units responded to more than a single taste quality. The latency of taste responses varied widely; some responses appeared very rapidly following a single reinforced lick (some under 20 ms) but the majority did not appear until much later, around 1 s or later. The majority of taste cells showed some degree of entrainment with the animals' licks, at ∼ 7 Hz. Firing patterns were analyzed using metric space analysis (see Dilorenzo and Victor 2003) to determine the time period over which each unit conveyed the most gustatory information. Across units, the number expressing maximal information increased steadily to a plateau at ∼1.75 to ∼2.25 s. Electrophysiological and behavioral evidence from other studies suggests that the distributed gustatory system as a whole evaluates the significance of gustatory cues over an interval exceeding a single second, even if a stimulus is only presented over a single lick. The present data demonstrate that voluntarily consuming a substance profoundly alters the structure of the neural response it evokes in the NTS. Similarities between the responses observed in the present study and those reported in forebrain nuclei indicate that network activity throughout the brain may play a fundamental role in NTS taste processing.