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Although the temporal characteristics of neural responses have been proposed as a mechanism for sensory neural coding, there has been little evidence thus far that this type of information is actually used by the nervous system. Here the authors show that patterned electrical pulses trains that mimic the response to the taste of quinine can produce a bitterlike sensation when delivered to the nucleus tractus solitarius of behaving rats. Following conditioned aversion training using either 'quinine simulation' patterns of electrical stimulation or natural quinine (0.1 mM) as a conditioned stimulus, rats specifically generalized the aversion to 2 bitter tastants: quinine and urea. Randomization of the quinine simulation patterns resulted in generalization patterns that resembled those to a perithreshold concentration (0.01 mM) of quinine. These data provide strong evidence that the temporal pattern of brainstem activity may convey information about taste quality and underscore the functional significance of temporal coding. Keywords: taste, temporal coding, nucleus of the solitary tract, conditioned taste aversion, electrical brain stimulation

Two experiments suggested that the temporal pattern of a taste response in the brain can convey meaningful information. In Experiment 1, rats avoided lick-contingent electrical stimulation of the nucleus of the solitary tract (NTS; the first synaptic relay for taste) when the temporal pattern of pulses mimicked the electrophysiological response to quinine, but not when the temporal pattern was randomized. In Experiment 2, rats avoided lick-contingent electrical stimulation of the NTS that mimicked the temporal pattern of a sucrose response following stimulation-illness pairings. This aversion generalized to sucrose but not to the other tastants; extinction of the aversion to electrical stimulation also extinguished the aversion to sucrose. Results replicate and extend previous findings (P. M. Di Lorenzo & G. S. Hecht, 1993).

To investigate the role of temporal coding in the neural processing of taste, trains of electrical pulses of varying frequency were delivered to the nucleus of the solitary tract (NTS) in awake rats. The temporal patterns of these trains mimicked the temporal patterns of electrophysiological responses of single neurons to natural tastes. In Experiment 1, water-deprived rats were first trained to lick water in an experimental chamber. On training days, licking water produced a sucroselike electrical pulse train in the NTS. At the end of these sessions, +experimental animals were made ill by an injection of LiCl and subsequently learned to avoid licking when LiCl was paired with NTS stimulation. In Experiment 2, rats refused to lick water when licking produced a quininelike pattern of NTS stimulation but licked enthusiastically when licking produced a pattern of NTS stimulation similar to the natural response to sucrose.

•Theories of taste coding in the CNS have been those derived from the periphery.•These theories ignore temporal dynamics and breadth of response properties in CNS.•Taste-related structures in CNS are multimodal and are linked to behavior.•Tasting invokes a brainwide shift in firing patterns (states) that identifies taste.•The taste code in CNS is a series of states related to both food and behavior.

Despite evidence for an abundance of inhibitory synaptic processes within the taste-responsive portion of the brain stem, little is known about how these processes are activated or modulated. In this context, this study tested the hypothesis that activation of the chorda tympani nerve (CT) invokes inhibition that influences gustatory neural information processing in the rostral nucleus of the solitary tract (NTS). Stimulating electrodes were implanted in the middle ear of urethane-anesthetized rats to enable the passage of current across the CT. Electrophysiological responses to sucrose, NaCl, HCl, and quinine were recorded from single NTS neurons both individually and immediately following tetanic electrical stimulation of the CT. Additionally, NTS field responses to paired pulse stimulation of the CT were recorded. Electrical pulses delivered to the CT were found to produce a compound action potential with four components. Taste-responsive units in the NTS showed tetanus-evoked responses that varied in latency and strength. Those cells that showed strong, short latency responses to CT stimulation showed large magnitude responses to NaCl and were relatively narrowly tuned. Units with longer latencies generally responded more broadly to taste stimuli and with lower response magnitudes. Following tetanus, taste responses in 20 (43%) of the 46 units were reversibly altered in a stimulus-selective manner. Taste responses in 18 units were both enhanced and attenuated following tetanic stimulation, although attenuation was much more common. Additionally, tetanus was found to affect the temporal organization of spikes within taste responses to one stimulus in seven units (15%), four of which also showed changes in response magnitude to a different stimulus following tetanus. The influence of tetanus on taste responses was shown to be reliable and repeatable in neurons from which stimulus trials were recorded more than once. Across all units, responses to quinine were most dramatically and frequently attenuated following tetanus, while those to NaCl were least susceptible to change. NTS field responses evoked by paired pulse stimulation of the CT suggested that the initial pulse evoked an inhibitory influence in the NTS that decayed and returned to baseline by 2 s. These data are consistent with the idea that afferent input to the NTS normally activates inhibitory synaptic activity. As with other sensory systems, such inhibition may serve to facilitate contrast in the neural representation of different stimulus qualities.

The hypothesis that sodium channels, located on taste receptors, enhance taste detection by adding noise to the neural signals generated by taste stimuli was tested in two behavioral experiments. Generalization of a conditioned taste aversion was used to assess detection of low concentrations of sucrose. Results showed that detection of a perithreshold concentration of sucrose was selectively disrupted by amiloride, a sodium channel blocker, and by novobiocin, a sodium channel enhancer. These data support the idea that detection of taste stimuli at threshold depends on the presence of an ideal level of noise. Further, this noise may be provided by stimulation of sodium channels.