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1.  Making Time Count: Functional Evidence for Temporal Coding of Taste Sensation 
Behavioral neuroscience  2009;123(1):14-25.
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.
doi:10.1037/a0014176
PMCID: PMC3759147  PMID: 19170426
taste; temporal coding; nucleus of the solitary tract; conditioned taste aversion; electrical brain stimulation
2.  Information Processing in the Parabrachial Nucleus of the Pons 
As the second synapse in the central gustatory pathway of the rodent, the parabrachial nucleus of the pons (PbN) receives information about taste stimuli directly from the nucleus of the solitary tract (NTS). Data show that NTS cells amplify taste responses before transmitting taste-related signals to the PbN. NTS cells of varied response profiles send converging input to PbN cells, though input from NTS cells with similar profiles is more effective at driving PbN responses. PbN cells follow NTS input for the first 3 s of taste stimulation for NaCl, HCl, and quinine, but are driven in cyclic bursts throughout the response interval for sucrose. Analyses of the temporal characteristics of NTS and PbN responses show that both structures use temporal coding with equal effectiveness to identify taste quality. Thus, the NTS input to the PbN is comprehensive, in that PbN cells receive NTS input that could support broad sensitivity, systematic, in that the time course of PbN firing patterns depend reliably on the tastant, and efficient, in that information from the NTS is preserved as it is communicated across structures. Comparisons of NTS and PbN taste responses in rats form the basis for our speculation that in primates, where the central gustatory pathway does not synapse in the PbN, the function of the PbN in taste processing may have been incorporated into that of the NTS.
doi:10.1111/j.1749-6632.2009.03903.x
PMCID: PMC3759149  PMID: 19686160
taste; parabrachial pons; temporal coding
3.  Taste Coding in the Nucleus of the Solitary Tract of the Awake, Freely Licking Rat 
It is becoming increasingly clear that the brain processes sensory stimuli differently according to whether they are passively or actively acquired, and these differences can be seen early in the sensory pathway. In the nucleus of the solitary tract (NTS), the first relay in the central gustatory neuraxis, a rich variety of sensory inputs generated by active licking converge. Here we show that taste responses in the NTS reflect these interactions. Experiments consisted of recordings of taste-related activity in the NTS of awake rats as they freely licked exemplars of the five basic taste qualities (sweet, sour, salty, bitter, umami). Nearly all taste-responsive cells were broadly tuned across taste qualities. A subset responded to taste with long latencies (>1.0 s), suggesting the activation of extra-oral chemoreceptors. Analyses of the temporal characteristics of taste responses showed that spike timing conveyed significantly more information than spike count alone in almost half of NTS cells, as in anesthetized rats, but with less information per cell. In addition to taste-responsive cells, the NTS contains cells that synchronize with licks. Since the lick pattern per se can convey information, these cells may collaborate with taste-responsive cells to identify taste quality. Other cells become silent during licking. These latter “anti-lick” cells show a surge in firing rate predicting the beginning and signaling the end of a lick bout. Collectively, the data reveal a complex array of cell types in the NTS, only a portion of which include taste-responsive cells, which work together to acquire sensory information.
doi:10.1523/JNEUROSCI.1856-12.2012
PMCID: PMC3427930  PMID: 22855799
4.  Not so fast: taste stimulus coding time in the rat revisited 
Behavioral and electrophysiological studies suggest that rats can identify a taste stimulus with a single lick, in <200 ms. However, the conditions under which these conclusions were drawn varied widely across experiments. We designed a series of experiments to assess the effects of the number of licks of a tastant that are available, tastant concentration and prior learning experience on the speed with which a tastant can modify behavior. To accomplish this we tested exemplars of four basic taste qualities (quinine, 0.1 mM; NaCl, 100 mM; saccharin, 4 mM, or sucrose, 100 mM; citric acid, 10 mM) in rats that were conditioned to avoid quinine. Taste stimuli were available for one, two, or three licks on separate days. All tastants were presented in a randomized order interspersed with water rinse licks presented on a variable ratio schedule. A tastant-specific significant increase in the proportion of long pauses in licking following quinine presentation was defined as evidence of “behavioral identification.” Rats with aversion training given three licks of all taste stimuli paused significantly more often after quinine by the fourth interlick interval, ~580 ms. Control rats showed no evidence of quinine (0.1 mM) identification. When rats in all conditioning groups were tested with a high concentration of quinine (10 mM), a single lick was sufficient to produce significant pausing after quinine, but not until the fourth interlick interval, i.e., ~580 ms. Testing rats with only two tastants rather than four in a session had no effect on the speed of quinine identification. Present data confirm that a single lick is sufficient for rats to identify a taste stimulus, but that additional licks occur before evidence of identification is apparent. Furthermore, learning, tastant concentration and motivation to drink can all modify the speed of behavioral identification.
doi:10.3389/fnint.2012.00027
PMCID: PMC3364696  PMID: 22666196
taste; identification; behavior; conditioned taste aversion; rat
5.  Two types of inhibitory influences target different groups of taste-responsive cells in the nucleus of the solitary tract of the rat 
Brain research  2009;1275:24-32.
Electrical stimulation of the chorda tympani nerve (CT; innervating taste buds on the rostral tongue) is known to initiate recurrent inhibition in cells in the nucleus of the solitary tract (NTS, the first central relay in the gustatory system). Here, we explored the relationship between inhibitory circuits and the breadth of tuning of taste-responsive NTS neurons. Initially, NTS cells with evoked responses to electrical stimulation of the CT (0.1 ms pulses; 1 Hz) were tested with each of four tastants (0.1 M NaCl, 0.01 M HCl, 0.01 M quinine and 0.5 M sucrose) in separate trials. Next, the CT was electrically stimulated using a paired-pulse (10-2000 ms interpulse interval; blocks of 100 trials) paradigm. Forty-five (30 taste-responsive) of 51 cells with CT-evoked responses (36 taste-responsive) were tested with paired pulses. The majority (34; 75.6%) showed paired-pulse attenuation, defined as fewer evoked spikes in response to the second (test) pulse compared with the first (conditioning) pulse. A bimodal distribution of the peak of paired-pulse attenuation was found with modes at 10 ms and 50 ms in separate groups of cells. Cells with early peak attenuation showed short CT-evoked response latencies and large responses to relatively few taste stimuli. Conversely, cells with late peak attenuation showed long CT-evoked response latencies and small taste responses with less selectivity. Results suggest that the breadth of tuning of an NTS cell may result from the combination of the sensitivities of peripheral nerve inputs and the recurrent influences generated by the circuitry of the NTS.
doi:10.1016/j.brainres.2009.03.069
PMCID: PMC2699607  PMID: 19371730
taste; gustation; chorda tympani nerve; nucleus of the solitary tract; electrical stimulation; inhibition
6.  Quality time: Representation of a multidimensional sensory domain through temporal coding 
Receptive fields of sensory neurons in the brain are usually restricted to a portion of the entire stimulus domain. At all levels of the gustatory neuraxis, however, there are many cells that are broadly tuned, i.e., they respond well to each of the basic taste qualities (sweet, sour, salty and bitter). Although it might seem that this broad tuning precludes a major role for these cells in representing taste space, here we show the opposite – namely, that the tastant-specific temporal aspects (firing rate envelope and spike timing) of their responses enable each cell to represent the entire stimulus domain. Specifically, we recorded the response patterns of cells in the nucleus of the solitary tract (NTS) to representatives of four basic taste qualities and their binary mixtures. We analyzed the temporal aspects of these responses, and used their similarities and differences to construct the taste space represented by each neuron. We found that for the more broadly tuned neurons in the NTS, the taste space is a systematic representation of the entire taste domain. That is, the taste space of these broadly tuned neurons is three-dimensional, with basic taste qualities widely separated and binary mixtures placed close to their components. Further, the way that taste quality is represented by the firing rate envelope is consistent across the population of cells. Thus, the temporal characteristics of responses in the population of NTS neurons, especially those that are more broadly tuned, produce a comprehensive and logical representation of the taste world.
doi:10.1523/JNEUROSCI.5995-08.2009
PMCID: PMC2766857  PMID: 19625513
taste; nucleus of the solitary tract; temporal coding; gustation; electrophysiology; rat
7.  Water as an Independent Taste Modality 
To qualify as a “basic” taste quality or modality, defined as a group of chemicals that taste alike, three empirical benchmarks have commonly been used. The first is that a candidate group of tastants must have a dedicated transduction mechanism in the peripheral nervous system. The second is that the tastants evoke physiological responses in dedicated afferent taste nerves innervating the oropharyngeal cavity. Last, the taste stimuli evoke activity in central gustatory neurons, some of which may respond only to that group of tastants. Here we argue that water may also be an independent taste modality. This argument is based on the identification of a water dedicated transduction mechanism in the peripheral nervous system, water responsive fibers of the peripheral taste nerves and the observation of water responsive neurons in all gustatory regions within the central nervous system. We have described electrophysiological responses from single neurons in nucleus of the solitary tract (NTS) and parabrachial nucleus of the pons, respectively the first two central relay nuclei in the rodent brainstem, to water presented as a taste stimulus in anesthetized rats. Responses to water were in some cases as robust as responses to other taste qualities and sometimes occurred in the absence of responses to other tastants. Both excitatory and inhibitory responses were observed. Also, the temporal features of the water response resembled those of other taste responses. We argue that water may constitute an independent taste modality that is processed by dedicated neural channels at all levels of the gustatory neuraxis. Water-dedicated neurons in the brainstem may constitute key elements in the regulatory system for fluid in the body, i.e., thirst, and as part of the swallowing reflex circuitry.
doi:10.3389/fnins.2010.00175
PMCID: PMC2967336  PMID: 21048894
taste; gustatory; water; nucleus of the solitary tract; parabrachial nucleus of the pons
8.  Variability in responses and temporal coding of tastants of similar quality in the nucleus of the solitary tract of the rat 
Journal of neurophysiology  2007;99(2):644-655.
In the nucleus of the solitary tract (NTS), electrophysiological responses to taste stimuli representing four basic taste qualities (sweet, sour, salty, or bitter) can be often be discriminated by spike count, but, in units for which the number of spikes is variable across identical stimulus presentations, spike timing (i.e., temporal coding) can also support reliable discrimination. The present study examined the contribution of spike count and spike timing to the discrimination of stimuli that evoke the same taste quality but are of different chemical composition. Responses to between 3 and 21 repeated presentations of two pairs of quality-matched tastants were recorded from 38 single cells in the NTS of urethane-anesthetized rats. Temporal coding was assessed in 24 cells, most of which were tested with salty and sour tastants, using an information-theoretic approach (Victor & Purpura, 1996; 1997). Within a given cell, responses to tastants of similar quality were generally closer in magnitude than responses to dissimilar tastants; however, tastants of similar quality often reversed their order of effectiveness across replicate sets of trials. Typically, discrimination between tastants of dissimilar qualities could be made by spike count. Responses to tastants of similar quality typically evoked more similar response magnitudes but were more frequently, and to a proportionally greater degree, distinguishable based upon temporal information. Results showed that nearly every taste-responsive NTS cell has the capacity to generate temporal features in evoked spike trains that can be used to distinguish between stimuli of different qualities and chemical compositions.
doi:10.1152/jn.00920.2007
PMCID: PMC2703738  PMID: 17913985
temporal coding; Nucleus of the solitary tract; taste; gustation
9.  Neural Coding Mechanisms for Flow Rate in Taste-Responsive Cells in the Nucleus of the Solitary Tract of the Rat 
Journal of neurophysiology  2006;97(2):1857-1861.
When a taste stimulus enters the mouth, intentional movement of the stimulus within the oropharyngeal cavity affects the rate at which taste receptors are exposed to the stimulus and may ultimately affect taste perception. Early studies have shown that stimulus flow rate, the experimental equivalent of the effects of these investigative movements, modulates the portion of the peripheral nerve response that occurs when behavioral assessments of tastants are made. The present experiment studied the neural coding mechanisms for flow rate in the nucleus of the solitary tract (NTS), the first central relay in the taste pathway. Responses to NaCl (0.1 M) presented at high (5 ml/s) and low (3 ml/s) flow rates, sucrose (0.5 M), quinine HCl (0.01 M), and HCl (0.01 M) were recorded extracellularly from single NTS units in multiple replications. Information conveyed by evoked responses was analyzed with a family of metrics that quantify the similarity of two spike trains in terms of spike count and spike timing. Information about flow rate was conveyed by spike timing and spike count in approximately equal proportions of units (each ∼1/3), whereas information about taste quality was conveyed by spike timing in about half of the units. Different subsets of units contributed information for discrimination of flow rate and taste quality.
doi:10.1152/jn.00910.2006
PMCID: PMC2659613  PMID: 17182909

Results 1-9 (9)