Temporal Characteristics of Gustatory Responses in Rat Parabrachial Neurons Vary by Stimulus and Chemosensitive Neuron Type

Abstract

It has been demonstrated that temporal features of spike trains can increase the amount of information available for gustatory processing. However, the nature of these temporal characteristics and their relationship to different taste qualities and neuron types are not well-defined. The present study analyzed the time course of taste responses from parabrachial (PBN) neurons elicited by multiple applications of “sweet” (sucrose), “salty” (NaCl), “sour” (citric acid), and “bitter” (quinine and cycloheximide) stimuli in an acute preparation. Time course varied significantly by taste stimulus and best-stimulus classification. Across neurons, the ensemble code for the three electrolytes was similar initially but quinine diverged from NaCl and acid during the second 500ms of stimulation and all four qualities became distinct just after 1s. This temporal evolution was reflected in significantly broader tuning during the initial response. Metric space analyses of quality discrimination by individual neurons showed that increases in information (H) afforded by temporal factors was usually explained by differences in rate envelope, which had a greater impact during the initial 2s (22.5% increase in H) compared to the later response (9.5%). Moreover, timing had a differential impact according to cell type, with between-quality discrimination in neurons activated maximally by NaCl or citric acid most affected. Timing was also found to dramatically improve within-quality discrimination (80% increase in H) in neurons that responded optimally to bitter stimuli (B-best). Spikes from B-best neurons were also more likely to occur in bursts. These findings suggest that among PBN taste neurons, time-dependent increases in mutual information can arise from stimulus- and neuron-specific differences in response envelope during the initial dynamic period. A stable rate code predominates in later epochs.

Taste Quality Decoding Parallels Taste Sensations

“…Our findings are in line with previous electrophysiological studies in rodents indicating that neuronal response patterns along the gustatory processing pathway, including the nucleus of the solitary tract [26], parabrachial nucleus [27], and gustatory . This classifier was then tested by using it to discriminate taste Y at all time points (testing time t y ).…”

Electrophysiological responses to sugars and amino acids in the nucleus of the solitary tract of type 1 taste receptor double-knockout mice

“…When possible, we repeated stimulations. If the cell remained viable after testing chemosensitivity, the receptive field location was assessed as described in Geran and Travers (2013) and Travers (2006, 2009). Briefly, using the operating microscope, we used a small paintbrush or a precision applicator brush (S379; Parkell, Inc.) to apply a taste mixture to different receptor subpopulations.…”

Bursting by taste-responsive cells in the rodent brain stem

“…where k ϭ a scaling constant, which is 1.661 for four stimuli, and p i ϭ the proportion of the neuron's response devoted to any one stimulus; and 2) a noise-to-signal ratio, which equaled the second largest response size to a basic stimulus divided by the size of the largest response (Geran and Travers 2013). Both measures have a maximum of 1, which would occur for an extremely nonselective neuron, and lower values represent greater specificity in responding.…”

“…Rat and hamster chorda tympani neurons have been reported to fire in bursts only in response to sweeteners (Mistretta 1972;Ogawa et al 1974), and bursting has been associated preferentially with responses to quinine in the rat PBN (Geran and Travers 2013). We focused primarily on bursting in the absence of taste stimulation, but we also looked at ISI distributions during responses to taste stimuli, which we found to be similar to ones during spontaneous firing for a given NST neuron.…”

“…Fujiwara et al (2007) described bursting neurons in the gustatory cortex of rats but did not look at the relationships between bursting during spontaneous activity and taste-evoked response profiles. In addition, several investigators have examined bursting in terms of its contribution to taste-evoked activity and found that bursts occurred primarily during responses to compounds with a particular taste quality (Geran and Travers 2013;Mistretta 1972;Ogawa et al 1974;Travers and Norgren 1989).…”