Topographic organizations of taste-responsive neurons in the parabrachial nucleus of C57BL/6J mice: An electrophysiological mapping study

Abstract

The activities of 178 taste-responsive neurons were recorded extracellularly from the parabrachial nucleus (PbN) in the anesthetized C57BL/6J mouse. Taste stimuli included those representative of 5 basic taste qualities, sweet, salty, sour, bitter and umami. Umami synergism was represented by all sucrose-best and sweet-sensitive sodium chloride-best neurons. Mediolaterally the PbN was divided into medial, brachium conjunctivum (BC) and lateral subdivisions while rostrocaudally the PbN was divided into rostral and caudal subdivisions for mapping and reconstruction of recording sites. Neurons in the medial and BC subdivisions had a significantly greater magnitude of response to sucrose and to the mixture of monopotassium glutamate and inosine monophosphate than those found in the lateral subdivision. In contrast, neurons in the lateral subdivision possessed a more robust response to quinine hydrochloride. Rostrocaudally no difference was found in the mean magnitude of response. Analysis on the distribution pattern of neuron types classified by their best stimulus revealed that the proportion of neuron types in the medial vs. lateral and BC vs. lateral subdivisions was significantly different, with a greater amount of sucrose-best neurons found medially and within the BC, and a greater amount of sodium chloride-, citric acid- and quinine hydrochloride-best neurons found laterally. There was no significant difference in the neuron type distribution between rostral and caudal PbN. We also assessed breadth of tuning in these neurons by calculating entropy (H) and noise-to-signal (N/S) ratio. Mean N/S ratio of all neurons (0.43) was significantly lower than that of H value (0.64). Neurons in the caudal PbN had a significantly higher H value than in the rostral PbN. In contrast, mean N/S ratio were not different both mediolaterally and rostrocaudally. These results suggest that although there is overlap in taste quality representation in the mouse PbN, taste-responsive neurons still possessed a topographic organization.

5‐HT3A‐driven green fluorescent protein delineates gustatory fibers innervating sour‐responsive taste cells: A labeled line for sour taste?

“…In summary, our results are consistent with a tendency for regional segregation of taste quality information within nTS, the primary sensory relay nucleus for taste. Taken together with the reports of quality‐segregation of responses within other levels of the taste neuroaxis (Chen et al, ; Tokita & Boughter, ), our results are consonant with a loosely represented version of the “labeled line” hypothesis of taste coding, that is, that dedicated chains of neurons convey information about a specific taste quality: sour, sweet, bitter, and so forth. Nonetheless, many other studies report that quality representation of taste is less specific depending on stimulus concentration (Wu et al, ), or plastic depending on behavioral or past experience of the animal (e.g., Accolla, Bathellier, Petersen, & Carleton, ; Accolla & Carleton, ).…”

Overlapping Representation of Primary Tastes in a Defined Region of the Gustatory Cortex

“…It must be emphasized, however, that, in these previous rat mapping studies, any such biasing at the extremes corresponded to a gradation of numbers of particular best-taste cell types rather than discrete and absolute spatial clustering (Yamamoto et al, 1985b;Accolla et al, 2007). This is similar to the way that taste qualities are organized in other central gustatory areas (Travers and Norgren, 1995;Geran and Travers, 2006;Yokota et al, 2011;Tokita and Boughter, 2016). In any case, our results point to the likelihood that significant taste responses, including to acids, are found across GC, including in between any more quality-specific regions.…”

“…Antigen expression, including c-Fos, was assessed using standard immunohistochemical procedures, with a rabbit polyclonal anti-cFos antibody (sc-52, Santa Cruz Biotechnology, RRID:AB_10609634); M2-type muscarinic acetylcholine receptors were labeled using a rat monoclonal anti-M2 antibody (MAB 367, Millipore, RRID:AB_94952). Primary antibody labeling was visualized with either fluorescent or nonfluorescent secondary antibodies (Savchenko and Boughter, 2011;Tokita et al, 2014; see our previous papers for detailed methods). Microscope sections were imaged using either a Leica DMRXA2 microscope equipped with a digital camera and imaging software or with a confocal microscope (Zeiss 710).…”

“…These data were not analyzed in a quantitative manner. Sample sizes were chosen to approximate those used in our previous studies of brainstem anatomy and taste-evoked Fos expression (Tokita et al, 2009(Tokita et al, , 2014Savchenko et al, 2011). Eight C57BL/6J mice (all male) were used for the licking behavior test (one was removed during the test for failure to lick water during the training sessions, leaving a final n ϭ 7).…”

“…such as entropy or N/S ratio; in these experiments, overall mean entropy was 0.40 Ϯ 0.01 and the N/S ratio was 0.38 Ϯ 0.01 (SEM); both of these values support a preponderance of narrowly tuned cells in GC. Studies of taste brainstem physiology in C57BL/6J mice reveal a greater degree of broad tuning: Higher entropy (0.73) for the nucleus of the solitary tract and higher entropy (0.64) and N/S (0.43) values for the parabrachial nucleus (Lemon and Margolskee, 2009;Tokita and Boughter, 2016). There does not appear to be greater convergence of taste quality information into individual cells in the cortex versus lower areas.…”