Taste-responsive neurons and their locations in the solitary nucleus of the hamster

McPheeters, Martha; Hettinger, Thomas P.; Nuding, Sarah C.; Savoy, Lawrence; Whitehead, Mark C.; Frank, Marion E.

doi:10.1016/0306-4522(90)90179-8

Cited by 64 publications

(29 citation statements)

References 28 publications

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“…6A). In close agreement with the localization of N-best and S-best neurons in the present study, a multiunit recording study in rNST indicated a taste-topic organization in which N-best neurons were localized rostrally whereas S-best and KCl (K)-best neurons were localized caudally in hamsters (HCl was not used) (McPheeters et al 1990). Whether the K-best neurons in that study correspond to the N-best, H-best, or NH-best neurons in the present study remains unknown, although a subset of the N-best (or H-best neurons) have been reported to respond widely to electrolytes including NaCl, HCl, and KCl (Smith et al 1983;St John and Smith 2000).…”

Section: Discussionsupporting

confidence: 90%

Topographical representations of taste response characteristics in the rostral nucleus of the solitary tract in the rat

Yokota

Eguchi

Hiraba

2014

Journal of Neurophysiology

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Yokota T, Eguchi K, Hiraba K. Topographical representations of taste response characteristics in the rostral nucleus of the solitary tract in the rat. J Neurophysiol 111: 182-196, 2014. First published October 16, 2013 doi:10.1152/jn.01031.2012.-The rostral nucleus of the solitary tract (rNST) is the first-order taste relay in rats. This study constructed topographical distributions of taste response characteristics (best-stimulus, response magnitude, and taste-tuning) from spike discharges of single neurons in the rNST. The rNST is divided into four subregions along the rostrocaudal (RC) axis, which include r1-r4. We explored single-neuron activity in r1-r3, using multibarreled glass microelectrodes. NaCl (N)-best neurons were localized to the rostral half of r1-r3, while HCl (H)-best and sucrose (S)-best neurons showed a tendency toward more caudal locations. NaCl and HCl (NH)-best neurons were distributed across r2-r3. The mean RC values and Mahalanobis distance indicated a significant difference between the distributions of N-best and NH-best neurons in which N-best neurons were located more rostrally. The region of large responses to NaCl (net response Ͼ5 spikes/s) overlapped with the distribution of N-best neurons. The region of large responses to HCl extended widely over r1-r3. The region of large responses to sucrose was in the medial part of r2. The excitatory region (Ͼ1 spike/s) for quinine overlapped with that for HCl. Neurons with sharp to moderate tuning were located primarily in r1-r2, while those with broad tuning were located in r2-r3. The robust responses to NaCl in r1-r2 primarily contributed to sharp to moderate taste-tuning. Neurons in r3 tended to have broad tuning, apparently due to small responses to both NaCl and HCl. Therefore, the rNST is spatially organized by neurons with distinct taste response characteristics, suggesting that these neurons serve different functional roles.best-stimulus; response magnitude; taste-tuning; Mahalanobis distance; medulla oblongata THE ROSTRAL NUCLEUS of the solitary tract (rNST), the first-order taste relay, has been reported to receive spatially organized projections on the rostrocaudal (RC) axis from four taste afferents [the chorda tympani (CT), the great superficial petrosal nerve (GSP), the glossopharyngeal nerve (IX), and the superior laryngeal nerves (SL)] in the rat (Contreras et al. 1982;Hamilton and Norgren 1984;Rhoton 1968;Torvik 1956) and the hamster (Whitehead and Frank 1983). However, recent studies have reported overlapping terminal projections from these afferent nerves (Corson et al. 2012;May and Hill 2006). In studies examining the oral receptive field properties of taste-sensitive neurons in the rNST, oral receptive field configurations in the horizontal plane were associated with afferent projections along the RC axis in the rNST (Halpern and Nelson 1965;Sweazey and Smith 1987;Travers and Norgren 1995). Of individual neurons, one-third actually received convergent inputs from the different receptive fields, primarily the anterior ton...

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Section: Discussionsupporting

confidence: 90%

Topographical representations of taste response characteristics in the rostral nucleus of the solitary tract in the rat

Yokota

Eguchi

Hiraba

2014

Journal of Neurophysiology

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“…However, in olfaction, the peripheral receptors are represented centrally, not on the basis of topography, but by the spatial convergence of synapses of neurons expressing specific receptors onto central neurons (Mombaerts et al, 1996;Gao et al, 2000;Vosshall et al, 2000). In taste, attempts to identify a spatial representation of taste receptors or taste qualities have revealed only an indistinct functional topography in the brain (Hamilton and Norgren, 1984;McPheeters et al, 1990). Nevertheless, taste ganglion cells must distribute peripheral fibers to particular receptor cell types and disseminate impulses centrally in a structurally organized manner.…”

Section: Introductionmentioning

confidence: 99%

Discrete Innervation of Murine Taste Buds by Peripheral Taste Neurons

Zaidi¹,

Whitehead²

2006

J. Neurosci.

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The peripheral taste system likely maintains a specific relationship between ganglion cells that signal a particular taste quality and taste bud cells responsive to that quality. We have explored a measure of the receptoneural relationship in the mouse. By injecting single fungiform taste buds with lipophilic retrograde neuroanatomical markers, the number of labeled geniculate ganglion cells innervating single buds on the tongue were identified. We found that three to five ganglion cells innervate a single bud. Injecting neighboring buds with different color markers showed that the buds are primarily innervated by separate populations of geniculate cells (i.e., multiply labeled ganglion cells are rare). In other words, each taste bud is innervated by a population of neurons that only connects with that bud. Palate bud injections revealed a similar, relatively exclusive receptoneural relationship. Injecting buds in different regions of the tongue did not reveal a topographic representation of buds in the geniculate ganglion, despite a stereotyped patterned arrangement of fungiform buds as rows and columns on the tongue. However, ganglion cells innervating the tongue and palate were differentially concentrated in lateral and rostral regions of the ganglion, respectively. The principal finding that small groups of ganglion cells send sensory fibers that converge selectively on a single bud is a new-found measure of specific matching between the two principal cellular elements of the mouse peripheral taste system. Repetition of the experiments in the hamster showed a more divergent innervation of buds in this species. The results indicate that whatever taste quality is signaled by a murine geniculate ganglion neuron, that signal reflects the activity of cells in a single taste bud.

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“…This projection arises from multipolar and elongate rNST neurons mainly located within the rostral central subdivision of rNST (Gill et al 1999; Halsell et al 1996;Whitehead 1990). About 60% of the neurons in the rostral central subdivision can be retrogradely labeled following injection of a neural tracer into the caudal PBN (Whitehead 1990), implying that a major role of the rNST is to convey gustatory information to the PBN, and estimates from electrophysiological data indicate that between 31 and 80% of taste-responsive rNST neurons project to the PBN (Cho et al 2002;McPheeters et al 1990;Monroe and Di Lorenzo 1995). The remaining rNST neurons although responding to chemical stimulation of the tongue have no role in taste perception functioning as the input limb of taste generated oral reflexes such as initiation of salivary secretion and other oral-motor reflexes (reviewed in Bradley and Kim 2006).…”

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Characteristics of Rostral Solitary Tract Nucleus Neurons With Identified Afferent Connections That Project to the Parabrachial Nucleus in Rats

Suwabe

Bradley

2009

Journal of Neurophysiology

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Suwabe T, Bradley RM. Characteristics of rostral solitary tract nucleus neurons with identified afferent connections that project to the parabrachial nucleus in rats. J Neurophysiol 102: 546 -555, 2009. First published May 13, 2009 doi:10.1152/jn.91182.2008. Afferent information derived from oral chemoreceptors is transmitted to second-order neurons in the rostral solitary tract nucleus (rNST) and then relayed to other CNS locations responsible for complex sensory and motor behaviors. Here we investigate the characteristics of rNST neurons sending information rostrally to the parabrachial nucleus (PBN). Afferent connections to these rNST-PBN projection neurons were identified by anterograde labeling of the chorda tympani (CT), glossopharyngeal (IX), and lingual (LV) nerves. We used voltage-and current-clamp recordings in brain slices to characterize the expression of both the transient A-type potassium current, I KA and the hyperpolarization-activated inward current, I h , important determinants of neuronal repetitive discharge characteristics. The majority of rNST-PBN neurons express I KA , and these I KA -expressing neurons predominate in CT and IX terminal fields but were expressed in approximately half of the neurons in the LV field. rNST-PBN neurons expressing I h were evenly distributed among CT, IX and LV terminal fields. However, expression patterns of I KA and I h differed among CT, IX, and LV fields. I KA -expressing neurons frequently coexpress I h in CT and IX terminal fields, whereas neurons in LV terminal field often express only I h . After GABA A receptor block all rNST-PBN neurons responded to afferent stimulation with all-or-none excitatory synaptic responses. rNST-PBN neurons had either multipolar or elongate morphologies and were distributed throughout the rNST, but multipolar neurons were more often encountered in CT and IX terminal fields. No correlation was found between the biophysical and morphological characteristics of the rNST-PBN projection neurons in each terminal field. I N T R O D U C T I O NThe rostral nucleus of the solitary tract (rNST) is the first central relay in the taste pathway (reviewed in Bradley 2006). Sensory information originating from taste buds and other receptors in the oral cavity is relayed to the CNS via afferent nerve fibers of the facial and glossopharyngeal nerves. The central processes of these nerves form the solitary tract (ST), which travels caudally in the brain stem giving off branches that terminate within the rNST (Hamilton and Norgren 1984;May and Hill 2006). The chorda tympani (CT) and greater superficial petrosal branches of the facial nerve innervate the anterior tongue and palate, respectively, and project to the most rostral portions of the nucleus. The terminals of these branches of the facial nerve intermingle within a region of the dorsal rNST just medial to the ST; an area corresponding to rostralcentral and medial rostral-lateral subdivisions (Whitehead 1988). The lingual-tonsilar branch of the glossopharyngeal nerve (IX) transmits senso...

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Taste-responsive neurons and their locations in the solitary nucleus of the hamster

Cited by 64 publications

References 28 publications

Topographical representations of taste response characteristics in the rostral nucleus of the solitary tract in the rat

Topographical representations of taste response characteristics in the rostral nucleus of the solitary tract in the rat

Discrete Innervation of Murine Taste Buds by Peripheral Taste Neurons

Characteristics of Rostral Solitary Tract Nucleus Neurons With Identified Afferent Connections That Project to the Parabrachial Nucleus in Rats

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