Topographic organization of Fos-like immunoreactivity in the rostral nucleus of the solitary tract evoked by gustatory stimulation with sucrose and quinine

doi:10.1016/0006-8993(95)01410-1

Brain Research

Volume 711, Issues 1–2, 4 March 1996, Pages 125-137

https://doi.org/10.1016/0006-8993(95)01410-1 Get rights and content

Abstract

Fos immunohistochemistry was used to elucidate the pattern of activation elicited by two qualitatively and hedonically distinct taste stimuli, sucrose and quinine, within the first-order gustatory relay, the rostral division of the nucleus of the solitary tract. Compared to unstimulated controls, both sucrose and quinine elicited significant increases in Fos-like immunoreactivity in the rostral central subnucleus, the region of the rostral solitary nucleus that receives the densest primary afferent input. Within the rostral central subnucleus, neurons that exhibited Fos-like immunoreactivity following quinine stimulation were concentrated medially, but neurons that exhibited Fos-like immunoreactivity following sucrose stimulation were distributed more evenly along the mediolateral axis. Despite their differential distribution, sucrose- and quinine-activated neurons also demonstrated notable intermingling. Further, the chemotopic arrangement was only partially consistent with what would be predicted if chemotopy was merely an outcome of orotopy. Our results suggest that a rough chemotopy characterizes the organization of taste responses in the nucleus of the solitary tract, and that the topographic pattern of taste afferent terminations in this nucleus is related to their chemosensitivity as well as to their peripheral spatial distribution.

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Citation Excerpt :
It is important to consider that only a subset of active neurons are labelled using this technique (Dragunow and Faull, 1989), so the number of Fos-IR neurons reported undoubtedly is lower than the total number activated by each treatment and therefore some potential differences caused by the treatments may have been missed. Although the concentrations of tastants used in the current study were similar to those used in previous work (DiNardo and Travers, 1997; Harrer and Travers, 1996; King et al., 1999; Travers, 2002) and have been shown to elicit TR behaviors and Fos expression in the gustatory system (Harrer and Travers, 1996; Spector et al., 1988; Tokita et al., 2007), differences in concentration could significantly influence the results. To address this issue, both relatively low and high concentrations of NaCl and sucrose were used in the current study.
The location of neurons in the gustatory cortex (GC) activated by intra-oral infusion of solutions in conscious rats was mapped using Fos immunohistochemistry. Groups of adult male Wistar rats (N's = 5) received an infusion of one of the following: dH₂O, 0.1 or 1.0 M NaCl, 0.1 or 1.0 M sucrose, 0.32 M MSG (with 100 µM amiloride and 2.5 M inosine 5′-monophosphate), 0.03 M HCl, or 0.003 M QHCl delivered via an intra-oral cannula (0.233 ml/min for 5 min). Unstimulated control rats received no infusion. Taste reactivity (TR) behaviors were videotaped and scored. The number of Fos-immunoreactive (Fos-IR) neurons was counted in eight sections throughout the anterior-posterior extent of the GC in the medial and lateral halves of the granular (GI), dysgranular (DI), and dorsal (AID) and ventral (AIV) agranular insular cortices. Intra-oral infusion of dH₂O, NaCl, or sucrose altered the number of Fos-IR neurons in only specific subareas of the GC and the effects of these tastants were concentration-dependent. For example, 1.0 M NaCl increased Fos-IR neurons in the posterior lateral AID and DI and elicited more aversive TR responses than 0.1 M NaCl. Compared to dH₂O, infusions of HCl or QHCl increased the total number of Fos-IR neurons in many subareas of the GC throughout its anterior-posterior extent and increased aversive TR behaviors. Linear regression analyses suggested that neurons in the medial AID of the posterior GC may influence aversive behavioral responses to HCl and QHCl while neurons in the posterior lateral AID and DI may play a role in aversive TR responses to 1.0 M NaCl.
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Zinc deficiency causes various symptoms including taste disorders. In the present study, changes in expression of c-Fos immunoreactivity in neurons of the parabrachial nucleus (PBN), one of the relay nuclei for transmission of gustatory information, after bitter stimulation to the dorsal surface of the tongue were examined in zinc-deficient rats. Experimental zinc-deficient animals were created by feeding a low-zinc diet for 4 weeks, and showed the following symptoms of zinc deficiency: low body weight, low serum zinc content and behavioral changes to avoid bitter stimulation. In normal control animals, intraoral application of 1 mM quinine caused increased numbers of c-Fos-immunoreactive (c-Fos-IR) neurons in the external lateral subnucleus and external medial subnucleus of the PBN (elPBN and emPBN, respectively) compared with application of distilled water. However, in the zinc-deficient animals, the numbers of c-Fos-IR neurons in the elPBN and emPBN did not differ significantly between application of quinine and distilled water. After feeding the zinc-deficient animals a normal diet for 4 weeks, the symptoms of zinc deficiency recovered, and the expression of c-Fos-IR neurons following intraoral bitter stimulation became identical to that in the normal control animals. The present results indicate that dietary zinc deficiency causes alterations to neuronal activities in the gustatory neural circuit, and that these neuronal alterations can be reversed by changing to a normal diet.
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This type of topography, which has also been referred to as “chemotopy” (Travers, 1993) or “gustotopy” (Chen et al., 2011), has been most extensively investigated in the NST, the first-order brain taste center. In line with previous rat studies (Harrer and Travers, 1996; Travers, 2002), QHCl stimulation evoked c-Fos expression in the medial third of the rostral part of the nucleus in inbred and transgenic mice (Travers et al., 2007). Recently, NaCl and MSG have also been shown to elicit distinctive c-Fos expression in this nucleus in wild-type mice (Stratford and Finger, 2011).
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Topographic organization of Fos-like immunoreactivity in the rostral nucleus of the solitary tract evoked by gustatory stimulation with sucrose and quinine

Abstract

J. Auton. Neru. Syst.

J. Neurosci. Meth.

Brain Res.

Brain Res.

Brain Res.

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Neurosci. Lett.

J. Auton. Nerv. Syst.

Neurosci. Lett.

Neurosci.

Trends Neurosci.

Mol. Cell. Neurosci.

Brain Res.

Mol. Brain Res.

Physiol. Behau.

Brain Res.

Brain Res.

Brain Res.

Brain Res.

Brain Res.

Brain Res.

Brain Res.

Physiol. Behav.

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J. Comp. Neurol.

Recovery of taste-induced expression of c fos in the CNS after peripheral nerve crush and regeneration

Soc. Neurosci. Abstr.

Efferent projections of electrophysiologically identified regions of the rostral nucleus of the solitary tract in the rat

Expression ofc-fos-like protein as a marker for neuronal activity following noxious stimulation in the rat

J. Comp. Neurol.

Learning to sham feed: behavioral adjustments to loss of physiological postingestional stimuli

Am. J. Physiol.

Topographic distribution of taste responsiveness in the hamster medulla

Chem. Senses

Sensorimotor mapping and oropharyngeal reflexes in goldfish,Carassius auratus

Brain, Behau. Evol.

An analysis of hamster afferent taste nerve response functions

J. Gen. Physiol.

Taste-responsive neurons of the glossopharyngeal nerve of the rat

J. Neurophysiol.

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J. Neurophysiol.

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Am. J. Physiol.

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Ann. NY Acad. Sci.

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Am. J. Physiol.

Chemotopic coding for sucrose and quinine hydrochloride in the nucleus of the fasciculus solitarius, Olfaction and Taste II