Developmental decrease in size of peripheral receptive fields of single chorda tympani nerve fibers and relation to increasing NaCl taste sensitivity

Nagai, Takatoshi; Mistretta, Charlotte M.; Bradley, Robert M.

doi:10.1523/jneurosci.08-01-00064.1988

Cited by 50 publications

(73 citation statements)

References 21 publications

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“…In cats, single geniculate ganglion cells responded to electrical stimulation of single buds in only one-fifth of tested neurons; fourfifths responded to two to five nearby buds (Boudreau et al, 1971). More recently, a similar result was obtained in sheep using more refined methods (Nagai et al, 1988). Thus, species differences in the selectivity of bud innervation by single ganglion cells seem likely.…”

Section: Bud Units In Mousesupporting

confidence: 63%

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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Section: Bud Units In Mousesupporting

confidence: 63%

Discrete Innervation of Murine Taste Buds by Peripheral Taste Neurons

Zaidi¹,

Whitehead²

2006

J. Neurosci.

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“…In developing sheep, there is a selective pruning of receptive fields for neurons that become responsive to sodium stimuli, while the receptive fields of other neuron types remain relatively large. 47 These data are important not only from a developmental framework (because they reveal structure/function relationships between taste receptors and afferent neurons during gustatory development), but also because they strongly suggest that such relationships may be modifiable through environmental factors. Such studies await examination.…”

Section: Plasticity Of Neuron/target Matchingmentioning

confidence: 99%

Neural Plasticity in the Gustatory System

Hill¹

2004

Nut. Rev.

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Sensory systems adapt to changing environmental influences by coordinated alterations in structure and function. These alterations are referred to as plastic changes. The gustatory system displays numerous plastic changes even in receptor cells. This review focuses on the plasticity of gustatory structures through the first synaptic relay in the brain. Unlike other sensory systems, there is a remarkable amount of environmentally induced changes in these peripheral-most neural structures. The most consistent and largest changes occur to stimuli that also impact on homeostatic systems, especially when the environmental manipulation is instituted during early development.

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“…The simplest description of the relationship between an afferent fiber of a GG/CT and the fungiform papillae that it innervates is that the axon travels to the tongue and then divides to innervate from one to eight fungiform papillae, forming a complex taste end organ. However, a number of investigators have demonstrated that characteristics of fungiform receptive field innervation are highly complex Nagai et al 1988). …”

Section: Receptive Field Characteristics Of Gg/ct Neuronsmentioning

confidence: 99%

“…In fact, it has been known for some time that, like finger mechanoreceptors, single CT afferent fibers terminate in fungiform taste buds that are organized in receptive fields. Investigators using rat (Miller 1971), cat (Boudreau et al 1971;Oakley 1975;Robinson 1988), goat (Boudreau et al 1985) and sheep (Nagai et al 1988) have shown that CT fiber receptive fields vary in size, ranging from 1 to 13 papillae. However, prior investigators have concentrated on the responses of GG neurons to chemical stimulation of the anterior tongue and omitted comprehensive study of the basic neurobiological properties of the GG neurons that include receptive field size, associated CT fiber properties and responses to nongustatory stimuli.…”

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confidence: 99%

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Receptive field size, chemical and thermal responses, and fiber conduction velocity of rat chorda tympani geniculate ganglion neurons

Yokota

Bradley

2016

Journal of Neurophysiology

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Yokota Y, Bradley RM. Receptive field size, chemical and thermal responses, and fiber conduction velocity of rat chorda tympani geniculate ganglion neurons. J Neurophysiol 115: 3062-3072, 2016. First published March 30, 2016 doi:10.1152/jn.00045.2016.-Afferent chorda tympani (CT) fibers innervating taste and somatosensory receptors in fungiform papillae have neuron cell bodies in the geniculate ganglion (GG). The GG/CT fibers branch in the tongue to innervate taste buds in several fungiform papillae. To investigate receptive field characteristics of GG/CT neurons, we recorded extracellular responses from GG cells to application of chemical and thermal stimuli. Receptive field size was mapped by electrical stimulation of individual fungiform papillae. Response latency to electrical stimulation was used to determine fiber conduction velocity. Responses of GG neurons to lingual application of stimuli representing four taste qualities, and water at 4°C, were used to classify neuron response properties. Neurons classified as SALT, responding only to NaCl and NH 4 Cl, had a mean receptive field size of six papillae. Neurons classified as OTHER responded to salts and other chemical stimuli and had smaller mean receptive fields of four papillae. Neurons that responded to salts and cold stimuli, classified as SALT/ THERMAL, and neurons responding to salts, other chemical stimuli and cold, classified as OTHER/THERMAL, had mean receptive field sizes of six and five papillae, respectively. Neurons responding only to cold stimuli, categorized as THERMAL, had receptive fields of one to two papillae located at the tongue tip. Based on conduction velocity most of the neurons were classified as C fibers. Neurons with large receptive fields had higher conduction velocities than neurons with small receptive fields. These results demonstrate that GG neurons can be distinguished by receptive field size, response properties and afferent fiber conduction velocity derived from convergent input of multiple taste organs. taste; taste bud; geniculate ganglion; chemosensory; chorda tympani PRIMARY AFFERENT NEURONS OF the chorda tympani nerve (CT) convey information to the central nervous system about sensory properties of food. CT fibers have cell bodies in the geniculate ganglion (GG) and respond to chemical, thermal and mechanical properties of oral stimuli (Finger et al. 2005;Fishman 1957;Kumari et al. 2015). Despite the obvious importance of their neurobiological and sensory roles, there is no comprehensive understanding of the full nature of the basic biology of GG neurons. As one example of the lack of information about GG/CT neuron biology, consider how primary afferents conveying skin sensation have been classified based on their peripheral targets (cutaneous, articular and visceral afferents), conduction velocity (afferent axon size and myelination), response properties (sensory modality and intensity thresholds) and neurochemical phenotype (such as peptide expression) (Lawson 2002;Le Pichon and Chesler 2014;McMahon and Priestley...

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Developmental decrease in size of peripheral receptive fields of single chorda tympani nerve fibers and relation to increasing NaCl taste sensitivity

Cited by 50 publications

References 21 publications

Discrete Innervation of Murine Taste Buds by Peripheral Taste Neurons

Discrete Innervation of Murine Taste Buds by Peripheral Taste Neurons

Neural Plasticity in the Gustatory System

Receptive field size, chemical and thermal responses, and fiber conduction velocity of rat chorda tympani geniculate ganglion neurons

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