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

Abstract

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 NH4Cl, 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.

Keywords: chemosensory; chorda tympani; geniculate ganglion; taste; taste bud.

Fig. 1.

A: dorsal surface of tongue stained with an aqueous solution of methylene blue. The fungiform papillae are apparent as pale staining spots. The papilla-stimulating electrode is indicated in contact with a single papilla. B: standard diagram of the tongue fungiform papillae distribution with a receptive field of 3 papillae innervated by a single GG neuron. C: response of the receptive field to stimulation with 0.5 M NaCl and 1.0 M sucrose. Electrical stimulation identifies the three papillae that constitute the receptive field. Arrowheads and stimulus artifacts indicate the application (solid arrowhead) and removal (open arrowhead) of the electrical stimulation.

Fig. 2.

A: relative receptive field size and location of all receptive fields anterior to the intermolar eminence. B: distribution of the number of receptive fields of different sizes.

Fig. 3.

Recordings from GG neurons to chemical and thermal stimulation of the receptive fields. A, top: neuron responds to stimulation of the receptive field to 0.5 M NaCl, 0.5 M NH₄Cl and 4°C water. The receptive field of this neuron did not respond to stimulation with other chemical stimuli. Middle: electrical stimulation of the fungiform papillae resulted in the identification of a receptive field made up of 8 papillae (b–i). Stimulation of papillae adjacent to this field confirmed the extent of the receptive field of this GG neuron. Bottom: electrical stimulation of 2 μA was used to define the field. Increasing current strength to 3 μA resulted in the same receptive field size. 1 μA was below the threshold to define receptive fields. B, top: neuron responds to 0.5 M NaCl, 0.5 M NH₄Cl, 0.01 N HCl and 0.03 M citric acid, but not to the other stimuli and 4°C water. Middle: electrical stimulation of the fungiform papillae resulted in the identification of a receptive field made up of 4 papillae (c–f). Stimulation of papillae adjacent to this field confirmed the extent of the receptive field of this GG neuron. Bottom: electrical stimulation of 3 μA was used to define the field. Increasing current strength to 4 μA resulted in the same receptive field size. 2 μA was below the threshold to define receptive fields.

Fig. 4.

Recordings from a GG neurons that respond specifically to thermal stimulation of the receptive field. Left: neuron responds to stimulation of the receptive field with 4°C water. The receptive field of this neuron did not respond to stimulation with chemical stimuli. Right, top: electrical stimulation of the fungiform papillae resulted in the identification of a receptive field made up of 2 papillae (c and d). Stimulation of papillae adjacent to this field confirmed the extent of the receptive field of this GG neuron. Right, bottom: electrical stimulation of 2 μA was used to define the field. Increasing current strength to 3 μA resulted in the same receptive field size. 1 μA was below the threshold to define receptive fields.

Fig. 5.

A: chemical and thermal response patterns of single GG neurons. Based on individual response characteristics, the neurons have been categorized. From left to right: SALT neurons respond to NaCl and NH₄Cl; SALT/THERMAL neurons respond to NaCl, NH₄Cl and to 4°C water; OTHER neurons respond to NaCl, NH₄Cl and to HCl and citric acids; OTHER/THERMAL neurons respond to NaCl, NH₄Cl and to HCl and citric acids, as well as 4°C water; and THERMAL respond only to 4°C water. B: arbitrary division of anterior tongue into anterior one-third and anterior two-thirds relative to the intermolar eminence and location of the receptive fields of the GG neuron response categories.

Fig. 6.

Distribution of receptive field size and response category. Except for the THERMAL category, there are no significant differences between receptive field size and response category. **Significant differences (P values < 0.05 or higher) by ANOVA, followed by Bonferroni post hoc tests.

Fig. 7.

A: examples of latency measures (double arrows) and based on time between stimulus artifact (large arrowhead) and the initiation of the first action potential. B: when latency is measured in the same GG neuron to electrical and chemical stimulation, electrical stimulation results in a significantly shorter latency. Values are means ± SE. **P < 0.001 indicates significant difference by paired t-test.

Fig. 8.

A: distribution of conduction velocities calculated from response latency to electrical stimulation of the fungiform papillae. The majority of conduction velocities correspond to published values for C fibers. Only one fiber had a conduction velocity of an Aδ fiber. B: relationship between conduction velocity and receptive field size. GG/CT neurons with faster conduction velocities innervate larger receptive fields of fungiform papillae.