Altered temperature and taste responses from cross-regenerated sensory nerves in the rat's tongue

1. The chorda tympani nerve, which innervates the front of the rat tongue, was found to be much less responsive to tongue cooling than the IXth nerve, which innervates the back of the tongue. The two nerves also differed in their relative responsiveness to various taste chemicals.

2. Through cross-union the IXth nerve was made to innervate the front of the tongue, and in other rats the chorda tympani nerve the back of the tongue.

3. After an average of 15 post-operative weeks, electrophysiological recordings of whole nerve action potential discharges were made from normal, control regenerated, and cross-regenerated nerves. Cooling, and chemical and mechanical stimulation of the tongue demonstrated that the control regenerated and cross-regenerated nerves had established functional connexions.

4. Neither the response to cooling nor the relative taste responses were altered by either of two types of control chorda tympani nerve regeneration.

5. In contrast, the cross-regenerated chorda increased its responsiveness to tongue cooling and the cross-regenerated IXthe nerve lost much of its responsiveness to cooling.

6. Cross-regeneration also caused the relative taste responses to change and appear quite similar to the responses obtained from the nerve which normally innervated that tongue region (e.g. the cross-regenerated IXth nerve responded like a chorda tympani nerve).

7. It is suggested that the sensory response evoked in the chorda tympani and IXth nerves by tongue cooling or taste stimulation is at least partially dependent upon the character of the tongue tissue in which the nerve terminates—the epithelium at the front differs from that at the back of the rat tongue.

8. These results rule out the following two hypotheses: (a) that the nerve ending itself functions as a taste receptor in direct contact with applied chemicals and yet is uninfluenced by the character of the tissue in which it terminates, (b) that assuming the taste bud cells are an integral part of the receptive process, the taste nerve ending determines the chemical specificity of the taste cell which it induces, without any previous modification of the nerve by the tissue in which it terminates.

     

Chorda tympani and lingual nerve responses to astringent compounds in rodents.

A wide variety of compounds in foods and beverages produce astringent sensations when introduced into the oral cavity. There is controversy, however, whether "astringency," with its associated puckering and drying sensations, is a fundamental taste quality or is a tactile sensation. To address this issue, electrophysiological recordings were made from the gerbil chorda tympani nerve and the rat lingual nerve. The chorda tympani nerve transmits taste information from the anterior 2/3 of the tongue, whereas the lingual nerve transmits tactile, thermal and pain sensations from the anterior 2/3 of the tongue. The astringent compounds tested were: tannic acid, tartaric acid, gallic acid, aluminum ammonium sulfate and aluminum potassium sulfate. Tannic acid, tartaric acid, and gallic acids were tested at concentrations up to 120 mM over a pH range from approximately 2 to 6. The aluminum salts were tested at concentrations up to 160 mM only at low pH's. All compounds rapidly (and at lower concentrations, reversibly) stimulate the chorda tympani nerve in a concentration-dependent manner at all pH's tested. The rapidity and reversibility of the chorda tympani responses suggest that astringent-tasting compounds interact directly with taste cells rather than indirectly by precipitating salivary proteins. At pH 6, tannic acid, tartaric acid, and gallic acid all elicit robust chorda tympani responses, implying that the ionized forms of these compounds produce taste sensations. None of these compounds stimulate lingual nerves over the same concentration and pH ranges used in the chorda tympani experiments.(ABSTRACT TRUNCATED AT 250 WORDS)     

Distribution of taste and general sensory nerve endings in fungiform papillae of the hamster

Sensory endings of chorda tympani and lingual (trigeminal) nerve fibers were identified by selective denervation and localized within specific regions of fungiform pipillae in the hamster. The chorda tympani was resected from the middle ear and the peripheral fibers were allowed to degenerate for 1, 3, or 8 days prior to perfusion-fixation and electron-microscopic examination of the anterior tongue. Taste buds were virtually devoid of intact nerves by 3 days following chorda tympani denervation. Remnants of the fibers were restricted to taste buds. Lingual fibers, on the other hand, persist in normal numbers after chorda tympani resection and populate perigemmal areas of connective tissue and extragemmal areas located apically in the squamous, nontaste epithelium surrounding the taste bud. This study provides evidence of a segregation of chorda tympani fibers in the taste bud and lingual nerve fibers in the apical fungiform papilla. The lingual nerve-epithelial arrangement and superficial location, near the least cornified area of the tongue, may be well suited for relatively sensitive somatosensation, possibly mechanoreception. Thus, the apical fungiform papilla appears to be a site where both taste and tactile oral stimuli interact with receptors.     

Taste placodes are primary targets of geniculate but not trigeminal sensory axons in mouse developing tongue

Tongue embryonic taste buds begin to differentiate before the onset of gustatory papilla formation in murine. In light of this previous finding, we sought to reexamine the developing sensory innervation as it extends toward the lingual epithelium between E 11.5 and 14.5. Nerve tracings with fluorescent lipophilic dyes followed by confocal microscope examination were used to study the terminal branching of chorda tympani and lingual nerves. At E11.5, we confirmed that the chorda tympani nerve provided for most of the nerve branching in the tongue swellings. At E12.5, we show that the lingual nerve contribution to the overall innervation of the lingual swellings increased to the extent that its ramifications matched those of the chorda tympani nerve. At E13.0, the chorda tympani nerve terminal arborizations appeared more complex than those of the lingual nerve. While the chorda tympani nerve terminal branching appeared close to the lingual epithelium that of the trigeminal nerve remained rather confined to the subepithelial mesenchymal tissue. At E13.5, chorda tympani nerve terminals projected specifically to an ordered set of loci on the tongue dorsum corresponding to the epithelial placodes. In contrast, the lingual nerve terminals remained subepithelial with no branches directed towards the placodes. At E14.5, chorda tympani nerve filopodia first entered the apical epithelium of the developing fungiform papilla. The results suggest that there may be no significant delay between the differentiation of embryonic taste buds and their initial innervation.     

The role of sucrose-sensitive neurons in ingestion of sweet stimuli by hamsters

The relationship between sweet preference and activity in sucrose-sensitive chorda tympani nerve fibers was investigated in hamsters (Mesocricetus auratus). Without exception, hamsters increased consumption of aqueous solutions of nonsweet 0.1 M NaCl, 0.001 M quinine-HCl, 0.01 M citric acid, 0.001 M dithiothreitol, 0.01 M pyridine, 0.01 M 2-phenylethanol, 0.005 M i-amyl acetate, 0.01 M vanillin, half-saturated 1-menthol and 0.033 mM capsaicin if they were made sweet by adding 0.5 M sucrose. Since sucrose activates chorda tympani S fibers, activity in these nerve fibers may be sufficient for increased preference. To determine if S-fiber activity is necessary for preference, equally preferred sweet stimuli were presented to the tongue while recording responses of single chorda tympani fibers. S fibers were clearly activated by 0.03 M sucrose, 0.001 M Na saccharin, 0.01 M D-phenylalanine, 0.1 M glycine, 0.005 M dulcin and 0.03 M Na 2-mercaptoethanesulfonate but not by 0.01 M Ca cyclamate and 0.003 M Na 3-nitrobenzenesulfonate. Ca cyclamate weakly activated H fibers and Na 3-nitrobenzenesulfonate weakly activated N fibers. Thus, S-fiber chorda tympani activity may be sufficient but not necessary for sweet preference, which may be influenced by activity in fibers of other taste nerves.     

Two distinct projection areas from tongue nerves in the frontal operculum of macaque monkeys as revealed with evoked potential mapping

Projection areas in the cerebral cortex from tongue nerves were investigated in anesthetized macaque monkeys (Macaca fuscata). Three tongue nerves (lingual nerve, chorda tympani, and a lingual branch of the glossopharyngeal nerve) were electrically stimulated and thereby evoked mass field potentials were recorded with microelectrodes roving through the exposed and buried frontal operculum. Two distinct tongue nerve projection areas were thus located; one in the lower part of the precentral gyrus ventral to the inferior precentral sulcus, and the other in the medial part of the buried frontal operculum. The former corresponds to the "cortical masticatory area", previously defined in macaque monkeys as involved in somatic sensation as well as mastication. However, the prominent projection from the chorda tympani and glossopharyngeal nerve branch, containing taste fibers, to this area suggests its involvement in taste sensation. The latter corresponds to the "pure gustatory area" defined in squirrel monkeys in both location and cytoarchitecture. However, projection to this area from the lingual nerve, which contains only somatic nerve fibers, suggests its involvement in somatic sensation, as well.     

The sweet taste in the calf. I. Chorda tympani proper nerve responses to taste stimulation of the tongue

Electrophysiological recordings were obtained from the chorda tympani nerve in calves during stimulation with NaCl, quinine hydrochloride, citric acid, acesulfan-K, aspartame, fructose, galactose, glucose, glycine, lactose, maltose, monellin, Na-saccharin, sucrose, thaumatin, and xylitol. In cattle the chorda tympani innervates the posterior third of the tongue as well as the anterior part. It was found that the posterior receptive field generally responded better to sweet substances than the anterior. Glycine and Na-saccharin followed by xylitol were the most effective sweet stimuli. The monosaccharides elicited larger responses than the disaccharides. Aspartame gave a weak nerve response in 5 of 13 calves. Monellin and thaumatin elicited no change in chorda tympani nerve activity and did not crossadapt with any sweetener. No effects on citric acid responses were observed after application of miraculin.     

Convergence of excitatory inputs from the chorda tympani, glossopharyngeal and vagus nerves onto superior salivatory nucleus neurons in the cat

Superior salivatory nucleus (SSN) neurons were identified by antidromic spike responses to stimulation of the chorda tympani nerve, and were tested to stimulation of the ipsilateral chorda tympani, glossopharyngeal, vagus and lingual nerves in urethane-chloralose anesthetized cats. In 48 SSN neurons identified, 33 (69%) responded with spikes to stimulation of at least one of these nerves, and 24 (50%) were excited with inputs from more than one stimulated nerve. The mean latencies of the reflex responses to stimulation of the chorda tympani, glossopharyngeal, vagus or lingual nerve were 13.2, 18.9, 24.6 or 11.4 ms, respectively.     

Possible involvement of undissociated acid molecules in the acid response of the chorda tympani nerve of the rat

To test whether undissociated acid is capable of exciting the chorda tympani nerves in rats, we have used buffered acid solutions as taste stimuli. These solutions were prepared by adding alkali to weak acids, such as acetic acid, so that the proportion of undissociated and dissociated acids was varied whereas keeping the total acid concentration constant. When acetic acid solutions, adjusted to wide ranges of pH by NaOH, were applied to the tongue, the response magnitude of the chorda tympani nerves was not varied systematically with pH changes. However, if the sodium effect was eliminated by amiloride or replacement of cation by potassium or Tris[hydroxymethyl]aminomethane; NH(2)C(CH(2)OH)(3) (Tris-base), the chorda tympani response was reduced systematically as pH increased. Similar results were obtained with citric acid and ascorbic acid. This pH-dependent change in taste nerve response to acid cannot be solely attributed to the proton gradient because the response magnitude induced by hydrogen itself, which was estimated from responses to strong acids, was much smaller than that by equi-pH acetic acid ( approximately 85%). Thus we cannot explain the pH-dependent responses of the chorda tympani nerves to weak acids unless effects of undissociated acid molecules are postulated. It is therefore concluded that undissociated acids in weak acid solutions can be a stimulant to taste receptor cells.     

Weight changes of the submandibular glands in the rat resulting from denervation

In the lingual nerve of the rat, the number of myelinated fibers ranged from 3,215 to 3,744, with diameters ranging from 0.7 to 9.7 μ. The nerves were unimodal with a peak at 2–3 or 3–4 μ. In the chorda tympani, the number of myelinated fibers ranged from 444 to 538, with diameters ranging from 1.1 to 8.7 μ. The nerves were unimodal with a peak at 1–3 μ. Sixteen days after section of the lingual, chordalingual (the lingual nerve distal to the union with chorda tympani) and chorda tympani nerves as well as intracranial section of the facial nerve, significant weight losses were recorded for the submandibular and retrolingual glands. The greatest weight losses occurred after intracranial section of the facial nerve or section of the chordalingual nerve (retrolingual glands lost 42 and 39%, submandibular glands lost 20 and 28% respectively). Intracranial section of the facial nerve demonstrates that the degree of weight loss is correlated with the number of myelinated fibers (1–3 μ diameter) which degenerate, and that the weight loss is not the result of operative damage to the vascular supply of the glands.     

The gustatory sense in foetal sheep during the last third of gestation

1. Histological studies revealed that presumptive taste buds are present in the foetal sheep tongue at 50 days. By 100 days the taste buds appear morphologically mature.2. To determine if foetal taste buds are functional, electrophysiological recordings were made of activity in the chorda tympani nerve of sheep foetuses. Single and multi-fibre preparations were studied in foetuses aged 100 days to term.3. Responses were recorded to lingual stimulation with salts, acids, glycerol, glycine, sodium saccharin, quinine HCl and amniotic fluid. Responses of the foetal chorda tympani to lingual stimulation with a series of monochloride salts and with increasing concentrations of one salt were similar to responses recorded in lambs and adults.4. The peripheral gustatory system of the foetal sheep is functional for at least the last third of gestation. Foetal taste experiences may influence the formation of adult taste preferences or may aid the foetus in monitoring its environment.     

The Linguo-Chorda Tympani Reflex—an Electrophysiologically Undescribed Reflex

The impulse activity in the central part of the chorda tympani nerve of the rat was recorded during mechanical stimulation of the oral region. The results obtained at a stimulation rate of 1 Hz show that a) a reflex discharge could be recorded about 6–10 ms after stimulation of the ipsilateral side of the tongue, b) stimulation of the contralateral side increased the latency by about 1–1.5 ms, c) the reflex could be evoked in animals which showed no spontaneous efferent activity in the chorda tympani nerve, d) recordings from nerve filaments showed that a filament could display spontaneous activity without being involved in the reflex, e) the lingual nerve serves as the main sensory link on the reflex to mechanical stimulation of the anterior part of the tongue, and f) the reflex evoked by stimulation of other parts of the oral region had a longer latency and less intense discharge. The results obtained at higher stimulation rate show that a) individual bursts of reflex discharge could be traced at stimulation frequencies up to 60 Hz, b) except for a moderate decrease the discharge did not disappear when stimulus frequencies of 5, 30 and 50 Hz were used.     

Sensitivity of the rat gustatory system to the rate of stimulus onset.

Responses of the rat chorda tympani nerve were obtained to stimulation of the tongue with both linearly rising anodal current of varying intensity and rate of rise and NaCl presented at different concentrations and rates of flow. The amplitude of the transient portion of the integrated chorda tympani response was a power function of the rate of current rise. The duration of the transient response paralleled the rising phase of the current and the neural response fell to a tonic level proportional to current intensity when the rising current reached its plateau. Anodal currents of different final intensities but presented at the same rate of rise produced transient responses of the same amplitude. Responses of single chorda tympani fibers exhibited the same phasic and tonic components that were characteristic of the whole nerve. When NaCl was presented to the tongue at different rates of flow, the chorda tympani response reflected a sensitivity to stimulus onset rate paralleling that shown to linearly rising current.     

The Effect of Stomach Distension on the Efferent Activity in the Chorda Tympani Nerve of the Rat

The efferent activity in the chorda tympani nerve of the rat was recorded under neuroleptic analgesia. The results show that this activity decreased when the stomach was distended. The effects caused originated from the stomach and diminished after cutting the vagal nerves. It is suggested that the efferent activity of the chorda tympani nerve can be influenced by hunger and satiety.     

Taste reception in the goat, sheep and calf

1. The goat, sheep and calf have gustatory chemoreceptors which respond to salt, sweet, sour and bitter solutions, from which the afferent fibres pass centrally in the chorda tympani and glossopharyngeal nerves.2. Action potentials in the afferent gustatory nerves can also be detected when the tongue is irrigated with sodium bicarbonate, ethylene glycol, glycerine, and saccharine.3. Distilled water reduces the background activity in the isolated gustatory nerves, thus demonstrating the absence of fibres in ruminant ungulates of receptors which respond to stimulation by distilled water.4. The responses from the chemoreceptors, associated especially with the circumvallate papillae, are enhanced if the papillae are gently moved at the time of irrigation with sapid solutions.5. The chorda tympani is most responsive to salt and acid solutions while the glossopharyngeal is more responsive to sugars, quinine and acid.     

Facial nerve parasympathetic preganglionic afferents to the accessory otic ganglia by way of the chorda tympani nerve in the cat

 The distribution of accessory otic ganglia and connections between the ganglia and the chorda tympani nerve were investigated in the cat in order to determine the parasympathetic preganglionic facial nerve afferents to the otic ganglia using whole mount acetylthiocholinesterase (WATChE) histochemistry. The otic ganglia consist of a sigle main prominent ganglion and many small accessory ganglia lying on a plexus around the origins of the branches of the mandibular nerve and near the junction of the chorda tympani nerve and lingual nerve. In cell analysis of Nissl-stained preparations, the neurons composing the accessory otic ganglia were morphologically similar to the main otic ganglion neurons. Connecting branches from the chorda tympani nerve to the peripherally located acccessory otic ganglia were found and they were not stained by WATChE histochemistry. WATChE-positive connecting branches from the ganglia to the inferior alveolar, lingual, and mylohyoid nerves were also found in the same preparations. The WATChE histochemistry on various autonomic nervous tissues revealed that autonomic postganglionic nerve fibers are selectively stained darkly and that preganglionic fibers remain unstained. Therefore, it is considered that the WATChE-negative connections from the chordra tympani nerve consist chiefly of autonomic preganglionic fibers, whereas the WATChE-positive connections to the branches of the mandibular nerve are mainly postganglionic fibers. This suggests that some of the facial nerve parasympathetic preganglionic fibers in the chorda tympani nerve are mediated in the accessory otic ganglia and then join the branches of the mandibular nerve to supply the target mandibular tissues. Accepted: 25 November 1997     

Multiple sensitivity of chorda tympani fibres of the rat and hamster to gustatory and thermal stimuli

1. Impulse discharges in single chorda tympani fibres of rats and hamsters in response to gustatory stimuli representing the four basic qualities of taste as well as to cooling and warming of the tongue were recorded.2. In both rats and hamsters many fibres responded to more than one kind of gustatory stimulus as well as to thermal ones. The thermal sensitivity of these fibres was found to be about -0.5 impulses/sec. degrees C for cooling and 0.5 impulses/sec. degrees C for warming.3. Statistical calculations of the frequency of responses of chorda tympani fibres to single gustatory stimuli or combinations of stimuli were made, assuming that responsiveness to any one stimulus is independent of that to other stimuli. Evidence for relatively specific sensitivity to a particular stimulus or a particular combination of stimuli was obtained in the rat and the hamster.4. Across-fibre correlation coefficients between the amounts of responses to a pair of stimuli were calculated. In both the rat and the hamster, significant positive correlations were obtained with HCl, quinine and cooling. In addition, a positive correlation between sucrose and warming and a negative correlation between sucrose and NaCl were obtained in the hamster. The results are discussed in relation to the interaction of gustatory and thermal sensations of the human tongue.     

Neonatal chorda tympani transection permanently disrupts fungiform taste bud and papilla structure in the rat

The present report examined the morphology of fungiform papillae in adult rats that received bilateral chorda tympani transection at 10 days of age. Tongue tissue was examined using surface-structure analysis. Counts were made of fungiform papillae with a pore, fungiform papillae with no pore and fungiform papillae with a keratinized conical surface; a feature referred to as "filiform-like. " Neonatal chorda tympani nerve transection resulted not only in a loss of taste buds but also in a permanent loss in numbers of fungiform papillae. Compared with an average of 152 fungiform papillae in sham-operated control rats, there was an average of only 54 fungiform papillae after neonatal chorda tympani transection. Nearly 80% of these fungiform papillae in neonatal chorda tympani transected rats were filiform-like. No filiform-like papillae were noted in sham-operated rats. These results suggest that the chorda tympani nerve is necessary during an early postnatal period of development to maintain normal fungiform papillae morphology.     

Anatomy of the lingual nerve: Application to oral surgery

The purpose of this research is to obtain morphological information about the traveling route, branching pattern, and distribution within the tongue of the lingual nerve, all of which are important for oral surgical procedures. Using 20 sides from 10 Japanese cadaveric heads, we followed the lingual nerve from its merging point with the chorda tympani to its peripheral terminal in the tongue. We focused on the collateral branches in the area before reaching the tongue and the communication between the lingual and hypoglossal nerves reaching the tongue. The collateral branches of the lingual nerve were distributed in the oral mucosa between the palatoglossal arch and the mandibular molar region. Two to eight collateral branches arose from the main trunk of the nerve, and the configuration of branching was classified into three types. More distally, the lingual nerve started to communicate with the hypoglossal nerve before passing the anterior border of the hyoglossus muscle. Nerve communications were also found in the main body and near the apex of the tongue. A thorough understanding of the collateral branches near the tongue, and the communication with the hypoglossal nerve inside the tongue, will help to prevent functional disorders from local anesthesia and oral surgical procedures associated with the lingual nerve. Clin. Anat. 32:635–641, 2019. © 2019 Wiley Periodicals, Inc.     

The nature of the substance P-containing nerve fibres in taste papillae of the rat tongue

The nature of the association of substance P (SP) with taste buds in the rat tongue was investigated by immunohistochemical and radioimmunoassay techniques. Both the circumvallate and fungiform papillae were found to receive a rich innervation by substance P-containing fibres. Although these fibres were closely associated with the taste buds in these structures, they assumed a perigemmal rather than an intragemmal location. Bilateral lesions of the glossopharyngeal nerve resulted in the depletion of taste buds from the vallate papilla and a large reduction in substance P immunoreactive fibres in this area. Lesions of the chorda tympani, which led to the degeneration of taste buds in fungiform papillae, had no effect on the immunohistochemical appearance of substance P in these papilla or on the substance P levels in the anterior part of the tongue. Lesions of the mandibular division of the trigeminal nerve or neonatal capsaicin treatment had no effect on the structural integrity of taste buds in fungiform papillae but led to the depletion of substance P-immunoreactive fibres from these papillae. Both of these procedures caused a 71% reduction in the substance P content of the anterior tongue, ipsilaterally after the nerve lesion and bilaterally after capsaicin treatment. The results are discussed in relation to the possible functional role of substance P-containing fibres within nerves supplying taste structures of the tongue.