Suzanne I. Sollars

Taste responses in the greater superficial petrosal nerve: Substantial sodium salt and amiloride sensitivities demonstrated in two rat strains.

A great quantity of research has focused on neural responses of the chorda tympani nerve (CT) to taste stimuli. This report examined salt and sugar sensitivity of the greater superficial petrosal nerve (GSP) and the effect of amiloride on these neural responses. In addition to Sprague-Dawley (SD) rats that have CT responses typical of most rat strains, we included Fischer 344 (F344) rats whose CT responses to sodium chloride (NaCl) are higher than those of other strains. After a stimulation series in which water served as the rinse, a series of stimuli was presented in 100 microM amiloride. The GSP was highly responsive to NaCl, sodium acetate (NaAc), ammonium chloride, and sucrose; NaCl and NaAc responses were strongly suppressed by amiloride. Relative responses to NaCl were significantly higher in F344 than in SD rats. In summary, the GSP is highly sensitive to salt and sugar stimulation, and palatal taste receptors have a considerable degree of amiloride sensitivity.

In vivo recordings from rat geniculate ganglia: taste response properties of individual greater superficial petrosal and chorda tympani neurones

Coding of gustatory information is complex and unique among sensory systems; information is received by multiple receptor populations located throughout the oral cavity and carried to a single central relay by four separate nerves. The geniculate ganglion is the location of the somata of two of these nerves, the greater superficial petrosal (GSP) and the chorda tympani (CT). The GSP innervates taste buds on the palate and the CT innervates taste buds on the anterior tongue. To obtain requisite taste response profiles of GSP neurones, we recorded neurophysiological responses to taste stimuli of individual geniculate ganglion neurones in vivo in the rat and compared them to those from the CT. GSP neurones had a distinct pattern of responding compared to CT neurones. For example, a small subset of GSP neurones had high response frequencies to sucrose stimulation, whereas no CT neurones had high response frequencies to sucrose. In contrast, NaCl elicited high response frequencies in a small subset of CT neurones and elicited moderate response frequencies in a relatively large proportion of GSP neurones. The robust whole‐nerve response to sucrose in the GSP may be attributable to relatively few, narrowly tuned neurones, whereas the response to NaCl in the GSP may relate to proportionately more, widely tuned neurones. These results demonstrate the diversity in the initial stages of sensory coding for two separate gustatory nerves involved in the ingestion or rejection of taste solutions, and may have implications for central coding of gustatory quality and concentration as well as coding of information used in controlling energy, fluid and electrolyte homeostasis.

The CS-US interval and taste aversion learning: a brief look.

Temporal parameters of taste aversion learning are known to differ markedly from other learning paradigms in that acquisition occurs despite lengthy delays between exposure to conditioned (CS) and unconditioned stimulus (US). Far less consideration has been paid to very brief CS-US intervals and the possibility that this learning may also be distinguished by an ineffectiveness of close temporal contiguity between CS and US. The effectiveness of a very brief CS-US interval (10 s) was compared with that of 2 lengthier intervals (15 and 30 min). Temporal control of CS delivery (0.15% saccharin solution) into the oral cavity and US delivery (7.5 mg/kg apomorphine hydrochloride) into circulation involved infusion pumps and indwelling catheters. Using a 1-trial learning paradigm, CS-US delays of 15 and 30 min led to significant aversions whereas the 10-s CS-US interval did not, suggesting that close temporal contiguity between CS and US is neither necessary nor sufficient for conditioned taste aversion acquisition.

Age-related decrease of the chorda tympani nerve terminal field in the nucleus of the solitary tract is prevented by dietary sodium restriction during development.

Institution of a low-NaCl diet beginning at embryonic day 3 and continued throughout pre- and postnatal development has widespread effects on the neuroanatomical organization of the first gustatory relay in the nucleus of the solitary tract. To determine when these effects are expressed postnatally, the terminal field of the chorda tympani nerve was compared between sodium-restricted and sodium-replete rats at postnatal days 15-17, postnatal days 25-27, postnatal days 35-37, and adults. Total terminal fields were significantly larger in postnatal days 35-37 and adult sodium-restricted rats compared with aged-matched controls. The group-related differences appear related more to a remodeling of the terminal field in the dorsal zone of the terminal field in controls. Specifically, the terminal field volume in the dorsal zone in controls decreased dramatically from postnatal days 25-27 to postnatal days 35-37 and then again from postnatal days 35-37 to adulthood. In contrast, the fields did not change during development in sodium-restricted rats. These findings suggest that remodeling of the chorda tympani field occurs in controls at about the developmental period of taste response maturation. The lack of remodeling in sodium-restricted rats may be explained by a corresponding lack of functional response development to sodium salts. These results also illustrate the specificity and extent of how early dietary manipulations shape the developing brainstem.

Reversal of the sodium chloride aversion of fischer 344 rats by chorda tympani nerve transection

Fischer 344 (F344) rats are atypical in their lack of preference for any concentration of NaCl solution over water. It was hypothesized that abnormal signals mediated by the chorda tympani nerve (CT) could be causally involved in NaCl avoidance by F344 rats. This study assessed whether CT transection would normalize the salt preference of F344 rats. Preference for NaCl solutions (0.6%, 0.8%, and 1.0%) versus water was assessed using two-bottle preference tests. At all concentrations tested, CT-transected animals preferred NaCl solutions to water. This preference differed dramatically from the avoidance of these solutions by controls. These findings are striking, particularly because CT transections have generally failed to significantly affect NaCl preference in other rat strains. The results are consistent with the hypothesis that in F344 rats the avoidance of the taste of NaCl stems from input mediated by the CT.

Sodium appetite after transection of the chorda tympani nerve in Wistar and Fischer 344 rats.

Acute sodium depletion in rats leads to dramatic increases in intake of hypertonic NaCl solutions, a behavior known as sodium appetite. The importance of signals conveyed by the chorda tympani (CT) nerve to the expression of sodium appetite is unclear. We examined the effects of bilateral CT transection on the short- and long-term response to sodium depletion in Wistar and Fischer 344 (F344) rat strains, because Wistar rats normally display a NaCl preference in the absence of need whereas F344 rats avoid NaCl. In both strains, sodium appetite after CT transection and treatment with the diuretic furosemide was delayed and blunted or eliminated. The results suggest that signals conveyed by the CT nerve are important in the expression of a sodium appetite. Effects on F344 rats are particularly interesting because CT transection surgery appears to have opposite effects on NaCl intake depending on whether F344 rats are sodium replete or deplete.

Each Sensory Nerve Arising From the Geniculate Ganglion Expresses a Unique Fingerprint of Neurotrophin and Neurotrophin Receptor Genes

Neurons in the geniculate ganglion, like those in other sensory ganglia, are dependent on neurotrophins for survival. Most geniculate ganglion neurons innervate taste buds in two regions of the tongue and two regions of the palate; the rest are cutaneous nerves to the skin of the ear. We investigated the expression of four neurotrophins, nerve growth factor (NGF), brain‐derived neurotrophic factor (BDNF), neurotrophin 3 (NT‐3), and NT‐4, and five neurotrophin receptors, trkA, trkB, trkC, p75, and truncated trkB (Trn‐B) in single sensory neurons of the adult rat geniculate ganglion associated with the five innervation fields. For fungiform papillae, a glass pipette containing biotinylated dextran was placed over the target papilla and the tracer was iontophoresed into the target papilla. For the other target fields, Fluoro‐Gold was microinjected. After 3 days, geniculate ganglia were harvested, sectioned, and treated histochemically (for biotinylated dextran) or immunohistochemically (for Fluoro‐Gold) to reveal the neurons containing the tracer. Single labeled neurons were harvested from the slides and subjected to RNA amplification and RT‐PCR to reveal the neurotrophin or neurotrophin receptor genes that were expressed. Neurons projecting from the geniculate ganglion to each of the five target fields had a unique expression profile of neurotrophin and neurotrophic receptor genes. Several individual neurons expressed more than one neurotrophin receptor or more than one neurotrophin gene. Although BDNF is significantly expressed in taste buds, its primary high affinity receptor, trkB, was not prominently expressed in the neurons. The results are consistent with the interpretation that at least some, perhaps most, of the trophic influence on the sensory neurons is derived from the neuronal somata, and the trophic effect is paracrine or autocrine, rather than target derived. The BDNF in the taste bud may also act in a paracrine or autocrine manner on the trkB expressed in taste buds, as shown by others.

Neuronal cell death and population dynamics in the developing rat geniculate ganglion.

In contrast to many neuronal systems, the pattern of developmental neuronal degeneration in the rat geniculate ganglion has remained undefined. To address this issue sectioned geniculate ganglia from embryonic day 13 to postnatal day 3 have been examined using standard histological techniques, TdT-mediated dUTP-digoxigenin nick end labeling to verify apoptotic activity, bromo-deoxyuridine incorporation to monitor neuronal precursor proliferation, and anti-beta-neurotubulin III to verify the neuronal identity of pycnotic cells. Results summed from alternate (embryonic day 13) or every third (embryonic day 14-postnatal day 3) section show that neuronal degeneration occurs as early as embryonic day 13 (6.8% of neurons counted), well before geniculate innervation of lingual taste buds at embryonic day 16. A degenerative peak occurs at embryonic day 17 (9.5%) followed by a decline (1.7% at embryonic day 18) and leveling off (0.1%-0.2% at embryonic day 22-postnatal day 3). Thus, geniculate neuronal degenerative pattern includes both innervation-associated histogenetic and morphogenetic cell death. Corresponding counts of mean neuronal numbers in the sections showed a continual rise from embryonic day 13 through embryonic day 18 (approx. 330-760) followed by a slight decline at embryonic day 19 (to approx. 630) and then a final leveling off at 800-825 by embryonic day 20. This pattern differs from many other developing neural systems which show a major population crash during initial target contact. It likely reflects different but slightly overlapping neuronal precursor proliferation and degeneration patterns in multiple geniculate neuronal subpopulations.

Contributory role of sex differences in the variations of gustatory function.

Remarkable variability between males and females occurs for an array of taste‐guided behaviors in both rodents and humans. Sex differences have been noted for taste preference, detection thresholds, and reactivity to taste stimuli. Manipulating sex hormones during early postnatal development or altering the amount of circulating estrogen in adulthood can dramatically alter the pattern of these behaviors. Receptors for sex hormones appear to be prominent in several nuclei associated with central gustatory pathways, indicating that steroid hormones may modulate central taste processing. Electrophysiological recordings from the rat brainstem suggest that taste‐elicited activity to sweet stimuli is organized by hormones during early development, and activity during bitter stimulation is altered by circulating ovarian hormones. Sex differences in gustatory function appear to emerge at the level of the taste bud. Among ovariectomized rats, estradiol treatment decreases activity in the chorda tympani nerve during NaCl stimulation. Although there is no evidence that chorda tympani responses to NaCl differ between intact male and female rats, glossopharyngeal nerve responses are lower in intact females for both NaCl and sodium acetate. Responses in the glossopharyngeal nerve to citric acid stimulation are also higher in female rats relative to males. These findings suggest that, in addition to differential central modulation of taste input based on sex, taste information from the periphery varies between males and females. Although the extent of sex differences in taste processing and the underlying causal mechanisms require further clarification, it is clear that studying one sex alone provides an incomplete picture of gustatory function.

Amiloride sensitivity in the neonatal rat.

Amiloride-sensitive sodium channels in taste buds appear to play a key role in the response to NaCl stimulation, at least in adult rats. The researchers examined whether neonatal rats, which display an exaggerated preference for hypertonic NaCl solutions, lack functional amiloride-sensitive sodium channels. NaCl intake was significantly reduced by amiloride pretreatment, but water and ammonium chloride, NH4Cl, were unaffected. The researchers assessed whether the early appearance of amiloride sensitivity was mediated by effects on chorda tympani (CT) activity by sectioning the CT before testing. CT transection reduced intake of NaCl solutions and eliminated evidence of amiloride sensitivity. Amiloride sensitivity was also assessed by recording of whole-nerve CT activity at 8-11 days of age; the response to NaCl stimulation was significantly suppressed by amiloride. These data indicate that amiloride-sensitive sodium channels develop earlier than previously believed.