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

Abstract

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 sodiumrestricted 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 sodiumrestricted 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.

Extensive Reorganization of Primary Afferent Projections into the Gustatory Brainstem Induced by Feeding a Sodium-Restricted Diet during Development: Less Is More

“…It must be pointed out that we use the terms "dorsal," "intermediate," and "ventral" zones here to be consistent with previous reports (King and Hill, 1991;Krimm and Hill, 1997;May and Hill, 2006;Sollars et al, 2006). However, the orientation of the NTS within the brainstem is such that the caudalmost portion of the NTS is dorsal to the rostralmost portion (i.e., the NTS expands ventrally and rostrally from the dorsalmost extent of the NTS) (Fig.…”

“…Although there are differences between diets (i.e., they are not matched), the goal of this and previous studies (King and Hill, 1991;Krimm and Hill, 1997;May and Hill, 2006;Sollars et al, 2006) is to compare neurobiological differences between a custom sodium-restricted diet and a commercial stock diet and not between specific dietary components. This choice was made primarily because the effects of a low-sodium diet in our studies are not attributable to altered taste stimulation but likely result in early undernutrition and/or malnutrition.…”

“…Moreover, we chose here and previously to use a standard rodent diet as our control diet because of the rich literature that exists in studies of rodent development with standard rodent diets. Therefore, we are examining the effects on terminal field organization between a diet proven to alter peripheral (Hill et al, 1983;Hill, 1987;Hill and Przekop, 1988) and central (Vogt and Hill, 1993) gustatory function and structure (King and Hill, 1991;Krimm and Hill, 1997;May and Hill, 2006;Sollars et al, 2006) with a nutritionally balanced commercial diet. We note, however, that our previous work used a sodium-replete diet matched to the sodium-restricted diet (Hill et al, 1983;Hill, 1987;Hill and Przekop, 1988), and the neurophysiological effects on the taste system were no different between the custom-made "control" diet and the sodium-replete diet used here.…”

“…To localize regions especially susceptible to the dietary manipulation and to be consistent with our previous studies of the CT terminal field in the NTS (King and Hill, 1991;Krimm and Hill, 1997;May and Hill, 2006;Sollars et al, 2006), the NTS was divided into dorsal, intermediate, and ventral zones. The dorsal zone contained sections in which the solitary tract was most visible and included sections in which the fourth ventricle occupied the largest mediolateral extent (Fig.…”

“…To test the hypothesis that the enlarged terminal fields in rats fed the sodium-restricted diet from E3 to E12 were attributable to altered afferent signals, as proposed to occur in rats fed the sodium-restricted diet from E3 through adulthood (Sollars et al, 2006), we recorded taste responses from the CT nerve in rats fed the sodium-restricted diet from E3 to E12 and in rats fed the control diet. In response to a concentration series of NaCl, sodium acetate, NH 4 Cl, and KCl, there were no group-related differences in response magnitudes ( p Ͻ 0.05).…”