Enduring alterations in neurophysiological taste responses after early dietary sodium deprivation

Abstract

1. Neurophysiological taste responses from neurons in the nucleus of the solitary tract (NST) were studied in four groups of rats during chemical stimulation of the tongue with sodium and non-sodium salts, citric acid, and sucrose. The four groups of rats consisted of those fed a NaCl-deficient diet (0.03% NaCl) from day 3 postconception to at least day 50 postnatal (deprived rats), rats initially fed the NaCl-deficient diet during development and then placed on a NaCl-replete diet at adulthood for > or = 5 wk (control-deprived rats), and rats always fed the NaCl-replete diet (control rats). 2. Compared with controls, dietary NaCl deprivation instituted early in development resulted in highly attenuated average response frequencies to sodium salts (as much as 50%) but not to nonsodium salts and nonsalt stimuli. Concomitantly, most NST neurons in deprived rats responded "best" to NH4Cl and few responded best to NaCl. This is in contrast to that observed in controls, where the same proportion of neurons responded best to NaCl and best to NH4Cl. 3. Taste responses in recovered rats exhibited a hyperresponsiveness to many sodium salts compared with controls. That is, sodium salts elicited average response frequencies significantly greater (as much as 100%) than that obtained in controls. The proportions of neurons responding best to NaCl or to NH4Cl were opposite to that in deprived rats. In recovered rats, the proportion of neurons that responded best to NaCl was much greater than that which responded best to NH4Cl. 4. Rats deprived of dietary NaCl only as adults responded like controls. Therefore the environmental manipulations must occur during early periods of development. 5. These findings show that early dietary manipulations of sodium and subsequent replacement of dietary sodium have neurophysiological effects relatively selective for sodium-elicited taste responses. Furthermore, because recordings in recovered rats were obtained > or = 5 wk after feeding the NaCl-replete diet, it appears as though early NaCl deprivation permanently alters the functional organization of the NTS. Although it is likely that alterations in peripheral neural activity play a role in the functional development of NTS neurons responsive to taste stimuli, other non-activity-related factors may also be important.

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

“…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.…”

“…However, unlike other sensory systems where neural alterations are most profound in cortex, large-scale changes occur in the gustatory brainstem (Hill et al, 1983;Hill, 1991, 1993;Lasiter, 1991;Vogt and Hill, 1993;May and Hill, 2006). In fact, introducing a custom diet featuring a low-sodium content from embryonic day 3 (E3) to E12 is sufficient to induce ϳ50% enlargement of the chorda tympani (CT) nerve terminal field in the nucleus of the solitary tract (NTS) compared with rats fed a nutritionally balanced commercial diet (Krimm and Hill, 1997).…”

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

“…Widespread functional alterations also occur at the first central relay. Early dietary sodium restriction reduces sodium salt response frequencies of neurons in the nucleus of the solitary tract (NTS) by as much as 50%, and severely decreases the proportion of cells that respond best to NaCl (Vogt and Hill, 1993). Similar to the periphery, only responses to sodium salts are affected in NTS neurons.…”

Neural Plasticity in the Gustatory System

“…NTS neurons in sodium-restricted rats respond with lower response frequencies to sodium salts, while activity to non-sodium salts and to non-salt stimuli are normal. 59 However, unlike in the periphery, sodium-restricted rats fed a sodium-replete diet for at least 5 weeks at adulthood have NTS neurons that are more responsive to sodium salts than in controls. 59 Accordingly, these neurons have an apparent shift in the stimulus to which they respond best.…”

“…59 However, unlike in the periphery, sodium-restricted rats fed a sodium-replete diet for at least 5 weeks at adulthood have NTS neurons that are more responsive to sodium salts than in controls. 59 Accordingly, these neurons have an apparent shift in the stimulus to which they respond best. The central functional changes, like the morphological changes, are permanent and specific.…”