To determine the type and extent of neural rearrangements that are made during functional differentiation of circuits for salt taste processing, we determined receptive field size and salt response characteristics of second-order taste cells in 3 age groups of sheep. Neurophysiological recordings were made from single cells in the nucleus of the solitary tract (NST) in fetal, perinatal, and postnatal sheep. Responses to NH4Cl, NaCl, and KCl were measured, and location and number of fungiform papillae in the receptive field were determined by stimulating individual papillae with anodal electrical current. The data are compared with previous, parallel measures from chorda tympani nerve afferent taste fibers to permit conclusions about convergence or divergence onto second-order cells. Receptive field size of second-order taste neurons increases during development, in contrast to the decrease in field size observed previously for chorda tympani nerve fibers during the same period. Furthermore, receptive fields of second-order cells are significantly larger than those of first-order fibers at perinatal and lamb ages, but not fetal. Thus, there is convergence of first-order taste afferents onto brain-stem neurons, and the convergence increases remarkably between fetal and perinatal periods. Associated with the increase in convergence are increased salt response frequencies relative to afferent fibers for NaCl in perinatal animals and lambs, and for KCl in lambs. The increase in frequencies occurs before NST neurons are functionally mature, as indicated by the rapid response adaptation of many cells in young animals. Convergence in NST during development apparently functions to maximize gain for processing neural responses to NaCl. In the periphery, response frequencies to NaCl are very low in fetuses, and increase progressively during development. In the NST, NaCl response frequencies are high even in fetuses, and remain high. The process of convergence onto second-order cells is accomplished with maintenance of order in afferent projections because receptive fields of NST neurons are composed of fungiform papillae that are clustered together, not dispersed over the tongue. Our quantification of taste receptive field size at 2 neural levels provides strong evidence for increasing convergence in the NST during development. Altering patterns of afferent neural input and geometry of second-order neurons may have a role in establishing convergence. The convergence has an apparently special function: to increase gain for NaCl taste sensation. Therefore, neural rearrangements during differentiation of salt taste pathways result in specific functional outcomes.

These experiments indicate that by Day 15 after birth, the processes that mediate a number of taste-controlled behaviors in the rat are functional. These include the sensory processes necessary to detect and respond reflexively to sucrose, the event-learning processes that reduce the rat's neophobic reaction to sucrose, and the integrative-learning processes that enable it to learn an aversion to sucrose when paired with lithium toxicosis, even when these events are separated by 1 hr. These capacities, however, did not emerge simultaneously. Those necessary to detect and respond reflexively to sucrose emerged prior to those that contribute to the learned control of taste-guided behaviors. It is argued that these age-related dissociations in behavioral capacities reflect a caudal-to-rostral maturational sequence of components of the ascending gustatory system that are thought to underlie these capacities.

1. The responses of single nucleus of the solitary tract (NST) neurons in the hamster were recorded to an array of Na+ and non-Na+ stimuli under each of three adaptation conditions: distilled H2O, 0.032 M NaCl, and 10 microM amiloride. Each adapting solution flowed for 60 s before delivery of one of seven test stimuli: 0.032 M NaCl, NaNO3, and Na-gluconate, 0.1 M KCl and sucrose, 1 mM HCl, and 3 mM quinine hydrochloride (QHCl). Stimuli were dissolved in distilled H2O (H2O and NaCl adaptation conditions) or 10 microM amiloride (amiloride adaptation condition). 2. Both amiloride treatment and NaCl adaptation reduced responses to the Na+ stimuli. The effects of NaCl adaptation were generally greater than those of amiloride, and the responses to the Na+ salts were reduced by NaCl adaptation in every cell that responded to NaCl, regardless of its best-stimulus classification. Amiloride treatment suppressed the responses to Na+ salts with larger anions (NaNO3 and Na-gluconate) more than the response to NaCl. 3. Unlike amiloride treatment, NaCl adaptation also reduced responses to several non-Na+ stimuli (KCl, HCl, and QHCl). This effect occurred primarily in the NaCl-best neurons that were most highly responsive to NaCl and that showed a postexcitatory suppression after NaCl. This suppression has been observed in recordings from the chorda tympani nerve in both rats and hamsters and in taste receptor cell responses recorded in situ in the rat. If it is a receptor phenomenon, these data would imply that some NaCl-sensitive receptor cells are also responsive to these non-Na+ electrolytes. 4. The effects of amiloride on the responses to Na+ stimuli were not limited to NaCl-best neurons, but occurred in sucrose-best cells as well. These results suggest that the sucrose-best cells in the NST receive converging input from sucrose- and NaCl-best chorda tympani fibers, because there is little Na+ sensitivity in the peripheral sucrose-best fibers and the amiloride sensitivity is restricted to NaCl-best chorda tympani fibers. The responses to NaCl in the few HCl- and QHCl-best NST neurons were not affected by amiloride. 5. Rinsing the tongue with amiloride for 60 s resulted in a reduction in the baseline response rate of NST cells. This effect occurred primarily in NaCl- and sucrose-best NST neurons and implies that much of the spontaneous activity in these brain stem cells arises from amiloride-sensitive channel activity in the peripheral receptor cells. 6. The results of human psychophysical studies show very different effects of NaCl adaptation and amiloride treatment. Adaptation to NaCl produces a robust and specific reduction in the saltiness of all salts. The present results show that NaCl adaptation reduces the responses of all cells sensitive to NaCl. Treatment of the human tongue with amiloride produces a proportionately smaller reduction in the response to NaCl than it does in rodents, and it appears to have no effect on saltiness. Rather, amiloride has been shown to specifically reduce the sour side taste of NaCl, Nag...

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.