Convergence in mammalian nucleus of solitary tract during development and functional differentiation of salt taste circuits

Abstract

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.