Journal of Neuroscience, Vol 10, 3148-3157, Copyright © 1990 by Society for Neuroscience
Convergence in mammalian nucleus of solitary tract during development and functional differentiation of salt taste circuits
MB Vogt and CM Mistretta
Department of Biologic and Materials Sciences, School of Dentistry, University of Michigan, Ann Arbor 48109-1078.
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.
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