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Convergence in Mammalian Nucleus of Solitary Tract During Development and Functional Differentiation of Salt Taste Circuits

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Convergence in Mammalian Nucleus of Solitary Tract During Development and Functional Differentiation of Salt Taste Circuits The Journal of Neuroscience, September 1990, fo(9): 3148-3157 Convergence in Mammalian Nucleus of Solitary Tract During Development and Functional Differentiation of Salt Taste Circuits Mark 6. VogP and Charlotte M. Mistrettalv* ‘Department of Biologic and Materials Sciences, School of Dentistry, %enter for Human Growth and Development and Center for Nursing Research, University of Michigan, Ann Arbor, Michigan 48109-1078 To determine the type and extent of neural rearrangements Our quantification of taste receptive field size at 2 neural that are made during functional differentiation of circuits for levels provides strong evidence for increasing convergence salt taste processing, we determined receptive field size in the NST during development. Altering patterns of afferent and salt response characteristics of second-order taste cells neural input and geometry of second-order neurons may in 3 age groups of sheep. Neurophysiological recordings have a role in establishing convergence. The convergence were made from single cells in the nucleus of the solitary has an apparently special function: to increase gain for NaCl tract (NST) in fetal, perinatal, and postnatal sheep. Re- taste sensation. Therefore, neural rearrangements during sponses to NH,CI, NaCI, and KCI were measured, and lo- differentiation of salt taste pathways result in specific func- cation and number of fungiform papillae in the receptive field tional outcomes. were determined by stimulating individual papillae with an- odal electrical current. The data are compared with previous, The receptive field of any neuron in a sensorypathway is com- parallel measures from chorda tympani nerve afferent taste posed of all the receptors that can influence its neural activity fibers to permit conclusions about convergence or diver- (Shepherd, 1983). Therefore, receptive field organization is an gence onto second-order cells. essentialcomponent of sensory circuits, and knowledge of re- Receptive field size of second-order taste neurons in- ceptive field development is important in understanding func- creases during development, in contrast to the decrease in tional differentiation of sensory pathways. field size observed previously for chorda tympani nerve fi- To understand better the development and maturation of bers during the same period. Furthermore, receptive fields neural circuits for salt taste processing,we have made measures of second-order cells are significantly larger than those of of receptive field size and salt responsecharacteristics of second- first-order fibers at perinatal and lamb ages, but not fetal. order taste cells in 3 age groups of sheep. These data can be Thus, there is convergence of first-order taste afferents onto compared with parallel measuresof receptive fields and salt brain-stem neurons, and the convergence increases re- responsesfrom first-order taste afferents. Receptive field size at markably between fetal and perinatal periods. Associated various neural levels is determined during development through with the increase in convergence are increased salt re- divergence and convergence of afferent input. For example, a sponse frequencies relative to afferent fibers for NaCl in primary sensory neuron may receive converging input from perinatal animals and lambs, and for KCI in lambs. The in- multiple receptors and then diverge to contact several second- crease in frequencies occurs before NST neurons are func- order cells; or several sensoryneurons may converge on a single tionally mature, as indicated by the rapid response adap- second-order cell. Thus, results from study of chorda tympani tation of many cells in young animals. fibers and second-ordertaste cells provide an indication of con- Convergence in NST during development apparently func- vergence and divergence at 2 neural levels during development tions to maximize gain for processing neural responses to of the taste system. NaCI. In the periphery, response frequencies to NaCl are In previous studies, the number of fungiform papillae and very low in fetuses, and increase progressively during de- associated taste buds innervated by a single chorda tympani velopment. In the NST, NaCl response frequencies are high nerve fiber was determined in fetal, perinatal, and postnatal even in fetuses, and remain high. The process of conver- sheep(Mistretta et al., 1988; Nagai et al., 1988). We found that gence onto second-order cells is accomplished with main- receptive fields of first-order taste afferents decreasedin size tenance of order in afferent projections because receptive during development; that is, a singlefiber innervated fewer fun- fields of NST neurons are composed of fungiform papillae giform papillae in postnatal lambs than in younger age groups. that are clustered together, not dispersed over the tongue. The decreasein field size of taste fibers was accompaniedby an increase in proportion of fibers that responded with highest Received Feb. 2, 1990; revised Apr. 13, 1990; accepted May 10, 1990. frequency to NaCl, compared to other salts, NH,Cl or KCl. This work was supported by National Science Foundation Grant BNS-83 11497 Furthermore, there was a correlation between receptive field and National Institutes of Health Grant DC00456 to C.M.M. Correspondence should be addressed to Dr. Charlotte M. Mistretta, Biologic size of first-order neurons and salt responsecharacteristics. Fi- and Materials Sciences, Room 6226, School of Dentistry, University of Michigan, bers with smaller receptive fields (fewer fungiform papillae) re- Ann Arbor, MI 48109-1078. spondedwith higher frequency to NaCI; fibers with larger fields = Current address: Department of Psychology, University of Virginia, Char- lottesville, VA 22903. responded with higher frequency to NH&l. These data led to Copyright 0 I990 Society for Neuroscience 0270-6474/90/093148-10$03.00/O the conclusion that there is an acquisition of small, highly NaCl- The Journal of Neuroscience, September 1990, IO(Q) 3149 responsive, receptive fields during development of the periph- 1988; Lawson et al., 1989) and in brain-stem areas other than the eral taste system in sheep. solitary nucleus, including trigeminal nuclei (e.g., Jacquin et al., 1989). Furthermore, in developmental studies of gustatory NST (Bradley and We now have parallel information on receptive field size and Mistretta, 1980; Hill et al., 1983) and other second-order sensory cells salt responses of second-order taste neurons in the nucleus of (e.g., Ferrington and Rowe, 1982; Fitzgerald, 1985) anesthetized prep- the solitary tract (NST) in the same age groups of sheep. Re- arations are used. In early development, neurons generally exhibit im- cordings were made from single NST neurons and responses to mature response characteristics including low response frequencies, rap- stimulation of the tongue with NaCl, NH&l, and KC1 were idly adapting responses, and longer response latencies. The immature neurophysiological response characteristics that we report here are typ- measured in fetal, perinatal, and postnatal sheep. Using elec- ical of those in other systems and we have no reason to assume that trical stimulation of single fungiform papillae, the number of they are attributed to anesthetic effects. papillae in the receptive field of each cell was also determined. In general, we have found that receptive fields of second-order ReceptiveJield neurophysiology NST neurons are larger than chorda tympani receptive fields. With obex as the zero reference point, extracellular recordings from Furthermore, NST fields increase in size during development single taste neurons in the rostra1 NST were made with tungsten mi- whereas chorda tympani fields decrease in size during the same croelectrodes (0.4-1.8 MB). Coordinates were based on previous studies of taste cells in NST of fetal and postnatal sheep (Bradley and Mistretta, period. Thus, there is convergence of first-order taste afferents 1980). Neural activity was monitored with a preamplifier, oscilloscope, onto brain-stem neurons and the extent ofconvergence increases and audio amplifier and recorded on tape with voice cues for subsequent during development. Associated with the increase in conver- analysis. gence is an increase in response frequency to salt stimuli and Single neuron recordings were identified during experiments by ex- amining the superimposition of successive action potentials within a changes in adaptation characteristics of the neurons. It appears spike train using a storage oscilloscope and delay circuit. Consistency that the extensive developmental convergence and resulting in- of waveform and amplitude were monitored. When neural data were creases in salt response frequencies eradicate the correlation digitized for subsequent data analysis, waveform was again reviewed. between receptive-field size and salt taste response that was Second-order neurons were identified during recording sessions by their observed in the periphery. However, this convergence might be biphasic action potentials and distinctive response characteristics, es- pecially receptive field size and NaCl responsiveness. In subsequent essential to maximize gain in the developing taste system and data analysis the very different neural response properties of the second- thereby ensure transmission of relatively weak peripheral input order cells. comoared to chorda tvmoani afferent fibers. were confirmed. about NaCl taste stimuli to the CNS. as demonstrated in Results. I _ Taste neurons with lingual receptive fields were identified by
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