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Relationship Between Structure and Function of Neurons in the Rat Rostra1 Nucleus Tractus Solitarii

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Relationship Between Structure and Function of Neurons in the Rat Rostra1 Nucleus Tractus Solitarii THE JOURNAL OF COMPARATIVE NEUROLOGY 344:50-64 (1994) Relationship Between Structure and Function of Neurons in the Rat Rostra1 Nucleus Tractus Solitarii MICHAEL S. KING AND ROBERT M. BRADLEY Department of Biologic and Materials Sciences, School of Dentistry (M.S.K., R.M.B.) and Department of Physiology, School of Medicine (R.M.B.), University of Michigan, Ann Arbor, Michigan 48109-1078 ABSTRACT To investigate the relationship between the structure and function of neurons in the rostral (gustatory) nucleus tractus solitarii (rNTS), we analyzed the morphological and biophysical properties of rNTS neurons by performing whole-cell recordings in a brain slice preparation. Overall, neurons (n = 58) had a mean soma1 diameter of 16 km, an average dendritic length of 598 km, an average dendritic thickness of 0.91 pm, and a spine density of 0.037 spines/ ym. Neurons were separated into three groups (elongate, multipolar, and ovoid) on the basis of previously established morphological criteria. The highest percentage (49%) of neurons were classified as ovoid, while 35% were multipolar and only 16% were elongate. The most frequently observed firing pattern, in all three cell types, elicited by a 1,200 ms, 100 PA depolarizing current pulse was a regularly firing spike train. However, the intrinsic firing properties of the remaining neurons were different. Thirty-one percent of the ovoid neurons responded with a short burst of action potentials and 44% of the elongate neurons showed a delay in the onset of the spike train following a hyperpolarizing prepulse. Less than 16% of the multipolar neurons demonstrated either of these firing characteristics. Therefore, rNTS neurons with similar morphology do not have unique biophysical properties. However, the data suggest that there may be subpopulations of the three morphological types, each of which displays a different firing pattern. Since the structure and function of the three morphological groups were not strictly correlated, these subpopulations may represent functional groups. o 1994 Wiley-Liss, Inc. Key words: biocytin, brain slice, taste, whole-cell recordings, neuron reconstruction Chemosensory information from the oral cavity, phar- in a region called the rostral central subdivision (Whitehead ynx, and larynx travels in the facial, glossopharyngeal and and Frank, 1983; Whitehead, 1988). This subdivision is also vagus nerves to the ipsilateral nucleus tractus solitarii the site of termination of the lingual branch of the glosso- (NTS), a longitudinal column of neurons extending from pharyngeal nerve and is therefore hypothesized to be the the first cervical segment of the spinal cord to the genu of major gustatory recipient zone of the rNTS. The projection the facial nerve (Torvik, 1956; Hamilton and Norgren, zones of these two taste nerves are not fully segregated 1984; Bradley et al., 1985; Housley et al., 1987). The facial since their distributions overlap within the rNTS (Hamil- nerve projection terminates in the rostral pole of the NTS ton and Norgren, 1984). (rNTS), the glossopharyngeal nerve terminates caudal to Analysis of Golgi-stained material of the gustatory zone the facial nerve, and the vagus nerve terminates caudal to of the rat and hamster rNTS has shown that it contains at the glossopharyngeal nerve. Chemosensory information least three neuron types (Davis and Jang, 1988; Lasiter and carried by the facial and glossopharyngeal nerves is believed Kachele, 1988; Whitehead, 1988; King and Hill, 1993). to be gustatory in nature while that conveyed by the vagus nerve appears to play a major role in upper airway protec- tive reflexes (Bradley et al., 1983; Smith and Hanamori, Accepted December 26, 1993. 1991). Michael S. King is now at Campus Box 8264, Biology Department, Stetson University, DeLand, FL 32720-3756. The gustatory input of the rNTS has been defined in Address reprint requests to Dr. Robert M. Bradley, 6228 School of some detail with neural tracing techniques. The chorda Dentistry, 1011 N. University Ave., University of Michigan, Ann Arbor, MI tympani projection terminates medial to the solitary tract 48109-1078. O 1994 WILEY-LISS, INC. STRUCTURE-FUNCTION OF rNTS NEURONS 51 Multipolar (stellate) neurons have a triangular or polygonal- Whole-cell recordings and biophysical shaped soma and three to five primary dendrites; elongate measurements (fusiform) neurons are characterized by an elongated soma and two thick primary dendrites that exit the cell body at Unpolished patch electrodes were pulled in two stages on opposite poles; and ovoid neurons have small somal diam- a Narishige PP83 electrode puller from 1.5 mm-OD borosili- eters and two to four primary dendrites that are thin and cate filament glass (WPI, TW 150F-4).The electrodes had sparsely branched. Based on neural tracing studies these tip resistances of 5-8 Mfl when filled with a solution different neuron types have been demonstrated to have containing (in mM) K gluconate 130, Hepes 10, EGTA 10, different projection patterns. Multipolar and elongate neu- MgCla 1, CaClz 1, ATP 2, and 1%biocytin. The pH was rons project rostrally to the pontine gustatory relay (Lasiter adjusted to 7.4 with KOH. Whole-cell recordings were made and Kachele, 1988; Whitehead, 1990). Multipolar neurons using the technique of Blanton et al. (1989), as previously in the ventral part of rNTS project to the reticular forma- described in detail (Bradley and Sweazey, 1992). Once a tion and the motor nuclei of cranial nerves V, VII, IX, X, giga-fl seal was formed and the patch ruptured, current and XI1 (Norgren, 1978; Travers, 1988; Beckman and stimulation protocols were performed and voltage data Whitehead, 1991). Thus, rostrally directed neurons are were acquired using the pCLAMP program (Axon Instru- believed to be important in processing and relaying gusta- ments). Current was injected into neurons using the bridge tory information while caudally connected neurons are circuit of an Axoclamp 1A amplifier in current clamp mode. presumably involved in the reflex control of salivation and The indifferent electrode was Ag-AgC1 wire connected to ingestive behavior (Beckman and Whitehead, 1991). The the extracellular solution via an agar bridge. ovoid neurons are believed to be interneurons because they Electrophysiological data were analyzed using the are relatively small, and in labeling studies they do not Clampfit program (Axon Instruments). Biophysical proper- project to the pontine taste relay, the caudal NTS, or the ties, such as input resistance, action potential amplitude, medullary reticular formation (Lasiter and Kachele, 1988; width, rise time and latency, and membrane time constants Davis, 1993). were determined by delivering a series of 100 ms hyperpolar- Neurons of rNTS have also been separated into four izing and depolarizing current pulses (-100 to 75 PA). different groups based on their repetitive firing properties Since recordings were made with a potassium gluconate (Bradley and Sweazey, 1992). However, the morphology of solution in the recording pipette, a junctional potential of these neurons was not determined so that the biophysical 10 mV was subtracted from the membrane potential values properties of intrinsic and projection neurons is unknown. (Staley and Mody, 1992). To be included in the electrophysi- We therefore used whole-cell recordings in brain slices of ological analysis neurons had to have a resting membrane rNTS combined with intracellular labeling to determine the potential more negative than -40 mV, an action potential intrinsic firing properties of morphologically identified neu- overshoot, and an input resistance greater than 100 Ma. rons. This information is important in understanding the Neurons were separated into four groups on the basis of neural circuits involved in processing gustatory informa- their repetitive firing pattern induced by a 1,200 ms, 100 PA tion at the first central relay in the taste pathway. Some of depolarizing current pulse, which was given alone or pre- these results have been presented in preliminary form ceded by a -200 PA hyperpolarizing pulse of increasing (King and Bradley, 1993a,b). duration (50,100,and 150 ms). The four biophysical groups have been described previously in detail (Bradley and Sweazey, 1992). Most rNTS neurons fire a repetitive spike MATERIALS AND METHODS train throughout the long-lasting (1,200 ms) depolarizing Brain slice preparation current pulse (groups I, 11, and 111). In a smaller population of neurons (group IV), the discharge pattern consists of a Brain slices containing the rostral 1.6 mm of the NTS short burst of action potentials which occurs at the onset of were obtained from 45 female Sprague-Dawley rats (Charles the depolarization. The firing patterns of group I, 11, and I11 River) weighing 125 to 175 grams, as previously described neurons are distinguished by hyperpolarizing the neurons (Bradley and Sweazey, 1990,1992). Rats anesthetized with prior to delivering the long depolarizing current pulse. In sodium pentobarbital (50 mg/kg) were decapitated and the group I neurons, the repetitive discharge pattern initiated brainstem quickly removed and cooled in physiological by membrane depolarization is changed to an irregular saline for 2 minutes. The physiological saline contained (in spike train by prior hyperpolarization. In group I1 neurons, mM) NaCl 124, KC1 5, CaClz 2.5, MgS04 1.3, NaHC03 26, hyperpolarization either delays the occurrence of the first KH2P04 1.25, and dextrose 25. The solution was gassed action potential or increases the length of the first inter- with 95% 02and 5% C02to maintain the pH at 7.4. After spike interval in the action potential train produced by cooling, the brainstem was secured onto the stage of a membrane depolarization. In group I11 neurons, hyperpolar- Vibratome with cyanoacrylate glue and cut into 400 ym ization has little effect on the repetitive discharge pattern. thick coronal or sagittal slices or 300 pm thick horizontal The effects of SP, GABA, and NMDA on neural activity of slices. Before recording, the slices were incubated for at several neurons in each group was also examined (see least 1 hour in physiological saline at room temperature.
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