CHARACTERISTIC FIRING BEHAVIOR OF CELL-TYPES IN THE CARDIORESPIRATORY REGION OF THE NUCLEUS-TRACTUS-SOLITARII OF THE RAT

The present in vitro study was performed to characterize neurons within dorsal regions of the nucleus tractus solitarii (NTS), principally at the level of area postrema, and known to receive inputs predominantly from cardiovascular and respiratory afferents (i.e. cardiorespiratory NTS). This report describes 4 classes of neurons (S1-S4) that were silent at their resting membrane potential and received relatively short ( < 3.6 ms) and consistent latency synaptic inputs (+/- 0.4 ms) comprising either an EPSP or EPSP/IPSP sequence following low intensity electrical stimulation of the solitary tract (ts). Intracellular recording with sharp electrodes were used-to characterize neuron types based on their different firing response patterns to injection of depolarizing current. Sl cells showed a single action potential; S2 fired repetitively; S3 produced a 2-5 spike burst coincident with the start of the current pulse and S4 neurons showed delayed excitation. Accommodation of firing frequency was seen in S2, S3 and some S4 cells. The voltage dependency of the different discharge patterns of the 4 cell groups was tested by current pulse stimulation at different holding potentials. However, in the majority of cells in any one cell class the firing pattern was qualitatively similar. Based on these findings it is suggested that the different firing characteristics reflect differences in intrinsic membrane properties between neuron classes. Representative examples from each of the defined cell classes were further studied in current and voltage clamp using the whole cell patch technique to define the presence and role of certain ionic currents in the firing response patterns of the 4 cell groups. In the current clamp configuration the firing behavior of S1 neurons (single spiking) was unaltered during exposure to 4-aminopyridine (4-AP; 2 mM), cobalt chloride (Co; 5 mM), norepinephrine (NE; 20 muM) and muscarine chloride (50 muM). It is suggested that the relatively low excitability of this neuron is due a persistent outward current which occurred at -40 mV during depolarizing voltage steps in the voltage clamp configuration. A common characteristic of S2 neurons (repetitively firing) was that they showed accommodation during current injection which was greatly attenuated in the presence of Co or NE. In addition, 4-AP slowed the firing frequency, reduced the afterhyperpolarization and broadened the spike width of S2 cells. Interestingly, the amount of accommodation observed in S2 cells was variable for cells of this class and was proportional to the magnitude of a Co-sensitive inward current present during depolarizing voltage steps between -45 to -5 mV. Exposure of S3 cells to NE resulted in repetitive firing with reduced accommodation during current pulse injection. The frequency of discharge during a current pulse was further increased by subsequent administration of 4-AP. Finally, the magnitude of the delayed excitation of S4 neurons was dependent on the voltage and was abolished by 4-AP. This was consistent with voltage clamp data showing a voltage-dependent and 4-AP sensitive outward current, first evident at -40 mV. The present study demonstrates the presence of 4 different cell types within the dorsal or cardiorespiratory region of the NTS. The distinction between the 4 cell groups are based on firing response pattern to injected current and these differences correlate with qualitative differences in the magnitude, time course and voltage dependency of: (1) a 4-AP sensitive current, (2) a Ca, and (3) Ca-dependent currents sensitive to NE and apamin. It is suggested that the intrinsic membrane properties of neurons within the cardiorespiratory NTS may play a role in the integration of afferent inputs. In order to explore these possibilities the following paper describes computational model neurons based on the present data and a previous study on rhythmically active neurons (Paton et al., J. Neurophysiol., 66 (1991) 824-838).