ELECTROPHYSIOLOGICAL PROPERTIES OF NEURONS WITHIN THE NUCLEUS AMBIGUUS OF ADULT GUINEA-PIGS

1. The purpose of this study was to determine the electrophysiological properties of neurons within the region of the nucleus ambiguus (NA), an area that contains the ventral respiratory group. By the use of an in vitro brain stem slice preparation, intracellular recordings from neurons in this region (to be referred to as NA neurons, n = 235) revealed the following properties: postinhibitory rebound (PIR), delayed excitation (DE), adaptation, and posttetanic hyperpolarization (PTH). NA neurons were separated into three groups on the basis of their expression of PIR and DE: PIR cells (58%), DE cells (31%), and Non cells (10%). Non cells expressed neither PIR nor DE and no cells expressed both PIR and DE. 2. PIR was a transient depolarization that produced a single action potential or a burst of action potentials when the cell was released from hyperpolarization. In the presence of tetrodotoxin (TTX), the maximum magnitude of PIR was 7-12 mV. Under voltage-clamp conditions, hyperpolarizing voltage steps elicited a small inward current during the hyperpolarization and a small inward tail current on release from hyperpolarization. These currents, which mediate PIR, were most likely due to Q-current because they were blocked with extracellular cesium and were insensitive to barium. 3. DE was a delay in the onset of action potential firing when cells were hyperpolarized before application of depolarizing current. When cells were hyperpolarized to -90 mV for greater-than-or-equal-to 300 ms, maximum delays ranged from 150 to 450 ms. The transient outward current underlying DE was presumed to be A-current because of the current's activation and inactivation characteristics and its elimination by 4-aminopyridine (4-AP). 4. Adaptation was examined by applying depolarizing current for 2.0 s and measuring the frequency of evoked action potentials. Although there was a large degree of variability in the degree of adaptation, PIR cells tended to express less adaptation than DE and Non cells. Nearly three-fourths of all NA neurons adapted rapidly (i.e., 50% adaptation in < 200 ms), but PIR cells tended to adapt faster than DE and Non cells. PTH after a train of action potentials was relatively rare and occurred more often in DE cells (43%) and Non cells (33%) than in PIR cells (13%). PTH had a magnitude of up to 18 mV and time constants that reflected the presence of one (1.7 +/- 1.4 s, mean +/- SD) or two components (0.28 +/- 0.13 and 4.1 +/- 2.2 s). 5. The action potential amplitude and duration and the resting membrane potential were similar for all NA neurons. PIR cells, however, had a smaller action potential undershoot and input resistance compared with DE and Non cells. 6. In 52 NA neurons intracellularly filled with Lucifer yellow dye, the calculated somatic surface area of PIR cells (3,300 +/-1,600-mu-m2) was significantly larger than DE cells (1,600 +/- 580-mu-m2) but not for Non cells (2,500 +/- 1,400-mu-m2). 7. We conclude that 1) NA neurons exhibit specific cellular properties such as PIR, DE, and PTH that probably contribute to shaping the firing pattern of ventral respiratory group neurons, because these properties are expressed in voltage ranges that are traversed by ventral respiratory group neurons in vivo; and 2) NA neurons can be classified into three major groups on the basis of the expression of PIR and DE as well as differences in terms of cell soma size, input resistance, membrane time constant, action potential undershoot, and distribution of PTH.