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The Journal of Neuroscience, September 15, 2002, 22(18):8230-8237
Vanilloid-Sensitive Afferents Activate Neurons with Prominent A-Type Potassium Currents in Nucleus Tractus Solitarius
Timothy W. Bailey, Young-Ho Jin, Mark W. Doyle, and Michael C. Andresen Department of Physiology and Pharmacology, Oregon Health and Science University, Portland, Oregon 97201-3098
Cranial visceral afferents innervate second-order nucleus tractus solitarius (NTS) neurons via myelinated (A-type) and unmyelinated (C-type) axons in the solitary tract (ST). A- and C-type afferents often evoke reflexes with distinct performance differences, especially with regard to their frequency-dependent properties. In horizontal brainstem slices, we used the vanilloid receptor 1 agonist capsaicin (CAP; 100 nM) to identify CAP-sensitive and CAP-resistant ST afferent pathways to second-order NTS neurons and tested whether these two groups of neurons had similar intrinsic potassium currents. ST stimulation evoked monosynaptic EPSCs identified by minimal synaptic jitter (<150 µsec) and divided into two groups: CAP-sensitive (n = 37) and CAP-resistant (n = 22). EPSCs in CAP-sensitive neurons had longer latencies (5.1 ± 0.3 vs 3.6 ± 0.3 msec; p = 0.001) but similar jitter (p = 0.57) compared with CAP-resistant neurons, respectively. Transient outward currents (TOCs) were significantly greater in CAP-sensitive than in CAP-resistant neurons. Steady-state currents were similar in both groups. 4-Aminopyridine or depolarized conditioning blocked the TOC, but tetraethylammonium had no effect. Voltage-dependent activation and inactivation of TOC were consistent with an A-type K+ current, IKA. In current clamp, the activation of IKA reduced neuronal excitability and action potential responses to ST transmission. Our results suggest that the potassium-channel differences of second-order NTS neurons contribute to the differential processing of A- and C-type cranial visceral afferents beginning as early as this first central neuron. IKA can act as a frequency transmission filter and may represent a key target for the modulation of temporal processing of reflex responsiveness such as within the baroreflex arc.
Key words: sensory; vanilloid; glutamate; presynaptic modulation; autonomic; visceral; baroreceptor; baroreflex
Copyright © 2002 Society for Neuroscience 0270-6474/02/22188230-08$05.00/0
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