Vanilloid-sensitive afferents activate neurons with prominent A-type potassium currents in nucleus tractus solitarius

Timothy W. Bailey, Young Ho Jin, Mark W. Doyle, Michael C. Andresen

Research output: Contribution to journalArticle

52 Scopus citations

Abstract

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.

Original languageEnglish (US)
Pages (from-to)8230-8237
Number of pages8
JournalJournal of Neuroscience
Volume22
Issue number18
DOIs
StatePublished - Sep 15 2002

Keywords

  • Autonomic
  • Baroreceptor
  • Baroreflex
  • Glutamate
  • Presynaptic modulation
  • Sensory
  • Vanilloid
  • Visceral

ASJC Scopus subject areas

  • Neuroscience(all)

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