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Volume 17, Number 18, Issue of September 15, 1997 pp. 6839-6849
Copyright ©1997 Society for Neuroscience

Serotonergic Inhibition of the T-Type and High Voltage-Activated Ca²⁺ Currents in the Primary Sensory Neurons of Xenopus Larvae

Received April 30, 1997; revised June 17, 1997; accepted June 26, 1997.

Qian-Quan Sun and Nicholas Dale

School of Biological and Medical Sciences, St. Andrews University, St. Andrews, Fife, KY16 9TS United Kingdom

The primary sensory Rohon-Beard (R-B) neurons of Xenopus larvae are highly analogous to the C fibers of the mammalian pain pathway. We explored the actions of 5-HT by studying the modulation of Ca²⁺ currents. In ~80% of the acutely isolated R-B neurons, 5-HT inhibited the high voltage-activated (HVA) currents by 16% (n = 29) and the T-type currents by 24% (n = 41). The modulation of the T-type and the HVA currents was mimicked by selective 5-HT_1A and 5-HT_1D agonists: 8-OH-DPAT and L-694,247. The effects of the agonists were blocked by their respective 5-HT_1A or 5-HT_1D antagonists: p-MPPI and GR127935, suggesting that both 5-HT_1A and 5-HT_1D receptors were involved. Approximately 70% of the actions of 5-HT on HVA currents was occluded by -conotoxin-GVIA (N-type channel blocker), whereas the rest of the modulation (~30%) was occluded by <100 nM -agatoxin-TK (P/Q-type channel blocker). This suggests that 5-HT acts on N- and P/Q-type Ca²⁺ channels. Neither the modulation of the T-type nor that of the HVA currents was accompanied by changes in their voltage-dependent kinetics. Cell-attached patch-clamp recordings suggest that the modulation of the T-type channel occurs through a membrane-delimited second messenger. We have studied the functional consequences of the modulation of T-type Ca²⁺ channels and have found that these channels play a role in spike initiation in R-B neurons. Modulation of T-type channels by 5-HT therefore could modulate the sensitivity of this sensory pathway by increasing the thresholds of R-B neurons. This is a new and potentially important locus for modulation of sensory pathways in vertebrates.

Key words: 5-HT_1A receptor; 5-HT_1D receptor; T-type Ca²⁺ currents; -conotoxin-GVIA; -agatoxin-TK; spike initiation; Xenopus; Rohon-Beard neurons

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