The Journal of Neurophysiology Vol. 77 No. 6 June 1997, pp. 2910-2924
Copyright ©1997 The American Physiological Society

Multiple Effects of Serotonin on Membrane Properties of Trigeminal Motoneurons In Vitro

C. F. Hsiao, P. R. Trueblood, M. S. Levine, and S. H. Chandler

Department of Physiological Science and the Mental Retardation Research Center, University of California at Los Angeles, California 90095

Hsiao, C. F., P. R. Trueblood, M. S. Levine, and S. H. Chandler. Multiple effects of serotonin on membrane properties of trigeminal motoneurons in vitro. J. Neurophysiol. 77: 2910-2924, 1997. Intracellular recordings from guinea pig trigeminal motoneurons (TMNs) in brain stem slices were used to determine the underlying ionic mechanisms responsible for our previously demonstrated enhancement of TMN excitability during jaw movements by serotonin (5-HT). 5-HT (0.5-100 µM) depolarized motoneurons and increased input resistance in the majority of neurons tested. Additionally, 5-HT reduced the amplitude of the postspike medium-duration afterhyperpolarization, decreased the current threshold for maintained spike discharge, and increased the maximum slope of the steady-state spike frequency-current relationship. Under voltage clamp, from holding potentials close to resting potential, 5-HT produced an inward current and a decrease in instantaneous slope conductance, suggesting a reduction in a resting K⁺ leak conductance (I_leak). The instantaneous current-voltage (I-V) relationship for the inward 5-HT current (I_5-HT) was linear throughout most of the voltage range tested. However, the steady-state I-V relationship showed some degree of inward rectification at potentials starting around 70 mV. The mean reversal potential for the instantaneous I_5-HT was 86.2 ± 4.5 (SE) mV (n = 9), a value slightly negative to the predicted potassium equilibrium potential of 82 mV in these neurons. In the presence of 2 mM Ba²⁺, 5-HT application did not produce a further reduction in input conductance, but did expose a Ba²⁺-insensitive residual inward current that was resistant to Cs⁺ application. The instantaneousI-V relationship during 5-HT application in the presence of Ba²⁺ was shifted downward and parallel to control, suggesting that Ba²⁺ and 5-HT block the same resting I_leak. The residual Ba²⁺- and Cs⁺-insensitive component of the total inward I_5-HT was voltage independent and was blocked when the extracellular Na⁺ was replaced by choline, suggesting that the predominant charge carrier for this residual current is Na⁺. 5-HT enhanced a hyperpolarization-activated cationic current, I_h. In the presence of Ba²⁺, the time course of I_5-HT resembled that of I_h and showed a similar voltage dependence that was blocked by extracellular Cs⁺ (1-3 mM). The effects of 5-HT on membrane potential, input resistance, and I_h were partially mimicked by 5-HT₂ agonists and suppressed by 5-HT₂ antagonists. It is concluded that 5-HT enhances TMN membrane excitability through modulation of multiple intrinsic membrane conductances. This provides for a mechanism(s) to fine tune the input-output discharge properties of these neurons, thus providing them with greater flexibility in output in response to time-varying synaptic inputs during various movements of the jaw.

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