The Journal of Neurophysiology Vol. 79 No. 6 June 1998, pp. 2847-2856
Copyright ©1998 The American Physiological Society

Ionic Basis for Serotonin-Induced Bistable Membrane Properties in Guinea Pig Trigeminal Motoneurons

Chie-Fang Hsiao¹, Christopher A. Del Negro¹, Peggy R. Trueblood², and Scott H. Chandler¹

¹ Department of Physiological Science, University of California at Los Angeles, Los Angeles, 90095-1568; and ² Department of Physical Therapy, California State University at Fresno, Fresno, California 93740

Hsiao, Chie-Fang, Christopher A. Del Negro, Peggy R. Trueblood, and Scott H. Chandler. Ionic basis for serotonin-induced bistable membrane properties in guinea pig trigeminal motoneurons. J. Neurophysiol. 79: 2847-2856, 1998. Intracellular recordings and pharmacological manipulations were employed to investigate the ionic basis for serotonin-induced bistable membrane behaviors in guinea pig trigeminal motoneurons (TMNs). In voltage clamp, 10 µM serotonin (5-HT) induced a region of negative slope resistance (NSR) in the steady-state current-voltage (I-V) relationship at potentials less negative than 58 mV, creating the necessary conditions for membrane bistability. The contributions of sustained Na⁺ and Ca²⁺ currents to the generation of the NSR were investigated using specific ion channel antagonists and agonists. The NSR was eliminated by the L-type Ca²⁺ channel antagonist nifedipine (5-10 µM), indicating the contribution of L channels. In nifedipine, inward rectification was present in the I-V relationship in a similar voltage range (greater than 58 mV). This region was subsequently linearized by tetrodotoxin (TTX), indicating the presence of a persistent Na⁺ current. When the 5-HT-induced NSR was eliminated by perfusion in low Ca²⁺ solution (0.4 mM), it was restored by the Na⁺ channel agonist veratridine (10 µM). Commensurate with bistability, in current clamp during bath application of 5-HT, plateau potentials were elicited by transient depolarizing or hyperpolarizing stimuli. Plateau potentials evoked by depolarization were observed under control and TTX conditions, but were blocked by nifedipine, suggesting the participation of an L-type Ca²⁺ current. Plateau potentials initiated after release from hyperpolarization (anode break) were blocked by 300 µM Ni²⁺, suggesting the responses relied on deinactivation of a T-type Ca²⁺ current. Conditional bursting was also observed in 5-HT. Nifedipine or low Ca²⁺ solutions blocked bursting, and the L-channel agonist Bay K 8644 (10 µM) extended the duration of individual bursts, demonstrating the role of L-type Ca²⁺ currents. Interestingly, when bursting was blocked by nifedipine or low Ca²⁺, it could be restored by veratridine application via enhancement of the persistent Na⁺ current. We conclude that bistable membrane behaviors in TMNs are mediated by L-type Ca²⁺ and persistent Na⁺ currents. 5-HT is associated with enhancement of TMN activity during oral-motor activity; the induction of bistable membrane properties by 5-HT represents a cellular mechanism for this enhancement.

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