Calcium dynamics during NMDA-induced membrane potential oscillations in lamprey spinal neurons – contribution of L-type calcium channels (CaV1.3)
Article first published online: 20 MAR 2013
© 2013 The Authors. The Journal of Physiology © 2013 The Physiological Society
The Journal of Physiology
Volume 591, Issue 10, pages 2509–2521, May 2013
How to Cite
Wang, D., Grillner, S. and Wallén, P. (2013), Calcium dynamics during NMDA-induced membrane potential oscillations in lamprey spinal neurons – contribution of L-type calcium channels (CaV1.3). The Journal of Physiology, 591: 2509–2521. doi: 10.1113/jphysiol.2012.248526
- Issue published online: 14 MAY 2013
- Article first published online: 20 MAR 2013
- Accepted manuscript online: 27 FEB 2013 08:45AM EST
- (Received 16 November 2012; accepted after revision 20 February 2013; first published online 25 February 2013)
- • Intrinsic NMDA-induced oscillations of membrane potential are important for the operation of the spinal locomotor network in the lamprey, and involve a cyclic influx of calcium.
- • The spatial and temporal calcium dynamics during oscillations were investigated, using calcium imaging combined with intracellular recordings.
- • Calcium fluctuations were observed in both soma and dendrites, timed to the membrane potential oscillations, with the peak in distal dendritic locations typically occurring earlier than in the soma.
- • The L-type calcium channel antagonist nimodipine prolonged the plateau phase of membrane potential oscillations, whereas the agonist Bay K 8644 shortened the plateau. Bay K 8644 also increased the amplitude of calcium fluctuations, particularly in distal dendrites. On the contrary, nimodipine decreased calcium fluctuation amplitudes.
- • Low-voltage-activated L-type (CaV1.3-like) calcium channels at distal dendrites are activated during membrane potential oscillations. The resulting calcium influx contributes to the activation of calcium-activated potassium channels and thereby the control of the plateau duration during oscillations.
Abstract NMDA receptor-dependent, intrinsic membrane potential oscillations are an important element in the operation of the lamprey locomotor network. They involve a cyclic influx of calcium, leading to an activation of calcium-activated potassium (KCa) channels that in turn contributes to the termination of the depolarized plateau and membrane repolarization. In this study, we have investigated the calcium dynamics in different regions of lamprey spinal neurons during membrane potential oscillations, using confocal calcium imaging in combination with intracellular recordings. Calcium fluctuations were observed in both soma and dendrites, timed to the oscillations. The calcium level increased sharply at the onset of membrane depolarization, to reach its maximum by the end of the plateau. The calcium peak in distal dendrites typically occurred earlier than in the soma during the oscillatory cycle. The L-type calcium channel blocker nimodipine increased the duration of the depolarized plateau phase in most cells tested, whereas the agonist Bay K 8644 decreased plateau duration. Bay K 8644 increased the amplitude of calcium fluctuations, particularly in distal dendrites, whereas nimodipine caused a decrease, suggesting that L-type low-voltage-activated calcium channels are mainly localized in these regions. Our results thus indicate that dendritic CaV1.3-like calcium channels are activated during NMDA-mediated membrane potential oscillations. This calcium influx activates KCa channels involved in plateau termination.