Calcium dynamics during NMDA-induced membrane potential oscillations in lamprey spinal neurons – contribution of L-type calcium channels (CaV1.3)

Authors

  • Di Wang,

    1. Department of Physiology, Liaoning Medical University, Jinzhou, PR China
    2. Nobel Institute for Neurophysiology, Department of Neuroscience, Karolinska Institutet, SE-171 77 Stockholm, Sweden
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  • Sten Grillner,

    1. Nobel Institute for Neurophysiology, Department of Neuroscience, Karolinska Institutet, SE-171 77 Stockholm, Sweden
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  • Peter Wallén

    1. Nobel Institute for Neurophysiology, Department of Neuroscience, Karolinska Institutet, SE-171 77 Stockholm, Sweden
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P. Wallén: Nobel Institute for Neurophysiology, Department of Neuroscience, Karolinska Institutet, SE-171 77 Stockholm, Sweden. Email: peter.wallen@ki.se

Key points

  • • 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.

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