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The Journal of Neuroscience, April 22, 2009, 29(16):5343-5353; doi:10.1523/JNEUROSCI.5458-08.2009

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Cellular/Molecular
Staircase Currents in Motoneurons: Insight into the Spatial Arrangement of Calcium Channels in the Dendritic Tree

Kevin P. Carlin,^3 * Tuan V. Bui,^2 * Yue Dai,³ and Robert M. Brownstone^1,2

Departments of ¹Surgery (Neurosurgery) and ²Anatomy and Neurobiology, Dalhousie University, Halifax, Nova Scotia B3H 1X5, Canada, and ³Department of Physiology, University of Manitoba, Winnipeg, Manitoba R3T 2N2, Canada

Correspondence should be addressed to Robert M. Brownstone, Department of Anatomy and Neurobiology, Dalhousie University, 14A Tupper Building, 5850 College Street, Halifax, NS B3H 1X5, Canada. Email: rob.brownstone{at}dal.ca

In spinal motoneurons, activation of dendritically located depolarizing conductances can lead to amplification of synaptic inputs and the production of plateau potentials. Immunohistochemical and computational studies have implicated dendritic Ca_V1.3 channels in this amplification and suggest that Ca_V1.3 channels in spinal motoneurons may be organized in clusters in the dendritic tree. Our goal was to provide physiological evidence for the presence of multiple discrete clusters of voltage-gated calcium channels in spinal motoneurons and to explore the spatial arrangement of these clusters in the dendritic tree. We recorded voltage-gated calcium currents from spinal motoneurons in slices of mature mouse spinal cords. We demonstrate that single somatic voltage-clamp steps can elicit multiple inward currents with varying delays to onset, resulting in a current with a "staircase"-like appearance. Recordings from cultured dorsal root ganglion cells at different stages of neurite development provide evidence that these currents arise from the unclamped portions of the dendritic tree. Finally, both voltage- and current-clamp data were used to constrain computer models of a motoneuron. The resultant simulations impose two conditions on the spatial distribution of Ca_V channels in motoneuron dendrites: one of asymmetry relative to the soma and another of spatial separation between clusters of Ca_V channels. We propose that this compartmentalization would provide motoneurons with the ability to process multiple sources of input in parallel and integrate this processed information to produce appropriate trains of action potentials for the intended motor behavior.

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Received Oct. 20, 2008; revised Feb. 16, 2009; accepted March 16, 2009.

Correspondence should be addressed to Robert M. Brownstone, Department of Anatomy and Neurobiology, Dalhousie University, 14A Tupper Building, 5850 College Street, Halifax, NS B3H 1X5, Canada. Email: rob.brownstone{at}dal.ca

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