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The Journal of Neuroscience, November 23, 2005, 25(47):10863-10873; doi:10.1523/JNEUROSCI.3436-05.2005

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Cellular/Molecular
A-Type and T-Type Currents Interact to Produce a Novel Spike Latency-Voltage Relationship in Cerebellar Stellate Cells

Michael L. Molineux, ^* Fernando R. Fernandez, ^* W. Hamish Mehaffey, and Ray W. Turner

Hotchkiss Brain Institute, University of Calgary, Calgary, Alberta, Canada T2N 4N1

The modification of first-spike latencies by low-threshold and inactivating K⁺ currents (I_A) have important implications in neuronal coding and synaptic integration. To date, cells in which first-spike latency characteristics have been analyzed have shown that increased hyperpolarization results in longer first-spike latencies, producing a monotonic relationship between first-spike latency and membrane voltage. Previous work has established that cerebellar stellate cells express members of the K_v4 potassium channel subfamily, which underlie I_A in many central neurons. Spike timing in stellate cells could be particularly important to cerebellar output, because the discharge of even single spikes can significantly delay spike discharge in postsynaptic Purkinje cells. In the present work, we studied the first-spike latency characteristics of stellate cells. We show that first-spike latency is nonmonotonic, such that intermediate levels of prehyperpolarization produce the longest spike latencies, whereas greater hyperpolarization or depolarization reduces spike latency. Moreover, the range of first-spike latency values can be substantial in spanning 20-128 ms with preceding membrane shifts of <10 mV. Using patch clamp and modeling, we illustrate that spike latency characteristics are the product of an interplay between I_A and low-threshold calcium current (I_T) that requires a steady-state difference in the inactivation parameters of the currents. Furthermore, we show that the unique first-spike latency characteristics of stellate cells have important implications for the integration of coincident IPSPs and EPSPs, such that inhibition can shift first-spike latency to differentially modulate the probability of firing.

Key words: I_A; I_T; I_H; first-spike latency; FSL; synaptic integration; cerebellum; K_v4; Ca_v3; stellate cell

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Received June 28, 2005; revised October 5, 2005; accepted October 5, 2005.

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