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The Journal of Neuroscience, August 18, 2004, 24(33):7335-7343; doi:10.1523/JNEUROSCI.1275-04.2004

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Behavioral/Systems/Cognitive
A Unique Role for Kv3 Voltage-Gated Potassium Channels in Starburst Amacrine Cell Signaling in Mouse Retina

Ander Ozaita,^1,2 * Jerome Petit-Jacques,^1,2,3 * Béla Völgyi,^1,3 * Chi Shun Ho,⁴ Rolf H. Joho,⁴ Stewart A. Bloomfield,^1,3 and Bernardo Rudy^1,2

Departments of ¹Physiology and Neuroscience, ²Biochemistry, and ³Ophthalmology, New York University School of Medicine, New York, New York 10016, and ⁴Center for Basic Neuroscience, The University of Texas Southwestern Medical Center, Dallas, Texas 75390-9111

Direction-selective retinal ganglion cells show an increased activity evoked by light stimuli moving in the preferred direction. This selectivity is governed by direction-selective inhibition from starburst amacrine cells occurring during stimulus movement in the opposite or null direction. To understand the intrinsic membrane properties of starburst cells responsible for direction-selective GABA release, we performed whole-cell recordings from starburst cells in mouse retina. Voltage-clamp recordings revealed prominent voltage-dependent K⁺ currents. The currents were mostly blocked by 1 mM TEA, activated rapidly at voltages more positive than -20 mV, and deactivated quickly, properties reminiscent of the currents carried by the Kv3 subfamily of K⁺ channels. Immunoblots confirmed the presence of Kv3.1 and Kv3.2 proteins in retina and immunohistochemistry revealed their expression in starburst cell somata and dendrites. The Kv3-like current in starburst cells was absent in Kv3.1-Kv3.2 knock-out mice. Current-clamp recordings showed that the fast activation of the Kv3 channels provides a voltage-dependent shunt that limits depolarization of the soma to potentials more positive than -20 mV. This provides a mechanism likely to contribute to the electrical isolation of individual starburst cell dendrites, a property thought essential for direction selectivity. This function of Kv3 channels differs from that in other neurons where they facilitate high-frequency repetitive firing. Moreover, we found a gradient in the intensity of Kv3.1b immunolabeling favoring proximal regions of starburst cells. We hypothesize that this Kv3 channel gradient contributes to the preference for centrifugal signal flow in dendrites underlying direction-selective GABA release from starburst amacrine cells

Key words: retina; direction selectivity; potassium channels; amacrine cells; GABAergic; inhibition

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Received April 5, 2004; revised July 6, 2004; accepted July 7, 2004.

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