Computation of the Directional Asymmetry in Starburst Amacrine Cell Dendrites Involves Voltage–Gated Channels

Abstract

Purpose: : The visual system dedicates substantial resources to the detection of image motion and its direction. In the retina this direction selectivity has been intensely studied for over 40 years. Nevertheless, the mechanism underlying the initial computation of the direction signal is still not fully understood. In this study we show that voltage–gated channels – very likely Ca²⁺ channels – play a major role in the dendrite–autonomous processing of direction selectivity in retinal starburst amacrine cells, where direction–selectivity is thought to arise.

Methods: : The electrical properties and Ca²⁺ responses of starburst cells were assessed using whole–cell tight–seal recordings and two–photon microscopy in whole–mounted rabbit retina during visual stimulation and/or voltage–clamp protocols. Specific motion stimuli (concentric sinusoidal wave gratings) which do not cancel out signals from different dendritic sectors and correspond to the radial morphological symmetry of starburst cells, were used to study the differential processing in response to motion direction (i.e. centrifugal or 'out–going' versus centripetal or 'in–going').

Results: : The dependence of electrical response non–linearity on motion direction and membrane potential suggests differential activation of voltage–gated channels. Ca²⁺ responses to voltage steps and pharmacological experiments indicate the involvement of Ca²⁺ channels and the existence of a voltage gradient between dendritic tips and soma, which seems at least partly to be caused by a sustained activation of Glutamate receptors. Detailed analysis and model calculations show that such a gradient and the motion direction–dependent activation of voltage gated Ca²⁺ channels might be central to starburst–cell motion responses.

Conclusions: : We show that the dendrite–autonomous computation of motion direction in starburst amacrine cells relies on the differential activation of voltage–gated channels.

Keywords: retina: proximal (bipolar, amacrine, and ganglion cells) • ion channels • calcium