The Synaptic Mechanism of Direction Selectivity in Distal Processes of Starburst Amacrine Cells

SummaryPatch-clamp recordings revealed that distal processes of starburst amacrine cells (SACs) received largely excitatory synaptic input from the receptive field center and nearly purely inhibitory inputs from the surround during both stationary and moving light stimulations. The direct surround inhibition was mediated mainly by reciprocal GABAA synapses between opposing SACs, which provided leading and prolonged inhibition during centripetal stimulus motion. Simultaneous Ca2+ imaging and current-clamp recording during apparent-motion stimulation further demonstrated the contributions of both centrifugal excitation and GABAA/C-receptor-mediated centripetal inhibition to the direction-selective Ca2+ responses in SAC distal processes. Thus, by placing GABA release sites in electrotonically semi-isolated distal processes and endowing these sites with reciprocal GABAA synapses, SACs use a radial-symmetric center-surround receptive field structure to build a polar-asymmetric circuitry. This circuitry may integrate at least three levels of interactions—center excitation, surround inhibition, and reciprocal inhibitions that amplify the center-surround antagonism—to generate robust direction selectivity in the distal processes.