Abstract
We commemorate the 40th anniversary of the classical study undertaken by Barlow-Levick with a new challenge: to show how direction selectivity in the dendritic plexus of starburst amacrine cells is being computed. In the rabbit retina, although the cellular locus of direction selectivity is known to occur predominantly in the dendrites of starburst amacrine cells, the biophysical mechanism by which this takes place and its essential topography are yet to be specified with precision. A cotransmission model, involving a conjoint release of excitation/inhibition (i.e., a bisynaptic relay of endogenous ACh and GABA) from the distal varicosities of individual starburst amacrines, will be non-diphasic when the vesicular release of Ach and the non-vesicular, carrier-mediated release of GABA by transporters in the anterograde direction are preferentially suppressed by a negative feedback mechanism involving autoreceptors. Such biophysical mechanisms, including the asymmetric distribution of chloride cotransporters, explain somatofugal motion bias in starburst amacrine cells leading to autonomous functioning "subunits" that underlie the formation of directional selectivity. However, the functional independence of starburst amacrine cell "subunits" is partly a question of their network organization. The topography of directionally selective "subunits" resides in the plexus of crisscrossing dendrites of juxtaposed starburst amacrines, consisting of (i) serial synapses of three or more starburst amacrines and a ON-OFF directionally selective ganglion cell; (ii) a synaptic couplet between two starburst amacrines; and (iii) a conventional synapse between a starburst amacrine and a ON-OFF directionally selective ganglion cell. Cholinergic and GABAergic monosynaptic interactions between starburst amacrine cells, including glutamatergic interactions with cone bipolar cells, are involved in the primary circuit underlying directional selectivity. Furthermore, the secondary circuit underlying directional selectivity, consists of starburst amacrine cells and cone bipolar cells arranged in a "push-pull" configuration, interacting synaptically onto ON-OFF directionally selective ganglion cells.
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