A structural basis for omnidirectional connections between starburst amacrine cells and directionally selective ganglion cells in rabbit retina, with associated bipolar cells

Abstract

Directionally selective (DS) ganglion cells of rabbit retina are of two principal types. ON DS ganglion cells prefer low velocity in one of three directions of movement and project axons to the accessory optic system (AOS), whereas ON-OFF DS ganglion cells prefer higher velocity in one of four directions and project to tectum and thalamus. Each has a distinct, recognizable dendritic morphology, based upon the correlation of form, physiology, and central projections. In previous Golgi studies, ON and ON-OFF DS cells were found to be partly co-stratified, and ON-OFF DS cells were found to co-stratify with starburst amacrine (SA) cells, the cholinergic amacrine cells of the retina, which also contain elevated levels of GABA. SA cells are radially symmetrical, have synaptic boutons in a distal annular zone of its dendritic tree, are presynaptic primarily to ganglion cell dendrites, co-stratify with ON-OFF DS ganglion cells, and contain the neurotransmitters shown pharmacologically to be involved in DS responses. For these reasons, SA cells are thought to play a role in the DS mechanism. Several models of this mechanism have utilized SA cell dendritic geometry in a centrifugal, radial format to impose directional inputs on DS ganglion cells. The opportunity to examine Golgi preparations containing ON DS ganglion cells that exhibit dendritic field overlap with both starburst amacrine cells and ON-OFF DS ganglion cells has resulted in several new findings. Co-stratification of ON DS ganglion cells and SA cells was demonstrated directly. Secondly, the boutons of single starburst amacrine cells make close contact in different lamellae of the starburst substratum in sublamina b of the inner plexiform layer (IPL) with three adjacent ON-OFF DS ganglion cells, which because of their considerable dendritic-field overlap must prefer different directions of motion. Thirdly, nearby presynaptic boutons of single SA cells make close contact with both ON and ON-OFF directionally selective ganglion cells. Single SA cells thus traverse all the lamellae of the starburst/cholinergic substratum. Fourthly, no directional bias is shown by vectors connecting the origins of dendritic sectors and distal synaptic boutons of starburst amacrine cells in those sectors that are in close contact with the dendrites of single ON or ON-OFF directionally selective ganglion cells. Fifthly, at least two distinct types of cone bipolar cell, nb1 and nb2, participate in the neural circuitry of directional selectivity for ON and ON-OFF DS ganglion cells, and nb1 cells co-stratify with ON DS cells. As a consequence of the second, third, and fourth points, starburst amacrine cells appear to be indiscriminate in their connections with DS ganglion cells, and therefore are unlikely to be the primary conduits for directionally selective information to retinal ganglion cells. This result is consistent with pharmacological studies showing that cholinergic antagonists do not block directional selectivity and a study showing that laser-ablation of SA cells does not reduce the directional selectivity of overlapping ON-OFF DS ganglion cells.