Territorial organization of direction-selective ganglion cells in rabbit retina

Abstract

The On-Off direction-selective (DS) ganglion cells in the rabbit retina comprise four discrete subtypes that orthogonally code the direction of image motion. This study examined the dendritic relationships between different subtypes of On-Off DS cells, which were identified by their distinctive type 1 bistratified (BiS 1) morphology following the intracellular injection of a biotinylated tracer or Lucifer yellow under direct microscopic control. The dendrites of BiS 1 cells that had closely spaced somata, which presumably comprised subtypes of On-Off DS cells with different preferred directions, were not randomly superimposed but were fasciculated into loose bundles. By contrast, tracer coupling revealed that neighboring On-Off DS cells of one subtype were highly territorial, providing complete coverage of the retina with minimal overlap. This mirrors, on a larger scale, the territorial organization within the dendritic tree of individual DS cells, suggesting that similar interactions shape both the branching pattern and the spatial extent of these neurons. Moreover, the dendrites at the edge of the dendritic field often formed tip-to-shaft or tip-to-tip contacts with dendrites from coupled cells, thus appearing to form closed dendritic loops that may be equivalent to those found within the dendritic tree. Consequently, the dendrites of one subtype are distributed uniformly and economically across the retina. The resulting plexus forms a strikingly regular scaffold on which the presynaptic interneurons generate direction selectivity.