A reconstructed On–Off DSGC, with the soma and proximal (On) dendrites in red and distal (Off) dendrites in green. Image supplied by David Vaney, University of Queensland, Australia.

Horace Barlow and William Levick first described the properties of the direction-selective ganglion cells (DSGCs) in the retina way back in the mid-1960's. They reported that the most common type of DSGC, which is activated by the onset and termination of light (On–Off DSGC), responds preferentially to image motion, the direction of which is aligned with one of four axes (up, down, forward or backward). Despite the intervening years and the relative simplicity of the retinal system (the DSGCs are located only two or three synapses from the photoreceptors), the precise locus and mechanism of direction selectivity in the retina has remained elusive.

Although image motion in both the preferred direction and the opposite `null' direction activates interneurons that excite the DSGCs, electrophysiological evidence indicates that the excitation in the null direction is cancelled by spatially offset input from inhibitory interneurons. Conversely, in the preferred direction, the excitation and inhibition are not spatially and temporally coincident, and the excitation therefore escapes the inhibition. This circuitry therefore provides a mechanism for direction selectivity. But where and how does the interaction between excitation and inhibition occur?

Logically, the null-direction inhibition could act either presynaptically on the excitatory inputs to the DSGCs or postsynaptically on the dendrites of the DSGCs. A report in the September 29 issue of Science suggests that spatially asymmetric inhibition acts postsynaptically. Recordings made in rabbit retina whole-mounts by Taylor, He, Levick and Vaney showed that the DSGCs responded strongly to a stimulus moving in the preferred direction and only weakly to a stimulus moving in the null direction or orthogonal directions. However, when the patch clamp was used to load the DSGC with chloride, thereby preventing the excitatory and inhibitory channels in the DSGC membrane from interacting, the difference between the synaptic currents elicited by image motion in the preferred and null directions disappeared, consistent with a postsynaptic site. These results show that direction selectivity is conferred by null-direction inhibition, acting postsynaptically on ganglion cell dendrites. The simplicity of this system should now allow the precise characterization of the computational properties of dendrites, and this may have far-reaching implications for our view of computation in the brain.