Organization and development of direction-selective circuits in the retina

Abstract

The direction-selective circuit in the retina extracts the directional information of image motion in the visual scene. It is a classic model for neural circuit analysis because its input and output are well-defined and accessible to physiological measurements. However, the neural basis of direction selectivity is still not fully understood. Indeed, this ostensibly simple computation arises from a collection of complex neural mechanisms at all levels of circuit organization. In this review, we describe recent advances in genetic, imaging and optogenetic techniques that have improved our understanding of the synaptic organization and development underlying retinal direction selectivity.

Figure 1. Major cellular components of the ON-OFF direction selective circuit and functional output of an ON-OFF direction selective ganglion cell (DSGC)

(a) Schematic drawings of mammalian retina and the key cell types involved in direction selectivity. ON- and OFF bipolar cells (BP) relay the light-evoked signals from the photoreceptors (PR) to the bistratified dendritic arbors of ON-OFF DSGCs at the sublaminae 2 and 4 (S2 and S4) of the inner plexiform layer (IPL). Two mirror symmetric populations of SACs, whose cell bodies reside in the inner nuclear layer (INL) and ganglion cell layer (GCL), modify forward transmission at S2 and S4 respectively. (b) NEUROLUCIDA reconstructions of the dendrites from the ON sublamina and side views of the complete dendritic arborizations from a synaptically connected pair of SACs and DSGCs. Dots represent dendritic contacts, with cofasciculation segments coloured white and the rest coloured purple. Scale bar, 25 mm. (Modified from ). (c) Spiking responses from loose patch cell recordings of an ON-OFF DSGC to a flashing spot. (d) Spike traces from loose patch cell recordings and a polar plot showing the response of the same ON-OFF DSGC in (c) to a moving bar in 12 directions, (c) and (d) are modified, with permission, from .

Figure 2. Schematic model demonstrating the pattern of inhibitory and excitatory input to ON-OFF DSGCs during image motion

For simplicity, only the ON dendritic arbor of the ON-OFF DSGC is illustrated. (a) GABAergic input is stronger between the DSGC and SAC processes pointing to the null direction, which is opposite to the preferred (Pref) direction ^{, ,} . The enhanced GABAergic conductance may be due to a greater number of synapses and/or to a stronger unitary conductance at each synapse. Arrows: preferred directions (Pref) for the DSGC (grey) and SAC processes (blue). (b) Cholinergic input is symmetric during direct stimulation via paired recordings, but asymmetric during image motion . Black dots represent cholinergic synapses. When the image is moving towards the null direction of the DSGC (red arrows), the cholinergic input is suppressed. The inhibitory circuit that mediates this suppression is currently not known. (c) Glutamatergic input from bipolar cells is reduced during null-direction motion (red arrows)