Stimulus-dependent recruitment of lateral inhibition underlies retinal direction selectivity.

Qiang Chen,Wei Wei,Zhe Pei,David Koren

doi:10.7554/elife.21053

Abstract

The dendrites of starburst amacrine cells (SACs) in the mammalian retina are preferentially activated by motion in the centrifugal direction, a property that is important for generating direction selectivity in direction selective ganglion cells (DSGCs). A candidate mechanism underlying the centrifugal direction selectivity of SAC dendrites is synaptic inhibition onto SACs. Here we disrupted this inhibition by perturbing distinct sets of GABAergic inputs onto SACs - removing either GABA release or GABA receptors from SACs. We found that lateral inhibition onto Off SACs from non-SAC amacrine cells is required for optimal direction selectivity of the Off pathway. In contrast, lateral inhibition onto On SACs is not necessary for direction selectivity of the On pathway when the moving object is on a homogenous background, but is required when the background is noisy. These results demonstrate that distinct sets of inhibitory mechanisms are recruited to generate direction selectivity under different visual conditions.

Highlights

Encoding of motion direction first appears in the inner plexiform layer (IPL) of mammalian retina (Barlow and Hill, 1963; Barlow and Levick, 1965; Oyster and Barlow, 1967), where positive- and negative-contrast motion stimuli are processed in anatomically distinct On and Off sublaminae
We have previously shown that these KO mice display disrupted GABAergic inhibition from SACs to direction selective ganglion cells (DSGCs) and no detectable developmental compensation (Pei et al, 2015)
Evoked GABAergic inhibitory postsynaptic currents (IPSCs) were measured from one SAC at holding potential of À80 mV while the other SAC was depolarized to 0 mV for 20 ms in voltage clamp configuration

Summary

Introduction

Encoding of motion direction first appears in the inner plexiform layer (IPL) of mammalian retina (Barlow and Hill, 1963; Barlow and Levick, 1965; Oyster and Barlow, 1967), where positive- and negative-contrast motion stimuli are processed in anatomically distinct On and Off sublaminae. One of the main output neurons that signal motion direction from the retina to higher visual centers, the On-Off DSGC, has bistratified dendritic arbors that receive directionally tuned inhibition from On and Off subtypes of SACs at each of these sublamina (Figure 1A) (Famiglietti, 1983, 1992; Kittila and Massey, 1997; Taylor and Vaney, 2002). GABAergic inputs preferentially originate from SAC dendritic sectors that extend in the anti-preferred (null) direction of On-Off DSGCs (Figure 1B, Briggman et al, 2011; Fried et al, 2002; Lee et al, 2010; Wei et al, 2011). The dendritic sectors of SACs are electrotonically isolated and directionally tuned to motion in the centrifugal direction (from soma to dendritic tips) (Figure 1B, Euler et al, 2002). Since null-direction motion for a DSGC corresponds to centrifugal motion for its presynaptic SAC dendrites, maximal GABA release from SACs to DSGCs occurs during motion in the null direction (Figure 1B)

Methods

Results

Conclusion