Abstract
Retinal circuits detect salient features of the visual world and report them to the brain through spike trains of retinal ganglion cells. The most abundant ganglion cell type in mice, the so-called W3 ganglion cell, selectively responds to movements of small objects. Where and how object motion sensitivity arises in the retina is incompletely understood. In this study, we use 2-photon-guided patch-clamp recordings to characterize responses of vesicular glutamate transporter 3 (VGluT3)-expressing amacrine cells (ACs) to a broad set of visual stimuli. We find that these ACs are object motion sensitive and analyze the synaptic mechanisms underlying this computation. Anatomical circuit reconstructions suggest that VGluT3-expressing ACs form glutamatergic synapses with W3 ganglion cells, and targeted recordings show that the tuning of W3 ganglion cells' excitatory input matches that of VGluT3-expressing ACs' responses. Synaptic excitation of W3 ganglion cells is diminished, and responses to object motion are suppressed in mice lacking VGluT3. Object motion, thus, is first detected by VGluT3-expressing ACs, which provide feature-selective excitatory input to W3 ganglion cells.DOI: http://dx.doi.org/10.7554/eLife.08025.001
Highlights
A diverse array of circuits in the retina processes signals from photoreceptors and parses information into spike trains of 20–30 types of retinal ganglion cells (RGCs), each encoding distinct aspects of the visual scene (Masland, 2012)
Postsynaptic inhibition and spike thresholds sharpen the tuning of W3-RGCs, similar to other OMS and local-edge-detector RGCs, key response properties appear to be inherited from their excitatory input
We find that VG3-amacrine cells (ACs), like W3-RGCs, combine properties of OMS and local-edgedetector neurons and selectively detect movements of small objects
Summary
A diverse array of circuits in the retina processes signals from photoreceptors and parses information into spike trains of 20–30 types of retinal ganglion cells (RGCs), each encoding distinct aspects of the visual scene (Masland, 2012). We obtained VG3-Cre mice (Grimes et al, 2011) in which all VG3-ACs express Cre (Figure 1—figure supplement 1), crossed them to Ai9, and targeted fluorescent somata in the inner nuclear layer (INL) for whole-cell patch-clamp recordings.
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