Crossover Inhibition Generates Sustained Visual Responses in the Inner Retina

Juliana M Rosa,Sabine Ruehle,Huayu Ding,Leon Lagnado

doi:10.1016/j.neuron.2016.03.015

Juliana M Rosa, Sabine Ruehle + Show 2 more

Open Access

https://doi.org/10.1016/j.neuron.2016.03.015

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Abstract

SummaryIn daylight, the input to the retinal circuit is provided primarily by cone photoreceptors acting as band-pass filters, but the retinal output also contains neuronal populations transmitting sustained signals. Using in vivo imaging of genetically encoded calcium reporters, we investigated the circuits that generate these sustained channels within the inner retina of zebrafish. In OFF bipolar cells, sustained transmission was found to depend on crossover inhibition from the ON pathway through GABAergic amacrine cells. In ON bipolar cells, the amplitude of low-frequency signals was regulated by glycinergic amacrine cells, while GABAergic inhibition regulated the gain of band-pass signals. We also provide the first functional description of a subset of sustained ON bipolar cells in which synaptic activity was suppressed by fluctuations at frequencies above ∼0.2 Hz. These results map out the basic circuitry by which the inner retina generates sustained visual signals and describes a new function of crossover inhibition.

Highlights

The retina transforms the visual input through a number of parallel channels containing distinct spatio-temporal filters (Masland, 2001, 2012; Roska and Werblin, 2001; Wassle, 2004)
retinal ganglion cells (RGCs) dendrites receive excitatory synaptic inputs from bipolar cells with different filtering properties, and at least two distinct temporal filters have been recognized for decades: in the ‘‘transient’’ channel, RGCs receive excitatory inputs from bipolar cells acting as band-pass filters, while in the ‘‘sustained’’ channel, RGCs receive synaptic inputs with low-pass characteristics (Awatramani and Slaughter, 2000)
Only one temporal filter operates on the input to the retinal circuit under normal daylight: the band-pass filter provided by cone photoreceptors (Schnapf et al, 1990)

Summary

Introduction

The retina transforms the visual input through a number of parallel channels containing distinct spatio-temporal filters (Masland, 2001, 2012; Roska and Werblin, 2001; Wassle, 2004). Most of these channels are generated by the circuitry of the inner plexiform layer (IPL), which contains the dendrites of about $30 functional types of retinal ganglion cells (RGCs) stratifying in 5–6 different strata (Roska and Werblin, 2001). We ask a fundamental question: how are sustained channels generated by the circuitry of the inner retina?

Results

Discussion

Conclusion