Spatially displaced excitation contributes to the encoding of interrupted motion by a retinal direction-selective circuit.

Albert Chen,Stephanie E Palmer,Jennifer Ding,Janet Chung,David M Berson,Mofei Wu,Wei Wei,Hector Acaron Ledesma

doi:10.7554/elife.68181

Albert Chen, Stephanie E Palmer + Show 6 more

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https://doi.org/10.7554/elife.68181

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Abstract

Spatially distributed excitation and inhibition collectively shape a visual neuron's receptive field (RF) properties. In the direction-selective circuit of the mammalian retina, the role of strong null-direction inhibition of On-Off direction-selective ganglion cells (On-Off DSGCs) on their direction selectivity is well-studied. However, how excitatory inputs influence the On-Off DSGC's visual response is underexplored. Here, we report that On-Off DSGCs have a spatially displaced glutamatergic receptive field along their horizontal preferred-null motion axes. This displaced receptive field contributes to DSGC null-direction spiking during interrupted motion trajectories. Theoretical analyses indicate that population responses during interrupted motion may help populations of On-Off DSGCs signal the spatial location of moving objects in complex, naturalistic visual environments. Our study highlights that the direction-selective circuit exploits separate sets of mechanisms under different stimulus conditions, and these mechanisms may help encode multiple visual features.

Highlights

How do sensory systems convert sensory inputs into behaviorally relevant neural signals? This question has been extensively investigated in the early visual system, where a neuron’s responses to a set of parameterizable visual stimuli can be systematically probed to reveal a cell’s receptive field (RF) properties in space and time.It has been increasingly appreciated that different visual stimuli can engage different mechanisms to shape the neuronal RF even at the earliest stage of visual processing in the retina
The spot stimulus delivered to the pDSGC RF periphery uncovered an asymmetric RF organization where some spots evoked maximal spiking (Max) and other spots presented to the opposite regions (Opp) across the dendritic span evoked minimal responses (Figures 1B – 1C, Figure 1-figure supplement 1A – 1B)
Our study reveals a new form of asymmetry in the direction-selective circuit: a spatial displacement of glutamatergic inputs to the preferred side of the Off dendrites (On)-Off pDSGCs due to a non-uniform distribution of synaptic conductances across the pDSGC dendritic span

Summary

Introduction

How do sensory systems convert sensory inputs into behaviorally relevant neural signals? This question has been extensively investigated in the early visual system, where a neuron’s responses to a set of parameterizable visual stimuli can be systematically probed to reveal a cell’s receptive field (RF) properties in space and time. Theoretical analyses of the On-Off DSGC population response allow us to speculate about the ethological relevance of the displaced RF in processing complex natural scenes, suggesting that it can allow for better estimation of object location when a moving object emerges from behind an occluder. We term this type of motion ‘interrupted motion’ to distinguish it from more standard smooth motion stimuli. This phenomenon might allow synchronous firing from different subtypes of DSGCs to serve as a useful alarm signal in complex scenes

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