Asymmetric retinal direction tuning predicts optokinetic eye movements across stimulus conditions
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Curated by eLife
eLife assessment
This work offers fundamental insights into how asymmetric behavioral features in optokinetic eye movements can be predicted from visual responses of direction-selective neurons in the retina. The electrophysiological experiments and model-based analyses are carefully performed and offer convincing conclusions. The presentation could improve in clarity for a stronger focus on the most important results.
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Abstract
Across species, the optokinetic reflex (OKR) stabilizes vision during self-motion. OKR occurs when ON direction-selective retinal ganglion cells (oDSGCs) detect slow, global image motion on the retina. How oDSGC activity is integrated centrally to generate behavior remains unknown. Here, we discover mechanisms that contribute to motion encoding in vertically tuned oDSGCs and leverage these findings to empirically define signal transformation between retinal output and vertical OKR behavior. We demonstrate that motion encoding in vertically tuned oDSGCs is contrast-sensitive and asymmetric for oDSGC types that prefer opposite directions. These phenomena arise from the interplay between spike threshold nonlinearities and differences in synaptic input weights, including shifts in the balance of excitation and inhibition. In behaving mice, these neurophysiological observations, along with a central subtraction of oDSGC outputs, accurately predict the trajectories of vertical OKR across stimulus conditions. Thus, asymmetric tuning across competing sensory channels can critically shape behavior.
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eLife assessment
This work offers fundamental insights into how asymmetric behavioral features in optokinetic eye movements can be predicted from visual responses of direction-selective neurons in the retina. The electrophysiological experiments and model-based analyses are carefully performed and offer convincing conclusions. The presentation could improve in clarity for a stronger focus on the most important results.
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Joint Public Review:
This manuscript by Harris and Dunn investigates the neurophysiology underlying the optokinetic reflex (OKR), by which image motion on the retina triggers a compensatory eye movement. The strength of the OKR varies with direction of motion, and the present study looks for the origins of that asymmetry in neural signals emerging from the retina, specifically the responses of On-direction-selective retinal ganglion cells (oDSGCs). The authors found that compared to oDSGCs in the inferior retina, superior oDSGCs exhibit higher firing rate and broader tuning width under both high and low contrast conditions. Using whole-cell patch clamp recording, imaging and modeling, they found that the enhanced excitation of superior oDSGCs not only accounts for the higher firing rate of these cells but also broadens their spike …
Joint Public Review:
This manuscript by Harris and Dunn investigates the neurophysiology underlying the optokinetic reflex (OKR), by which image motion on the retina triggers a compensatory eye movement. The strength of the OKR varies with direction of motion, and the present study looks for the origins of that asymmetry in neural signals emerging from the retina, specifically the responses of On-direction-selective retinal ganglion cells (oDSGCs). The authors found that compared to oDSGCs in the inferior retina, superior oDSGCs exhibit higher firing rate and broader tuning width under both high and low contrast conditions. Using whole-cell patch clamp recording, imaging and modeling, they found that the enhanced excitation of superior oDSGCs not only accounts for the higher firing rate of these cells but also broadens their spike tuning curves through spike thresholding. To link these retinal signal to behavior, they used the difference in spike rate between superior and inferior oDSGCs to predict vertical optokinetic responses and show matching results.
This is the first study that systematically compares spiking, synaptic and dendritic properties between superior and inferior oDSGCs. The functional differences between two cell types are interesting and significant, and provide a plausible explanation of OKR. This study also raises the important point that E/I balance is often insufficient to account for the spiking behavior. The data presented are of high quality and comprehensive. Suggestions for revision include clarification of technical issues, and consideration of alternative interpretations. Furthermore, the paper could improve from a better focus on the core results.
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