Asymmetric retinal direction tuning predicts optokinetic eye movements across stimulus conditions

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. Specifically, 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 direction and magnitude of vertical OKR across stimulus conditions. Thus, asymmetric synaptic input across competing sensory input channels can critically shape behavior.

Contrast Sensitivity of ON and OFF Human Retinal Pathways in Myopia

“…Light and dark visual stimuli are encoded by ON and OFF visual pathways that differ in their response modulations to luminance, contrast, and the spatiotemporal properties of the stimulus ( Chichilnisky and Kalmar, 2002 ; Zaghloul et al, 2003 ; Jin et al, 2008 , 2011 ; Komban et al, 2014 ; Kremkow et al, 2014 ; Rekauzke et al, 2016 ; Ravi et al, 2018 ; Rahimi-Nasrabadi et al, 2021 ; Williams et al, 2021 ; Harris and Dunn, 2023 ). In the primary visual cortex of cats and humans, ON pathways have higher contrast sensitivity and more pronounced contrast response saturation than OFF pathways, and the difference increases with luminance range ( Kremkow et al, 2014 ; Pons et al, 2017 ; Rahimi-Nasrabadi et al, 2021 ).…”