Gap Junctions Contribute to Differential Light Adaptation across Direction-Selective Retinal Ganglion Cells

Abstract

Direction-selective ganglion cells (DSGCs) deliver signals from the retina to multiple brain areas to indicate the presence and direction of motion. Delivering reliable signals in response to motion is critical across light levels. Here we determine how populations of DSGCs adapt to changes in light level, from moonlight to daylight. Using large-scale measurements of neural activity, we demonstrate that the population of DSGCs switches encoding strategies across light levels. Specifically, the direction tuning of superior (upward)-preferring ON-OFF DSGCs becomes broader at low light levels, whereas other DSGCs exhibit stable tuning. Using a conditional knockout of gap junctions, we show that this differential adaptation among superior-preferring ON-OFF DSGCs is caused by connexin36-mediated electrical coupling and differences in effective GABAergic inhibition. Furthermore, this adaptation strategy is beneficial for balancing motion detection and direction estimation at the lower signal-to-noise ratio encountered at night. These results provide insights into how light adaptation impacts motion encoding in the retina.

Global motion processing by populations of direction-selective retinal ganglion cells

“…Visually driven responses of retinal ganglion cells (RGCs) were measured ex vivo using a multi-electrode array (MEA) 11,25 . Responses to drifting gratings distinguished ooDSGCs and oDSGCs from other RGCs over the MEA (see Methods).…”

“…Retina dissection was optimized to maintain response sensitivity. Mice were dark-adapted overnight, euthanized via decapitation, eyes were enucleated, and a piece of retina (~1-2mm 2 ) was isolated from the pigmented epithelium 11 . Retina isolation was performed in Ames solution (room temperature) bubbled with 95% O2 and 5% CO2.…”

“…Electrical activity was measured from RGCs on a multielectrode array (MEA). Spikes were identified, sorted into individual cell clusters, and soma positions on the MEA were estimated as previously described 11,63 . Electrical activity was measured from RGCs using a hexagonal largescale MEA, which was ~490 µm along an edge with 30 µm spacing between 519 electrodes 63,64 .…”

“…In the mammalian retina, there are four types of ooDSGCs, each tiling space with their dendritic and receptive fields [5][6][7][8][9] . These types differ primarily in their preferred direction of motion, which are organized along four cardinal axes [10][11][12][13][14] . Direction is encoded across the four types by their relative firing rates.…”

“…To study DSGC responses, we recorded simultaneously the spiking activity from hundreds of retinal ganglion cells (RGCs) using a large-scale multielectrode array (MEA). We distinguished DSGCs from other RGCs based on their responses to drifting gratings 11,25 . We then projected dynamically moving natural images onto the retina.…”