Global Motion Processing by Populations of Direction-Selective Retinal Ganglion Cells

Simple stimuli have been critical to understanding neural population codes in sensory systems. Yet it remains necessary to determine the extent to which this understanding generalizes to more complex conditions. To examine this problem, we measured how populations of direction-selective ganglion cells (DSGCs) from the retinas of male and female mice respond to a global motion stimulus with its direction and speed changing dynamically. We then examined the encoding and decoding of motion direction in both individual and populations of DSGCs. Individual cells integrated global motion over ∼200 ms, and responses were tuned to direction. However, responses were sparse and broadly tuned, which severely limited decoding performance from small DSGC populations. In contrast, larger populations compensated for response sparsity, enabling decoding with high temporal precision (<100 ms). At these timescales, correlated spiking was minimal and had little impact on decoding performance, unlike results obtained using simpler local motion stimuli decoded over longer timescales. We use these data to define different DSGC population decoding regimes that use or mitigate correlated spiking to achieve high-spatial versus high-temporal resolution. SIGNIFICANCE STATEMENT ON-OFF direction-selective ganglion cells (ooDSGCs) in the mammalian retina are typically thought to signal local motion to the brain. However, several recent studies suggest they may signal global motion. Here we analyze the fidelity of encoding and decoding global motion in a natural scene across large populations of ooDSGCs. We show that large populations of DSGCs are capable of signaling rapid changes in global motion