Direction selective (DS) ganglion cells (GC) in the retina maintain their tuning across a broad range of light levels. Yet very different circuits can shape their responses from bright to dim light, and their respective contributions are difficult to tease apart. In particular, the contribution of the rod bipolar cell (RBC) primary pathway, a key player in dim light, is unclear. To understand its contribution to DSGC response, we designed an all-optical approach allowing precise manipulation of single retinal neurons. Our system activates single cells in the bipolar cell (BC) layer by two-photon (2P) temporally focused holographic illumination, while recording the activity in the ganglion cell layer by 2P Ca 2 imaging. By doing so, we demonstrate that RBCs provide an asymmetric input to DSGCs, suggesting they contribute to their direction selectivity. Our results suggest that every circuit providing an input to direction selective cells can generate direction selectivity by itself. This hints at a general principle to achieve robust selectivity in sensory areas.A major goal in neuroscience is to understand the circuits that embody the computations performed by sensory neurons. In particular, a striking feature of sensory processing is the ability of neurons to perform the same computation in different contexts. For example, neurons in the piriform cortex represent odor identity while remaining invariant to its exact concentration (Bolding and Franks, 2018). Similarly, neurons in the visual cortex can keep the same orientation tuning curve over different contrasts (Sclar and Freeman, 1982).In the retina, direction selective (DS) ganglion cells (GC) respond selectively to a motion direction in different contexts such as different backgrounds (Chen et al., 2016), different natural scenes (Im and Fried, 2016), and over a broad range of luminosities (Pearson and Kerschensteiner, 2015; Vaney et al., 2001;Yao et al., 2018). Switching the average luminance from dim to bright light will change the dominant circuits that convey visual information inside the retina, leading to major changes in the responses of ganglion cells (Pearson and Kerschensteiner, 2015;Wässle, 2004). For example, cells will change their ON-OFF polarity (Tikidji-Hamburyan et al., 2015). It is therefore particularly striking that direction selectivity remains constant across the ten billion fold change of luminance separating day from night (Yao et al., 2018), despite the involvement of distinct circuits. A major challenge is to understand how this feature is achieved.During daylight conditions, where rods are saturated and cones transmit light input, the major component responsible for direction selectivity is a functional asymmetry. This results either from an asymmetric inhibition or an asymmetric morphology. For example, in the ON-OFF
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