Visual Stimulation Induces Distinct Forms of Sensitization of On-Off Direction-Selective Ganglion Cell Responses in the Dorsal and Ventral Retina

Experience-dependent modulation of neuronal responses is a key attribute in sensory processing. In the mammalian retina, the On-Off direction-selective ganglion cell (DSGC) is well known for its robust direction selectivity. However, how the On-Off DSGC light responsiveness dynamically adjusts to the changing visual environment is underexplored. Here, we report that On-Off DSGCs tuned to posterior motion direction [i.e. posterior DSGCs (pDSGCs)] in mice of both sexes can be transi-ently sensitized by prior stimuli. Notably, distinct sensitization patterns are found in dorsal and ventral pDSGCs. Although responses of both dorsal and ventral pDSGCs to dark stimuli (Off responses) are sensitized, only dorsal cells show the sensiti-zation of responses to bright stimuli (On responses). Visual stimulation to the dorsal retina potentiates a sustained excitatory input from Off bipolar cells, leading to tonic depolarization of pDSGCs. Such tonic depolarization propagates from the Off to the On dendritic arbor of the pDSGC to sensitize its On response. We also identified a previously overlooked feature of DSGC dendritic architecture that can support dendritic integration between On and Off dendritic layers bypassing the soma. By contrast, ventral pDSGCs lack a sensitized tonic depolarization and thus do not exhibit sensitization of their On responses. Our results highlight a topographic difference in Off bipolar cell inputs underlying divergent sensitization patterns of dorsal and ventral pDSGCs. Moreover, substantial crossovers between dendritic layers of On-Off DSGCs suggest an interactive den-dritic algorithm for processing On and Off signals before they reach the soma.

Automated summary

Experience-dependent modulation of neuronal responses is a key attribute in sensory processing. This study explores the dynamic adjustment of light responsiveness in On-Off direction-selective ganglion cells (DSGCs) of the mammalian retina. The results show that DSGCs can be transiently sensitized by prior stimuli, and this sensitization is found to be different in dorsal and ventral DSGCs. Visual stimulation to the dorsal retina potentiates an excitatory input from Off bipolar cells, leading to a tonic depolarization of dorsal DSGCs and sensitization of their On responses. In addition, the study identifies a previously overlooked feature of DSGC dendritic architecture that supports integration between On and Off dendritic layers.