Visual stimulation induces distinct forms of sensitization of On-Off direction-selective ganglion cell responses in the dorsal and ventral retina

Abstract

Experience-dependent modulation of neuronal responses is a key attribute in sensory processing. In the mammalian retina, the On-Off direction-selective ganglion cell (On-Off 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 the On-Off DSGC can be transiently sensitized by prior stimuli. Notably, distinct sensitization patterns are found in dorsal and ventral DSGCs that receive visual inputs from lower and upper visual fields respectively. Although responses of both dorsal and ventral DSGCs to dark stimuli (Off responses) are sensitized, only dorsal cells show sensitization 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 dorsal DSGCs. Such tonic depolarization propagates from the Off to the On dendritic arbor of the DSGC to sensitize its On response. We also identified a previously overlooked feature of DSGC dendritic architecture that can support direct electrotonic propagation between On and Off dendritic layers. By contrast, ventral DSGCs 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 On-Off DSGCs. Moreover, substantial crossovers between dendritic layers of On-Off DSGCs suggest an interactive dendritic algorithm for processing On and Off signals before they reach the soma.

Temporal pattern recognition in retinal ganglion cells is mediated by dynamical inhibitory synapses

“…Previous works have shown that inhibitory synapses can be depressing [16, 15, 23]. In particular, glycinergic synapses that input to bipolar cells can be depressing [14]. However, there is no method to experimentally remove the depressing nature of the synapse without affecting the inhibitory weight, so we could not show experimentally that the depressing nature of the synapse is necessary to the OSR.…”

“…Several previous reports have shown that inhibitory synapses can be depressing, i.e. have a decreasing weight depending on previous inputs [18, 36, 23, 17, 14]. It has been hypothesized that the variation in synaptic strength results from varying availability of vesicles in the readily releasable vesicle pool, which gets gradually depleted upon persistent inputs [31, 5, 25].…”