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Shai Sabbah, John Gemmer, Gabriel Castro, Jesse Siegel, Nathan Jeffery, David M Berson; ON-DS retinal ganglion cells encode global motion in vestibular coordinates. Invest. Ophthalmol. Vis. Sci. 2015;56(7 ):5868.
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© ARVO (1962-2015); The Authors (2016-present)
When the head rotates, two reflexes stabilize the retinal image: the vestibulo-ocular reflex fed by the semicircular canals; and optokinetic nystagmus, driven by ON-type direction-selective ganglion cells (ON-DSGCs). There are 3 types of ON-DSGCs, differing in preferred direction and target nucleus within the accessory optic system (AOS). AOS cells encode global retinal slip around three axes that match the ‘best axes’ of the canals. How is their selectivity for rotatory motion assembled from 3 ON-DSGCs types with preferred directions that are widely assumed to be topographically invariant? We hypothesized that each ON-DSGC type topographically varies its preferred direction to match the optic flow resulting from head rotation around the axis of one canal.
We mapped the direction preferences of ON-DSGCs in wildtype mouse retina by 2-photon Ca2+ imaging. Drifting bars and gratings revealed DS preference and sorted ON, ON-OFF or OFF types. ON-DSGCs innervating specific AOS nuclei were identified by retrograde transport. We 3D-reconstructed vestibular and ocular anatomy using micro-computed tomography and modeled retinal optic flow produced by head rotation about each canal axis.
Preferred directions of ON-DSGCs (n = 237) varied retinotopically. DS preferences defined clear clusters, but these changed in orientation over the retina, and were always aligned with slip flow fields produced by rotation around each canal axis. ON-DSGCs projecting to the dorsal medial terminal nucleus (MTNd) preferred retinal slip produced by rotation around the lateral canal axis, while those projecting to the ventral division (MTNv) preferred rotation about the posterior canal axis. Among ON-DSGCs matching a given canal-centric flow field, some preferred slip produced by clockwise rotation, others preferred the reverse.
These data challenge the view that ON-DSGCs comprise three subtypes each with a topographically invariant DS preference. Instead, they demonstrate the existence of three pairs of ON-DSGCs channels, each pair matching its direction preference to the optic flow resulting from sense and antisense rotation around one semicircular canal axis. Simple spatial convergence of outputs of one ON-DSGC type yields a rotatory motion field like those in the AOS. Thus, ON-DSGCs encode slip in a vestibulocentric coordinate system that is easily integrated with canal signals for image stabilization.
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