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Maureen Estevez, Lauren Quattrochi, Onkar Dhande, Inkyu Kim, Timothy Firman, Rana Eldanaf, Andrew Huberman, David Berson; Form and function of the three ON-type direction-selective retinal ganglion cells in the Hoxd10 mouse. Invest. Ophthalmol. Vis. Sci. 2013;54(15):1298.
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© ARVO (1962-2015); The Authors (2016-present)
As the head moves, retinal motion signals drive compensatory eye movements that stabilize the retinal image to optimize visual performance. A critical relay for these motion signals is the accessory optic system (AOS), a group of midbrain nuclei that receive visual inputs from ON-type direction-selective retinal ganglion cells (ON-DSGCs). We discovered a transgenic mouse (Hoxd10-GFP; GENSAT) in which green fluorescent protein (GFP) expression is largely confined to ganglion cells innervating the AOS. Here, we use it to characterize the structure and function of ON-DSGCs that project to AOS targets in this species.
GFP-positive ganglion cells in isolated Hoxd10 retinas were targeted for whole-cell current-clamp recording and dye filling. Tuning for direction, spatial frequency and speed were assessed with computer-generated high-contrast sinusoidal gratings projected through the microscope objective. Stratification of filled cells was analyzed by ChAT (starburst amacrine cell marker) immunostaining and confocal microscopy.
Hoxd10-GFP RGCs included two types. Approximately 50% were ON-DSGCs. These were grouped into three subtypes preferring motion in the visual field either forward, up and slightly back, or down and slightly back. As noted by Simpson, each of these directions matches the optic flow produced by head rotation about the best axis of one of the three semicircular canals. Cells of all three subtypes preferred low spatial frequencies and slow speeds (0.05-0.1 cyc/deg; 1.3-8.4 deg/s, n=9). They had large receptive fields, reflecting their large dendritic fields (288±41μm diameter, n=53), and had weak surround antagonism. Their space-filling dendrites were abundant and highly-branched (75±11 branchpoints, 4755±672 μm total dendritic length, n=53). Most dendrites co-fasciculated with the ON-ChAT plexus, but nearly all cells had a smaller secondary arbor in the OFF ChAT band (0-40% of total dendritic length; mean 13%). We also encountered bistratified cells resembling ON-OFF DSGCs, but their arbor diameter was ~50% smaller than ON-OFF DSGCs, and they lacked direction selectivity.
We introduce the first transgenic reporter mouse marking all three subtypes of ON-DSGCs with high selectivity. Our data suggest that the AOS nuclei stabilize images based on inputs received from canonical ON-DSGCs, echoing the classic descriptions of this system in the rabbit.
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