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Orin S Packer, Richard Schalek, Rachel O Wong, Christine Curcio, John E Dowling, Jeff Lichtman, Dennis M Dacey; Restricted cone connections of horizontal cells in the human foveal center. Invest. Ophthalmol. Vis. Sci. 2017;58(8):1035. doi: https://doi.org/.
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© ARVO (1962-2015); The Authors (2016-present)
The exquisite spatial resolution afforded by the foveal cone mosaic is preserved by a unique, non-divergent excitatory circuit: a midget bipolar cell receives synaptic input from a single long- (L) or middle-wavelength (M) sensitive cone and in turn makes synaptic output to a single midget ganglion cell. This ‘private-line’ circuit also shows L vs M cone (‘red-green’) color opponency that arises from receptive field surround antagonism. The surround arises by horizontal cell negative feedback to L and M cones (Crook et al., J.Neurosci. 2011). Horizontal cells in the retinal periphery make indiscriminant, divergent connections to large numbers of L and M cones. However little is known about the connectivity of foveal horizontal cells that could contribute to the L or M cone specificity critical for color opponency. Our purpose therefore was to use volume electron microscopy to reconstruct the horizontal cell circuit for cones in the center of the human fovea.
Eyes were acquired from a single 21 yr old male donor at the time of death. After corneal removal the eyecup was immersed in oxygenated Ames medium and fixed in 4% glutaraldehyde. The macular region was dissected, epoxy-embedded and serially sectioned at 65 nm in the horizontal plane using the Automated Tape Ultramicrotome (ATUM) method. A 250 x 250 µm region centered on the fovea was imaged at 6 nm resolution and sections that encompassed the cone pedicles, outer plexiform and inner nuclear layers were used for reconstruction.
All of the horizontal cell invaginating contacts at a single pedicle linked to a cone at the foveal center (Dacey et al., ARVO 2017) were reconstructed. 53 contacts at 26 ribbon synapses were traced to 11 distinct horizontal cells. However the majority of contacts to this single pedicle arose from just 3 horizontal cells (32 contacts; 60%). The cone connectivity of single horizontal cells showed the complementary pattern: individual cells made ~20-30 contacts with 7-8 neighboring cones but the majority of contacts (~60%) were directed to just 1-2 pedicles.
By contrast with the retinal periphery human foveal horizontal cells are greatly reduced in size and contact 1-2 cones preferentially. We hypothesize that the restricted cone connectivity of foveal horizontal cells contributes to a similarly restricted ‘midget surround’ and in turn to L vs M cone opponency in the midget receptive field.
This is an abstract that was submitted for the 2017 ARVO Annual Meeting, held in Baltimore, MD, May 7-11, 2017.
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