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Raunak Sinha, Mrinalini Hoon, Haruhisa Okawa, Rachel Wong, Fred Rieke; Signal processing in the fovea : A specialized mode of synaptic integration by midget ganglion cells. Invest. Ophthalmol. Vis. Sci. 2015;56(7 ):5863.
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© ARVO (1962-2015); The Authors (2016-present)
Our visual perception is dominated by information conveyed from the fovea. A hallmark of the fovea is the specialized midget circuitry in which an individual midget ganglion cell (MGC), collects signal from a single cone photoreceptor resulting in the highest spatial resolution. This is very different in peripheral retina, where a single MGC pools information from 10-30 cones. Despite profound differences in the anatomy and function of the neural circuitry in the fovea and periphery, we know almost nothing about the mechanisms that underlie the signaling properties of cells in the fovea.
We used cell-attached and whole-cell patch clamp recordings to measure light-evoked spike responses and excitatory and inhibitory synaptic currents from MGCs at three retinal eccentricities i.e. foveal, central and peripheral retina. Excitatory and inhibitory postsynaptic receptors were labeled by immunohistochemistry and particle-mediated gene transfer. Dynamic clamp experiments were performed on MGCs to delineate the role of synaptic excitation and inhibition in shaping spike output.
Using whole-cell voltage clamp recordings, we discovered that the responses of MGCs in macaque fovea are not shaped by pre- or postsynaptic inhibition. This is unlike most retinal ganglion cells including peripheral MGCs processing the same stimuli. This physiological finding had an anatomical correlate. Immunolabeling and particle-mediated gene expression displayed a strikingly dense expression of excitatory than inhibitory postsynaptic receptors on foveal MGC dendrites. The ratio of inhibitory to excitatory receptors expressed on foveal MGC dendrites is remarkably less compared to the ratio for peripheral MGCs and foveal wide-field ganglion cells. The light responses of MGCs also exhibted differences in their kinetics between fovea and periphery. Foveal MGCs exhibit sustained responses with slower kinetics compared to peripheral MGCs.
Our findings reveal a distinctive mode of synaptic integration in the foveal midget circuit such that MGC responses are largely dictated by excitatory input, unlike other retinal ganglion cells. This suggests that the retinal circuit, which mediates single cone signaling and high acuity vision, is designed to relay cone signals to higher visual centers with little downstream refinement in the retina.
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