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Joanna D. Crook, Orin S. Packer, Michael B. Manookin, Dennis M. Dacey; Distinct Spatio-chromatic Receptive Field Structure Mediates Red-green Opponency And High Achromatic Contrast Sensitivity In Primate Midget Ganglion Cells. Invest. Ophthalmol. Vis. Sci. 2011;52(14):3905.
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The primate midget pathway has long been thought to serve a dual role in both 'red-green' color processing and peak achromatic spatial acuity. A difficulty with this 'double duty' hypothesis is that midget cells reportedly show poor achromatic contrast sensitivity (eg., Kaplan and Shapley, PNAS, 83:2755, 1986) and primarily signal color (eg., Martin et al., Nature, 410:933, 2001). In our recent study (Crook et al., in press) we found midget ganglion cells responsive to both fine achromatic stimuli restricted to the center and coarse chromatic stimuli that engaged center-surround interaction without recourse to a specialized color-coding circuitry. Our purpose therefore was to determine how both chromatic and achromatic responses arise from the strength of L and M cone inputs to the receptive field and to reexamine the achromatic contrast sensitivity of the midget pathway.
Spikes were recorded in vitro from midget ganglion cells from central retina to near peripheral retina driven by input from 1-5 L and/or M cones to the receptive field center. L and M cone selective drifting gratings were used to measure spatial and contrast sensitivity. Data were fit with a difference-of-Gaussian model and cone input weights to the center vs surround were derived. Contrast gain as a function of chromatic (L vs M), achromatic (L+M), and L or M cone contrast was determined.
Midget cells showed either ‘chromatic-achromatic’ or ‘pure achromatic’ responses. For both groups L and M cones contributed with about equal weight to the surround (n=110). However, in chromatic-achromatic cells L vs M cone opponency arose via center-surround antagonism where either L or M cone input to the center was weak or absent (n=70). The weaker cone input to the center was cancelled by the surround giving rise to a distinctive dip or ‘notch’ in the spatial frequency response associated with a 180 deg reversal in response phase. By contrast, in pure achromatic cells both center and surround received combined L+M inputs of similar strength (n=40). Both cell groups showed band-pass tuning and high contrast sensitivity in response to L+M achromatic stimuli around the peak of the spatial frequency response (contrast gain mean±std=3±2, n=37).
In support of the ‘double-duty’ hypothesis, midget cells show high achromatic contrast sensitivity. The red-green chromatic signal is dependent on the locally variable weighting of L vs M cone inputs to the small receptive field center and on cancellation by the surround of the weaker cone input to the center.
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