Circuitry and receptive field structure underlying ‘double duty’ performance by midget ganglion cells

Abstract

The potential for midget cells to do ‘double duty’ and encode chromatic and achromatic responses has long been recognized (DeValois, 1975, Wiesel and Hubel, 1966, Lennie et al., 1991) but not supported due to two outstanding problems. The midget cells achromatic sensitivity is poor (Derrington and Lennie, 1984, Kaplan and Shapley, 1986) and the number of ‘red-green’ chromatic cells outside the fovea is greater than expected suggesting the development of specialized circuitry for color coding (Lee, 2004). Here we record from central midget ganglion cells in the choroid-RPE attached in-vitro macaque retina and reexamine these issues. We characterized the midget cell receptive field with cone-specific stimuli. All midget cells displayed clear center-surround receptive field structure. Either one or both cone types contributed to the center; both cone types always contributed to the surround (n=60). Achromatic responses were elicited to stimuli restricted to the center while chromatic responses were highly dependent on broad stimuli that engaged center and surround. Varying the contrast of stimuli constrained to the receptive field center revealed high achromatic contrast sensitivity with gains greater than 2 (n=30). To test for cone-specific inhibitory circuits we blocked glycinergic and GABAergic inhibition and found that chromatic responses persisted unperturbed (n=48). In contrast, blocking ‘randomly wired’ horizontal cell feedback (Dacey et al., 1996), by increasing the retinas buffering capacity (Davenport, 2008), abolished opponent responses (n=14). Thus we find that the midget cells classic center and surround receptive field structure permits relay of both chromatic and achromatic signals with high contrast sensitivity and without recourse to specialized inhibitory circuits.