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Joanna Diane Crook, John B. Troy, Orin S. Packer, Julian D. Vrieslande, Dennis M. Dacey; Contribution of excitatory and inhibitory conductances to receptive field structure in midget and parasol ganglion cells of macaque monkey retina. Journal of Vision 2009;9(14):57. doi: https://doi.org/10.1167/9.14.57.
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The two classically recognized populations of primate retinal ganglion cells that project to the lateral geniculate nucleus (LGN), the midget and parasol cells, show center-surround receptive field organization (Wiesel and Hubel, 1966; Croner and Kaplan, 1995). Direct excitatory ON or OFF synaptic input from bipolar cells provides an obvious mechanism for generating the receptive field center. However, recent studies in non-primate mammalian retina suggest that vertical inhibition from ON to OFF pathways can also significantly contribute, in a push-pull manner, to the center response (e.g., Manookin et al., 2008). The origin of the inhibitory surround is controversial because of the difficulty of sorting out the contribution from horizontal cell feedback to cone photoreceptors in the outer retina and from amacrine cell lateral inhibition in the inner retina. In this study, we made whole cell voltage-clamp recordings from identified midget and parasol ganglion cells in the in vitro macaque retina and characterized excitatory and inhibitory conductances associated with center and surround receptive field components. Light-evoked synaptic currents were measured at a series of holding potentials (−100 to +40 mV) while stimulating center and surround with spots and annuli. For all cells excitatory conductances were isolated for modulation of both center and surround consistent with the relay of center-surround receptive field structure from midget and diffuse bipolar cells. However feedforward inhibition was also present for all stimuli. In addition for OFF parasol cells a significant cross-pathway inhibitory input, abolished by ON-pathway blockade with the MGluR6 receptor agonist L-AP4, was clearly observed. To determine receptive field structure of the direct excitatory and inhibitory synaptic inputs cells were voltage clamped near the cation (inhibition isolated) or chloride (excitation isolated) reversal potentials and drifting gratings were used to measure spatial frequency tuning. Both excitatory and inhibitory fields showed band-pass tuning well fit by a difference-of-Gaussian receptive field model. Unexpectedly the inhibitory receptive field center was typically narrower than that of the excitatory center suggesting significant feedforward inhibition from small-field, presumably glycinergic amacrine cells. After blocking all inhibitory conductances with antagonists of GABAergic and glycinergic transmission the isolated excitatory conductance retained clear center-surround organization also consistent with non-GABAergic horizontal cell feedback as a primary source for the classic receptive field surround. In addition, block of inhibition revealed a clear excitatory, cross-pathway OFF input to ON parasol ganglion cells as previously observed (Crook et al., 2008). YIA
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