The role of NMDA channels in rabbit retinal directional selectivity

Abstract

It has been previously demonstrated that the majority of the glutamatergic input to directionally selective (DS) ganglion cells in the rabbit retina is mediated by NMDA receptors. To examine whether NMDA channels have any role in directional selectivity, we eliminated magnesium from the superfusion medium to prevent the magnesium block of the channels at hyperpolarized membrane potentials. During superfusion in magnesium-free media, the response to null-direction motion increased to the level of the response to preferred-direction motion. This effect was specifically mediated by NMDA channels because subsequent blocking of the NMDA channels with AP7 restored directional selectivity. We also tested whether the increase in the null-direction response in magnesium-free medium was due to an increased release of acetylcholine from the cholinergic amacrine cells, rather than an effect on the DS ganglion cells themselves, by blocking acetylcholine transmission with d-tubocurarine during superfusion with the magnesium-free medium. During zero-magnesium superfusion, d-tubocurarine reduced both the preferred- and null-direction responses of DS ganglion cells but did not restore directional selectivity. These findings suggest that null-direction motion normally causes portions of the dendritic membrane of the directionally selective ganglion cell to be maintained at a sufficiently negative potential that the NMDA channels are blocked by magnesium ions. This result is discussed in terms of several models for the mechanisms of directional selectivity.

Localization of neuropeptide Y1 receptor immunoreactivity in the rat retina and the synaptic connectivity of Y1 immunoreactive cells

“…Alternatively, Y1 may not be coupled to inhibitory G-proteins in these cells. Cholinergic amacrine cells have been implicated in directional selectivity; however, their exact role is not fully understood (Kittila and Massey, 1997;He and Masland, 1997;Grzywacz et al, 1998;Tjepkes and Amthor, 2000;Yoshida et al, 2001). Our present findings suggest NPY acting by means of Y1 receptors could also have an influence on the response properties of these cells, perhaps to produce long-lasting changes in the cholinergic plexus.…”

NMDA Receptors Multiplicatively Scale Visual Signals and Enhance Directional Motion Discrimination in Retinal Ganglion Cells

“…Synaptic inputs to DSGCs comprise GABAergic inhibition and cholinergic excitation from SACs (Briggman et al, 2011; Lee et al, 2010; Wei et al, 2010; Yonehara et al, 2010) and glutamatergic input, predominantly from bipolar cells (Lee et al, 2014), that is received postsynaptically by AMPA receptors (AMPARs) and NMDARs (Lee et al, 2010; Stafford et al, 2014; Tjepkes and Amthor, 2000; Weng et al, 2005). Direction selectivity (DS) computation originates in starburst amacrine cell (SAC) dendrites, which respond preferably to stimuli moving from the cell body towards the dendritic tips (Euler et al, 2002).…”

Synaptic pathways that shape the excitatory drive in an OFF retinal ganglion cell

“…Unlike LEDs, in which ␣-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid/kainate (AMPA/KA) receptor currents are primary drivers of excitation, at least in rabbit (van Wyk et al 2006), cat homologues of BSGCs receive a significant N-methyl-D-aspartate (NMDA) receptor-mediated synaptic input (Cohen 1998(Cohen , 2000. NMDA receptors have been detected in many types of vertebrate ganglion cell Miller 1994, 1999;Diamond and Copenhagen 1993;Kittila and Massey 1997;Manookin et al 2010;Massey and Miller 1990;Matsui et al 1998;Mittman et al 1990;Tjepkes and Amthor 2000), and recent studies have begun to elucidate the role of these inputs in retinal processing (Manookin et al 2010;Venkataramani and Taylor 2010). One of our goals was to establish that rabbit OFF-BSGCs also receive a significant NMDA receptor-mediated input and to investigate its functional significance.…”