NMDA Receptor Contributions to Visual Contrast Coding

Manookin, Michael B.; Weick, Michael; Stafford, Benjamin K.; Demb, Jonathan B.

doi:10.1016/j.neuron.2010.06.020

Cited by 49 publications

(96 citation statements)

References 76 publications

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“…The apparent K Mg is approximately twofold higher than GluN2A-or GluN2B-containing NMDA receptors and may be consistent with an alternative subunit composition, having a lower Mg 2ϩ sensitivity (Monyer et al 1994). Lower Mg 2ϩ sensitivity for NMDA receptors has been reported for other RGC types (Manookin et al 2010;Venkataramani and Taylor 2010). To take into account the Mg 2ϩ block and better compare the excitatory effects of the NMDA and AMPA conductances near resting potential, the NMDA conductance in all figures has been scaled to show the chord conductance at Ϫ70 mV; i.e., G NMDA(Ϫ70) …”

Section: Methodssupporting

confidence: 70%

“…The density and receptive field size indicate that OFF-BSGCs represent the visual input at a high spatial resolution. Previous studies examining the physiological roles of ON pathway crossover inhibition and NMDA receptor-mediated transmission have targeted wide-field RGCs, which represent low spatial-resolution pathways (Manookin et al 2008(Manookin et al , 2010van Wyk et al 2009;Venkataramani and Taylor 2010). Here, we explore the possible role of these inputs for visual processing in a high spatial-resolution pathway.…”

Section: Resultsmentioning

confidence: 97%

“…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.…”

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confidence: 99%

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

Buldyrev

Puthussery

Taylor

2012

Journal of Neurophysiology

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Different types of retinal ganglion cells represent distinct spatiotemporal filters that respond selectively to specific features in the visual input. Much about the circuitry and synaptic mechanisms that underlie such specificity remains to be determined. This study examines how N-methyl-d-aspartate (NMDA) receptor signaling combines with other excitatory and inhibitory mechanisms to shape the output of small-field OFF brisk-sustained ganglion cells (OFF-BSGCs) in the rabbit retina. We used voltage clamp to separately resolve NMDA, α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA), and inhibitory inputs elicited by stimulation of the receptive field center. Three converging circuits were identified. First is a direct glutamatergic input, arising from OFF cone bipolar cells (CBCs), which is mediated by synaptic NMDA and AMPA receptors. The NMDA input was saturated at 10% contrast, whereas the AMPA input increased monotonically up to 60% contrast. We propose that NMDA inputs selectively enhance sensitivity to low contrasts. The OFF bipolar cells, mediating this direct excitatory input, express dendritic kainate (KA) receptors, which are resistant to the nonselective AMPA/KA receptor antagonist, 2,3-dioxo-6-nitro-1,2,3,4-tetrahydrobenzo[f]quinoxaline-7-sulfonamide disodium salt (NBQX), but are suppressed by a GluK1- and GluK3-selective antagonist, (S)-1-(2-amino-2-carboxyethyl)-3-(2-carboxy-thiophene-3-yl-methyl)-5-methylpyrimidine-2,4-dione (UBP-310). The second circuit entails glycinergic crossover inhibition, arising from ON-CBCs and mediated by AII amacrine cells, which modulate glutamate release from the OFF-CBC terminals. The third circuit also comprises glycinergic crossover inhibition, which is driven by the ON pathway; however, this inhibition impinges directly on the OFF-BSGCs and is mediated by an unknown glycinergic amacrine cell that expresses AMPA but not KA receptors.

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Section: Methodssupporting

confidence: 70%

Section: Resultsmentioning

confidence: 97%

mentioning

confidence: 99%

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

Buldyrev

Puthussery

Taylor

2012

Journal of Neurophysiology

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“…Plotting the average peak amplitude of events measured in five cells (one ON, three OFF, and one ON-OFF) against the holding potential revealed a nonlinear relationship characteristic of events mediated by a combination of AMPA/KA and NMDA receptors (Fig. 2C) (Diamond and Copenhagen, 1993;Sagdullaev et al, 2006;Manookin et al, 2010). Indeed, these events were largely suppressed by NBQX and AP-5 (89 Ϯ 6% block; n ϭ 3), which are selective antagonists for AMPA/ kainate (KA) and NMDA receptors, respectively.…”

Section: Blocking Inhibitory Receptors Augments Sepscs In Rd1 Gangliomentioning

confidence: 99%

“…L-AP-4 might also act on axonal terminals of bipolar cells (Awatramani and Slaughter, 2001) and amacrine cells (Quraishi et al, 2007); therefore, these data need to be interpreted with caution. To monitor activity in ganglion cells in the presence of NBQX, in these experiments, we took advantage of the selective expression of synaptic NMDA receptors in these cells (Diamond and Copenhagen, 1993;Sagdullaev et al, 2006;Manookin et al, 2010) and monitored output of bipolar cells as NMDA-receptor-mediated sEPSCs at a holding potential of ϩ40 mV (in which these receptors would be relieved of their Mg 2ϩ block) (Jahr and Stevens, 1990). Using this method, the intrinsic activity of the cone bipolar/AII amacrine cell network was assessed in relative isolation.…”

Section: Spontaneous Synaptic Output From Cone Bipolar Cells Measuredmentioning

confidence: 99%

An Intrinsic Neural Oscillator in the Degenerating Mouse Retina

Borowska¹,

Trenholm²,

Awatramani³

2011

J. Neurosci.

107

171

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The loss of photoreceptors during retinal degeneration (RD) is known to lead to an increase in basal activity in remnant neural networks. To identify the source of activity, we combined two-photon imaging with patch-clamp techniques to examine the physiological properties of morphologically identified retinal neurons in a mouse model of RD (rd1). Analysis of activity in rd1 ganglion cells revealed sustained oscillatory (ϳ10 Hz) synaptic activity in ϳ30% of all classes of cells. Oscillatory activity persisted after putative inputs from residual photoreceptor, rod bipolar cell, and inhibitory amacrine cell synapses were pharmacologically blocked, suggesting that presynaptic cone bipolar cells were intrinsically active. Examination of presynaptic rd1 ON and OFF bipolar cells indicated that they rested at relatively negative potentials (less than Ϫ50 mV). However, in approximately half the cone bipolar cells, low-amplitude membrane oscillation (ϳ5 mV, ϳ10 Hz) were apparent. Such oscillations were also observed in AII amacrine cells. Oscillations in ON cone bipolar and AII amacrine cells exhibited a weak apparent voltage dependence and were resistant to blockade of synaptic receptors, suggesting that, as in wild-type retina, they form an electrically coupled network. In addition, oscillations were insensitive to blockers of voltage-gated Ca 2ϩ channels (0.5 mM Cd 2ϩ and 0.5 mM Ni 2ϩ ), ruling out known mechanisms that underlie oscillatory behavior in bipolar cells. Together, these results indicate that an electrically coupled network of ON cone bipolar/AII amacrine cells constitutes an intrinsic oscillator in the rd1 retina that is likely to drive synaptic activity in downstream circuits.

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A general principle governs vision‐dependent dendritic patterning of retinal ganglion cells

Sun

Tian

2014

J of Comparative Neurology

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Dendritic arbors of retinal ganglion cells (RGCs) collect information over a certain area of the visual scene. The coverage territory and the arbor density of dendrites determine what fraction of visual field is sampled by a single cell and at what resolution. Yet it is not clear whether visual stimulation is required for the establishment of branching patterns of RGCs, and is there a general principle directs the dendritic patterning of diverse RGCs. By analyzing the geometric structures of RGC dendrites, we found that dendritic arbors of RGCs underwent a substantial spatial rearrangement after eye-opening. Light deprivation blocked both the dendritic growth and the branch patterning, suggesting that visual stimulation is required for the acquisition of specific branching patterns of RGCs. We further showed that vision dependent dendritic growth and arbor refinement were occurred mainly in the middle portion of the dendritic tree. This non-proportional growth and selective refinement suggested that the late-stage dendritic development of RGCs is not a passive stretching with the growth of eyes, but an active process of selective growth/elimination of dendritic arbors of RGCs driven by visual activity. Finally, our data showed that there was a power law relationship between the coverage territory and dendritic arbor density of RGCs on a cell by cell basis. RGCs are systematically less dense when they cover larger territories regardless of their cell types, retinal locations and developmental stages. These results suggest that there is a general structural design principle directs the vision dependent patterning of RGC dendrites.

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NMDA Receptor Contributions to Visual Contrast Coding

Cited by 49 publications

References 76 publications

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

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

An Intrinsic Neural Oscillator in the Degenerating Mouse Retina

A general principle governs vision‐dependent dendritic patterning of retinal ganglion cells

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