Desensitizing glutamate receptors shape excitatory synaptic inputs to tiger salamander retinal ganglion cells

Lukasiewicz, Peter D., James A. Wilson, and Jean E. Lawrence. AMPA-preferring receptors mediate excitatory synaptic inputs to retinal ganglion cells. J. Neurophysiol. 77: 57–64, 1997. Pharmacological studies were performed to determine whether α-amino-3-hydroxy-5-methyl-4-isoazoleprionic acid (AMPA)- and/or kainate (KA)-preferring receptors mediate excitatory synaptic inputs to tiger salamander retinal ganglion cells. Excitatory postsynaptic currents (EPSCs), evoked either by light or by stimulating bipolar cells with puffs of K+, were measured using whole cell recording techniques in the tiger salamander retinal slice. The AMPA/KA component of the EPSCs was isolated by including antagonists of glycine-, γ-aminobutyric acid (GABA)- and NMDA-receptors in the bath. The AMPA-preferring receptor antagonists, 1-(4-aminophenyl)-4-methyl-7,8-methylenedioxy-5H-2,3-benzodiazepine hydrochloride (GYKI-52466) and 1-(4-aminophenyl)-3-methylcarbamyl - 4 - methyl - 7,8 - methylenedioxy - 3,4 - dihydro - 5H - 2,3 - benzodiazepine (GYKI-53665), reduced light-evoked EPSCs and K+ puff-evoked EPSCs amplitudes in a concentration-dependent manner. The IC50 values for GYKI-52466 were 3.6 and 4.2 μM for the light- and puff-evoked responses, respectively. The more potent GYKI-53665 had IC50 values of 0.7 μM for both the light- and puff evoked responses. KA activates both KA- and AMPA-preferring receptors. KA-evoked currents were completely blocked by 10–40 μM GYKI-53665, indicating that little or no excitatory synaptic current was mediated by KA-preferring receptors. Concanavalin A, a compound that preferentially potentiates responses mediated by KA-preferring receptors, did not enhance either EPSCs or glutamate-evoked responses. By contrast, cyclothiazide, which selectively enhances AMPA-preferring receptor mediated responses, was found to enhance both EPSCs and glutamate-evoked currents. Our results indicate that the non-NMDA component of ganglion cell EPSCs is mediated by AMPA-preferring receptors and not significantly by KA-preferring receptors.

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Membrane Properties and Monosynaptic Retinal Excitation of Neurons in the Turtle Accessory Optic System

Journal of Neurophysiology ◽

10.1152/jn.1997.78.2.614 ◽

1997 ◽

Vol 78 (2) ◽

pp. 614-627 ◽

Cited By ~ 10

Author(s):

Naoki Kogo ◽

Michael Ariel

Keyword(s):

Receptive Field ◽

Retinal Ganglion Cells ◽

Ganglion Cells ◽

Membrane Properties ◽

Retinal Ganglion ◽

Optic System ◽

Accessory Optic System ◽

Postsynaptic Potentials ◽

Synaptic Inputs ◽

Bon Cells

Kogo, Naoki and Michael Ariel. Membrane properties and monosynaptic retinal excitation of neurons in the turtle accessory optic system. J. Neurophysiol. 78: 614–627, 1997. Using an eye-attached isolated brain stem preparation of a turtle, Pseudemys scripta elegans, in conjunction with whole cell patch techniques, we recorded intracellular activity of accessory optic system neurons in the basal optic nucleus (BON). This technique offered long-lasting stable recordings of individual synaptic events. In the reduced preparation (most of the dorsal structures were removed), large spontaneous excitatory synaptic inputs [excitatory postsynaptic potentials (EPSPs)] were frequently recorded. Spontaneous inhibitory postsynaptic potentials were rarely observed except in few cases. Most EPSPs disappeared after injection of lidocaine into the retina. A few EPSPs of small size remained, suggesting that these EPSPs either were from intracranial sources or may have been miniature spontaneous synaptic potentials from retinal ganglion cell axon terminals. Population EPSPs were synchronously evoked by electrical stimulation of the contralateral optic nerve. Their constant onset latency and their ability to follow short-interval paired stimulation indicated that much of the population EPSP's response was monosynaptic. Visually evoked BON spikes and EPSP inputs to BON showed direction sensitivity when a moving pattern was projected onto the entire contralateral retina. With the use of smaller moving patterns, the receptive field of an individual BON cell was identified. A small spot of light, projected within the receptive field, guided the placement of a bipolar stimulation electrode to activate retinal ganglion cells that provided input to that BON cell. EPSPs evoked by this retinal microstimulation showed features of unitary EPSPs. Those EPSPs had distinct low current thresholds. Recruitment of other inputs was only evident when the stimulation level was increased substantially above threshold. The average size of evoked unitary EPSPs was 7.8 mV, confirming the large size of synaptic inputs of this system relative to nonsynaptic noise. EPSP shape was plotted (rise time vs. amplitude), with the use of either evoked unitary EPSPs or spontaneous EPSPs. Unlike samples of spontaneous EPSPs, data from many unitary EPSPs formed distinct clusters in these scatterplots, indicating that these EPSPs had a unique shape among the whole population of EPSPs. In most BON cells studied, hyperpolarization-activated channels caused a slow depolarization sag that reached a plateau within 0.5–1 s. This property suggests that BON cells may be more complicated than a simple site for convergence of direction-sensitive retinal ganglion cells to form a central retinal slip signal for control of oculomotor reflexes.

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Tailoring of the axon initial segment shapes the conversion of synaptic inputs into spiking output in OFF-α T retinal ganglion cells

Science Advances ◽

10.1126/sciadv.abb6642 ◽

2020 ◽

Vol 6 (37) ◽

pp. eabb6642

Author(s):

Paul Werginz ◽

Vineeth Raghuram ◽

Shelley I. Fried

Keyword(s):

Retinal Ganglion Cells ◽

Initial Segment ◽

Ganglion Cells ◽

Axon Initial Segment ◽

Retinal Ganglion ◽

Light Responses ◽

Synaptic Inputs ◽

Dorsal Cells ◽

Axon Initial Segments ◽

Dorsal Retina

Recently, mouse OFF-α transient (OFF-α T) retinal ganglion cells (RGCs) were shown to display a gradient of light responses as a function of position along the dorsal-ventral axis; response differences were correlated to differences in the level of excitatory presynaptic input. Here, we show that postsynaptic differences between cells also make a strong contribution to response differences. Cells in the dorsal retina had longer axon initial segments (AISs)—the greater number of Nav1.6 channels in longer AISs directly mediates higher rates of spiking and helps avoid depolarization block that terminates spiking in ventral cells with shorter AISs. The pre- and postsynaptic specializations that shape the output of OFF-α T RGCs interact in different ways: In dorsal cells, strong inputs and the long AISs are both necessary to generate their strong, sustained spiking outputs, while in ventral cells, weak inputs or the short AISs are both sufficient to limit the spiking signal.

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Enhancement of low-voltage-activated calcium currents by group II metabotropic glutamate receptors in rat retinal ganglion cells

Molecular and Cellular Neuroscience ◽

10.1016/s1044-7431(03)00056-3 ◽

2003 ◽

Vol 23 (3) ◽

pp. 341-350 ◽

Cited By ~ 11

Author(s):

Jon Robbins ◽

A.Martyn Reynolds ◽

Sarah Treseder ◽

Richard Davies

Keyword(s):

Glutamate Receptors ◽

Retinal Ganglion Cells ◽

Metabotropic Glutamate Receptors ◽

Low Voltage ◽

Ganglion Cells ◽

Calcium Currents ◽

Retinal Ganglion ◽

Metabotropic Glutamate ◽

Group Ii

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An offset ON-OFF receptive field is created by gap junctions between distinct types of retinal ganglion cells

10.1101/2020.07.15.205336 ◽

2020 ◽

Author(s):

Sam Cooler ◽

Gregory W. Schwartz

Keyword(s):

Retinal Ganglion Cells ◽

Ganglion Cells ◽

Cell Model ◽

Receptive Fields ◽

Visual Space ◽

Retinal Ganglion ◽

Precise Location ◽

Synaptic Inputs ◽

Retinotopic Maps ◽

Edge Location

SummaryReceptive fields (RFs) are a foundational concept in sensory neuroscience. The RF of a sensory neuron is shaped by the properties of its synaptic inputs from connected neurons. In the early visual system, retinotopic maps define a strict relationship between the location of a cell’s dendrites and its RF location in visual space1–3. Retinal ganglion cells (RGCs), the output cells of the retina, form dendritic mosaics that tile retinal space and have corresponding RF mosaics that tile visual space1,2. The precise location of dendrites in some RGCs has been shown to predict their RF shape4. Previously described ON-OFF RGCs have aligned dendrites in ON and OFF synaptic layers, so the cells respond to increments and decrements of light at the same locations in visual space5–8. Here we report a systematic offset between the ON and OFF RFs of an RGC type. Surprisingly, this property does not come from offset ON and OFF dendrites but instead arises from electrical synapses with RGCs of a different type. This circuit represents a new channel for direct communication between ON and OFF RGCs. Using a multi-cell model, we find that offset ON-OFF RFs could improve the precision with which edge location is represented in an RGC population.

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Slow Excitation of Cultured Rat Retinal Ganglion Cells by Activating Group I Metabotropic Glutamate Receptors

Journal of Neurophysiology ◽

10.1152/jn.00650.2009 ◽

2009 ◽

Vol 102 (6) ◽

pp. 3728-3739 ◽

Cited By ~ 14

Author(s):

Jianing Yu ◽

Bryan A. Daniels ◽

William H. Baldridge

Keyword(s):

Glutamate Receptors ◽

Retinal Ganglion Cells ◽

Metabotropic Glutamate Receptors ◽

Ganglion Cells ◽

Membrane Resistance ◽

Resting Membrane Potential ◽

Receptor Subtype ◽

Retinal Ganglion ◽

Metabotropic Glutamate ◽

Group I

As in many CNS neurons, retinal ganglion cells (RGCs) receive fast synaptic activation through postsynaptic ionotropic receptors. However, the potential role of postsynaptic group I metabotropic glutamate receptors (mGluRs) in these neurons is unknown. In this study we first demonstrated that the selective group I mGluR agonist ( S)-3,5-dihydroxyphenylglycine (DHPG) increased intracellular calcium concentration in neurons within the ganglion cell layer of the rat retina. This prompted us to use an immunopanned-RGC and cortical astroglia coculture preparation to explore the effect of group I mGluR activation on the electrophysiological properties of cultured RGCs. Using perforated patch-clamp recordings in current-clamp configuration, we found that application of DHPG increased spontaneous spiking and depolarized the resting membrane potential of RGCs. This boosting effect was attributed to an increase in membrane resistance due to blockade of a background K+ conductance. Further experiments showed that the group I mGluR-sensitive K+ conductance was not blocked by 3 mM Cs+, but was sensitive to acidification. Pharmacological studies indicated that the effect of DHPG on RGCs was mediated by the mGluR1 rather than the mGluR5 receptor subtype. Our results suggest a facilitatory role for group I mGluR activation in modulating RGC excitability in the mammalian inner retina.

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Synaptic inputs from identified bipolar and amacrine cells to a sparsely branched ganglion cell in rabbit retina

Visual Neuroscience ◽

10.1017/s0952523819000014 ◽

2019 ◽

Vol 36 ◽

Cited By ~ 4

Author(s):

Andrea S. Bordt ◽

Diego Perez ◽

Luke Tseng ◽

Weiley Sunny Liu ◽

Jay Neitz ◽

...

Keyword(s):

Ganglion Cell ◽

Retinal Ganglion Cells ◽

Amacrine Cell ◽

Ganglion Cells ◽

Amacrine Cells ◽

Bipolar Cells ◽

Rabbit Retina ◽

Retinal Ganglion ◽

Synaptic Inputs ◽

Class Iv

AbstractThere are more than 30 distinct types of mammalian retinal ganglion cells, each sensitive to different features of the visual environment. In rabbit retina, they can be grouped into four classes according to their morphology and stratification of their dendrites in the inner plexiform layer (IPL). The goal of this study was to describe the synaptic inputs to one type of Class IV ganglion cell, the third member of the sparsely branched Class IV cells (SB3). One cell of this type was partially reconstructed in a retinal connectome developed using automated transmission electron microscopy (ATEM). It had slender, relatively straight dendrites that ramify in the sublamina a of the IPL. The dendrites of the SB3 cell were always postsynaptic in the IPL, supporting its identity as a ganglion cell. It received 29% of its input from bipolar cells, a value in the middle of the range for rabbit retinal ganglion cells studied previously. The SB3 cell typically received only one synapse per bipolar cell from multiple types of presumed OFF bipolar cells; reciprocal synapses from amacrine cells at the dyad synapses were infrequent. In a few instances, the bipolar cells presynaptic to the SB3 ganglion cell also provided input to an amacrine cell presynaptic to the ganglion cell. There was apparently no crossover inhibition from narrow-field ON amacrine cells. Most of the amacrine cell inputs were from axons and dendrites of GABAergic amacrine cells, likely providing inhibitory input from outside the classical receptive field.

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