Excitatory Synaptic Inputs to Mouse On-Off Direction-Selective Retinal Ganglion Cells Lack Direction Tuning

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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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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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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Evidence for glycine modulation of excitatory synaptic inputs to retinal ganglion cells

Journal of Neuroscience ◽

10.1523/jneurosci.15-06-04592.1995 ◽

1995 ◽

Vol 15 (6) ◽

pp. 4592-4601 ◽

Cited By ~ 27

Author(s):

PD Lukasiewicz ◽

RC Roeder

Keyword(s):

Retinal Ganglion Cells ◽

Ganglion Cells ◽

Retinal Ganglion ◽

Synaptic Inputs

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Analysis of Excitatory and Inhibitory Spontaneous Synaptic Activity in Mouse Retinal Ganglion Cells

Journal of Neurophysiology ◽

10.1152/jn.1998.80.3.1327 ◽

1998 ◽

Vol 80 (3) ◽

pp. 1327-1340 ◽

Cited By ~ 54

Author(s):

Ning Tian ◽

Thomas N. Hwang ◽

David R. Copenhagen

Keyword(s):

Retinal Ganglion Cells ◽

Time Constant ◽

Decay Time ◽

Ganglion Cells ◽

Glycine Receptor ◽

Synaptic Activity ◽

Decay Time Constant ◽

Retinal Ganglion ◽

Synaptic Inputs ◽

Perforated Patch

Tian, Ning, Thomas N. Hwang, and David R. Copenhagen. Analysis of excitatory and inhibitory spontaneous synaptic activity in mouse retinal ganglion cells. J. Neurophysiol. 80: 1327–1340, 1998. Spontaneous inhibitory and excitatory postsynaptic currents (sIPSCs and sEPSCs) were identified and characterized with whole cell and perforated patch voltage-clamp recordings in adult mouse retinal ganglion cells. Pharmacological dissection revealed that all cells were driven by spontaneous synaptic inputs mediated by glutamate and γ-aminobutyric acid-A (GABAA) receptors. One-half (7/14) of the cells also received glycinergic spontaneous synaptic inputs. Both GABAA and glycine receptor–mediated sIPSCs had rise times (10–90%) of <1 ms. The decay times of the GABAA receptor–mediated sIPSCs were comparable with those of the glycine receptor–mediated sIPSCs. The average decay time constant for monoexponentially fitted sIPSCs was 63.2 ± 74.1 ms (mean ± SD, n = 3278). Glutamate receptor–mediated sEPSCs had an average rise time of 0.50 ± 0.20 ms ( n = 109) and an average monoexponential decay time constant of 5.9 ± 8.6 ms ( n = 2705). Slightly more than two-thirds of the spontaneous synaptic events were monoexponential (68% for sIPSCs and 76% for sEPSCs). The remainder of the events was biexponential. The amplitudes of the spontaneous synaptic events were not correlated with rise times, suggesting that the electrotonic filtering properties of the neurons and/or differences in the spatial location of synaptic inputs could not account for the difference between the decay time constants of the glutamate and GABAA/glycine receptor–mediated spontaneous synaptic events. The amplitudes of sEPSCs were similar to those recorded in tetrodotoxin (TTX), consistent with the events measured in control saline being the response to the release of a single quantum of transmitter. The range of the sIPSC amplitudes in control saline was wider than that recorded in TTX, consistent with some sIPSCs being evoked by presynaptic spikes having an average quantal size greater than one. The rates of sIPSCs and sEPSCs were determined under equivalent conditions by recording with perforated patch electrodes at potentials at which both types of event could be identified. Two groups of ganglion cell were observed; one group had an average sEPSCs/sIPSCs frequency ratio of 0.96 ± 0.77 ( n = 28) and another group had an average ratio of 6.63 ± 0.82 ( n = 7). These findings suggest that a subset of cells is driven much more strongly by excitatory synaptic inputs. We propose that this subset of cells could be off ganglion cells, consistent with the higher frequency of spontaneous action potentials found in off ganglion cells in other studies.

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Synaptic inputs to physiologically defined turtle retinal ganglion cells

Visual Neuroscience ◽

10.1017/s0952523800009718 ◽

1991 ◽

Vol 7 (5) ◽

pp. 409-429 ◽

Cited By ~ 17

Author(s):

Jay F. Muller ◽

Josef Ammermüller ◽

Richard A. Normann ◽

Helga Kolb

Keyword(s):

Ganglion Cell ◽

Retinal Ganglion Cells ◽

Bipolar Cell ◽

Ganglion Cells ◽

Bipolar Cells ◽

Inner Plexiform Layer ◽

Retinal Ganglion ◽

Electron Microscopic Autoradiography ◽

Golgi Impregnation ◽

Synaptic Inputs

AbstractTwo physiologically distinct, HRP-marked turtle retinal ganglion cells were examined for their morphology, GABAergic, glycinergic, and bipolar cell synaptic inputs, using electron-microscopic autoradiography and postembedding immunocytochemistry. One cell was a color-opponent, transient ON/OFF ganglion cell. Its center response to red was a sustained hyperpolarization, and its center response to green was a depolarization with increased spiking at onset. The HRP-injected cell most resembled G6, from previous Golgi-impregnation studies (Kolb, 1982; Kolb et al., 1988). It was a narrow-field bistratified cell, whose two broad dendritic strata peaked at approximately levels L20–25 (sublamina a) and L60 (sublamina b) of the inner plexiform layer. Bipolar cell synapses onto G6 were found evenly distributed between its distal and proximal dendritic strata, spanning L20–75. These inputs probably originated from several different bipolar cells, reflecting the complexity of the center response. GABAergic inputs were found onto both the distal and proximal strata, from near L20–L85. Only a few glycinergic inputs, confined to dendrites at L50–70, were observed.A second ganglion cell type that we physiologically characterized and HRP-injected had sustained ON-center, sustained OFF-surround responses. Two examples were studied; both were bistratified in sublamina b, near L60–70 and L85–100, with branches up to near L40. They resembled G10, from previous Golgi-impregnation studies (Kolb, 1982; Kolb et al., 1988). One cell was partially reconstructed to look at the distributions of GABAergic and glycinergic amacrine cell, and bipolar cell inputs. Although synapses from bipolar cells were equally divided between the two major dendritic strata of G10, the inputs to the distal stratum were close to the soma, and the inputs to the more proximal stratum were on the peripheral dendrites. This arrangement may reflect input from two distinct types of ON-bipolar cell. GABAergic and glycinergic inputs to G10 costratified to both strata and to the distal branches; but where glycinergic inputs were found distributed throughout the arbor, GABAergic inputs appeared to be confined to peripheral dendrites. We hypothesize on the neural elements involved and the circuitry that may underlie the physiologically recorded receptive fields of these two very different ganglion cell types in the turtle retina.

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Heterogeneous Intrinsic Firing Properties of Vertebrate Retinal Ganglion Cells

Journal of Neurophysiology ◽

10.1152/jn.00179.2001 ◽

2002 ◽

Vol 87 (1) ◽

pp. 30-41 ◽

Cited By ~ 15

Author(s):

Toshihide Tabata ◽

Masanobu Kano

Keyword(s):

Retinal Ganglion Cells ◽

Firing Pattern ◽

Ganglion Cells ◽

Light Response ◽

Firing Frequency ◽

Retinal Ganglion ◽

Synaptic Inputs ◽

Firing Properties ◽

Intrinsic Firing ◽

Frequency Current

Retinal ganglion cells (RGCs) use their characteristic firing patterns to encode various aspects of visual information and carry them to the brain. It has been thought that the firing pattern of an RGC's light response is determined primarily by the time course and spatiotemporal interaction of the synaptic inputs. However, it is unclear whether there is a difference in intrinsic firing properties among RGCs that could contribute to the cell-to-cell distinction of the light response firing pattern. We investigated the intrinsic firing properties of isolated goldfish RGCs, minimizing cytoplasmic disturbance with a perforated-patch, whole-cell recording technique. In response to a 1-s depolarizing current step, the majority of the examined RGCs ( n = 84) displayed sustained firing that lasted over 800 ms ( n = 24; tonic RGCs) or transient firing accommodated within 200 ms of the step onset ( n = 47; phasic RGCs). Tonic and phasic RGCs also differed in their firing frequency–current intensity dynamics. There was a significant difference in the soma sizes of phasic and tonic RGCs, indicating that some parts of these groups originate from distinct morphological subtypes. In the presence of extracellular Ba2+ (1 mM), phasic RGCs displayed sustained firing and firing frequency–current intensity dynamics similar to those of tonic RGCs. Thus a Ba2+-sensitive ion current (IBa-s) underlies the firing characteristics of phasic RGCs. Under voltage-clamp conditions, IBa-s was identified as a low-threshold, noninactivating voltage-dependent K+current. Because of its slow kinetics (time constant of activation, ∼100 ms), IBa-s may confer a gradually increasing hyperpolarizing driving force during maintained excitatory stimulus, which eventually would result in firing accommodation. These findings suggest that RGCs have heterogeneous intrinsic firing properties that could aid synaptic inputs in shaping light responses.

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