Mechanism of High-Frequency Signaling at a Depressing Ribbon Synapse

Grabner, Chad P.; Ratliff, Charles P.; Light, Adam; DeVries, Steven H.

doi:10.1016/j.neuron.2016.05.019

Cited by 30 publications

(70 citation statements)

References 67 publications

(105 reference statements)

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“…The recovery time constant in mouse RBC is 417 ms (Wan et al 2008). Cb2 BC in ground squirrels has a time constant of 70-140 ms (Light and DeVries 2007;Grabner et al 2016), while this number for the Cb3 BC is 524-888 ms (Light and DeVries 2007;Grabner et al 2016) and for the Cb1 is 482-734 ms (Grabner et al 2016). To our knowledge, the recovery time constant of BCs in rabbit and monkey…”

Section: Discussionmentioning

confidence: 86%

Two mathematical frameworks for vesicle release from a ribbon synapse of a retinal bipolar cell

Bassereh¹,

Rattay²

2020

Preprint

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Background: Bipolar cells communicate with amacrine and ganglion cells of the retina via both transient and sustained neurotransmitter release in ribbon synapses. Reconstructing the published quantitative release data from electrical soma stimulation (voltage clamp experiments) of rat rod bipolar cells were used to develop two simple models to predict the number of released vesicles as time series. In the experiment, the currents coming to the AII amacrine cell originating from releasing vesicles from the rod bipolar cell were recorded using paired-recordings in whole-cell voltage-clamp method. One of the models is based directly on terminal transmembrane voltage, so-called ‘modelV’, whereas the temporally exacter modelCa includes changes of intracellular calcium concentrations at terminals. Results: The intracellular calcium concentration method replicates a 0.43-ms signal delay for the transient release to pulsatile stimulation as a consequence of calcium channel dynamics in the presynaptic membrane, while the modelV has no signal delay. Both models produce the quite similar results in low stimuli amplitudes. However, for large stimulation intensities that may be done during extracellular stimulations in retinal implants, the modelCa predicts that the reversal potential of calcium limits the number of transiently released vesicles. Adding sodium and potassium ion channels to the axon of the cell enable to study the impact of spikes on the transient release in BC ribbons. A spike elicited by somatic stimulation causes the rapid release of all vesicles that are available for transient release, while a non-spiking BC with a similar morphometry needs stronger stimuli for any transient vesicle release. During extracellular stimulation, there was almost no difference in transient release between the active and passive cells because in both cases the terminal membrane of the cell senses the same potentials originating from the microelectrode. An exception was found for long pulses when the spike has the possibility to generate a higher terminal voltage than the passive cell. Simulated periodic 5 Hz stimulation showed a reduced transient release of 3 vesicles per stimulus, which is a recovery effect. Conclusions: We presented two mathematical concepts for vesicle release in ribbon synapses and explained decreasing efficiency in retinal implants for suprathreshold stimulation.

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Section: Discussionmentioning

confidence: 86%

Two mathematical frameworks for vesicle release from a ribbon synapse of a retinal bipolar cell

Bassereh¹,

Rattay²

2020

Preprint

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“…Our results showed that ribbon-mediated release in rods recovered from paired pulse depression with a biexponential time course similar to that observed in cones ( Van Hook et al, 2014 ; Thoreson et al, 2016 ). Under normal circumstances, the principal rate-limiting step that limits synaptic transmission to HCs during sinusoidal stimulation of cones is the fast component of this replenishment process that has a time constant of 600–800 ms ( Innocenti and Heidelberger, 2008 ; Van Hook et al, 2014 ; Grabner et al, 2016 ; Thoreson et al, 2016 ). In both rods and cones, this fast replenishment process involves actions of Ca 2+ operating through calmodulin to enhance vesicle attachment to the ribbon and thereby speed replenishment of ribbon release sites ( Van Hook et al, 2014 ; Van Hook and Thoreson, 2015 ).…”

Section: Discussionmentioning

confidence: 99%

Endocytosis sustains release at photoreceptor ribbon synapses by restoring fusion competence

Wen

Hook

Grassmeyer

et al. 2018

Journal of General Physiology

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“…For example, the high frequency‐encoding BC type in the ground squirrel expresses high‐affinity glutamate receptors, which saturate quickly and therefore do not profit from a broad glutamate concentration range (Grabner et al . ).…”

Section: Introductionmentioning

confidence: 97%

How do horizontal cells ‘talk’ to cone photoreceptors? Different levels of complexity at the cone–horizontal cell synapse

Chapot

Euler

Schubert

2017

The Journal of Physiology

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The first synapse of the retina plays a fundamental role in the visual system. Due to its importance, it is critical that it encodes information from the outside world with the greatest accuracy and precision possible. Cone photoreceptor axon terminals contain many individual synaptic sites, each represented by a presynaptic structure called a 'ribbon'. These synapses are both highly sophisticated and conserved. Each ribbon relays the light signal to one ON cone bipolar cell and several OFF cone bipolar cells, while two dendritic processes from a GABAergic interneuron, the horizontal cell, modulate the cone output via parallel feedback mechanisms. The presence of these three partners within a single synapse has raised numerous questions, and its anatomical and functional complexity is still only partially understood. However, the understanding of this synapse has recently evolved, as a consequence of progress in understanding dendritic signal processing and its role in facilitating global versus local signalling. Indeed, for the downstream retinal network, dendritic processing in horizontal cells may be essential, as they must support important functional operations such as contrast enhancement, which requires spatial averaging of the photoreceptor array, while at the same time preserving accurate spatial information. Here, we review recent progress made towards a better understanding of the cone synapse, with an emphasis on horizontal cell function, and discuss why such complexity might be necessary for early visual processing.

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Mechanism of High-Frequency Signaling at a Depressing Ribbon Synapse

Cited by 30 publications

References 67 publications

Two mathematical frameworks for vesicle release from a ribbon synapse of a retinal bipolar cell

Two mathematical frameworks for vesicle release from a ribbon synapse of a retinal bipolar cell

Endocytosis sustains release at photoreceptor ribbon synapses by restoring fusion competence

How do horizontal cells ‘talk’ to cone photoreceptors? Different levels of complexity at the cone–horizontal cell synapse

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