Multivesicular Release Increases the Efficiency of Information Transmission at Sensory Synapses

The statistics of vesicle release determine how information is transferred in neural circuits. The classical model is of Poisson synapses releasing vesicles independently but ribbon synapses transmit early sensory signals by multivesicular release (MVR) when two or more vesicles are coordinated as a single synaptic event. To investigate the impact of MVR on the spike code we used leaky integrate-and-fire models with inputs simulating the statistics of vesicle release measured experimentally from retinal bipolar cells. Comparing these with models of independent release we find that MVR increases spike generation and the efficiency of information transfer (bits per spike) over a range of conditions that mimic retinal ganglion cells of different time-constant receiving different number of synaptic inputs of different strengths. When a single input drives a neuron with short time-constant, as occurs when hair cells transmit auditory signals, MVR increases information transfer whenever spike generation requires depolarization greater than that caused by a single vesicle. This study demonstrates how presynaptic integration of vesicles by MVR can compensate for less effective summation post-synaptically to increase the efficiency with which sensory information is transmitted at the synapse.

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

10.21203/rs.2.21155/v1 ◽

2020 ◽

Author(s):

Hassan Bassereh ◽

Frank Rattay

Keyword(s):

Intracellular Calcium ◽

Voltage Clamp ◽

Bipolar Cell ◽

Reversal Potential ◽

Bipolar Cells ◽

Signal Delay ◽

Vesicle Release ◽

Ribbon Synapses ◽

Retinal Implants ◽

The Impact

Abstract 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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Multiple Firing Patterns in Deep Dorsal Horn Neurons of the Spinal Cord: Computational Analysis of Mechanisms and Functional Implications

Journal of Neurophysiology ◽

10.1152/jn.00919.2009 ◽

2010 ◽

Vol 104 (4) ◽

pp. 1978-1996 ◽

Cited By ~ 11

Author(s):

Yann Le Franc ◽

Gwendal Le Masson

Keyword(s):

Spinal Cord ◽

Dorsal Horn ◽

Information Transfer ◽

Network Effects ◽

Neuronal Response ◽

Sensory Information ◽

Firing Patterns ◽

Dorsal Horn Neurons ◽

The Impact

Deep dorsal horn relay neurons (dDHNs) of the spinal cord are known to exhibit multiple firing patterns under the control of local metabotropic neuromodulation: tonic firing, plateau potential, and spontaneous oscillations. This work investigates the role of interactions between voltage-gated channels and the occurrence of different firing patterns and then correlates these two phenomena with their functional role in sensory information processing. We designed a conductance-based model using the NEURON software package, which successfully reproduced the classical features of plateau in dDHNs, including a wind-up of the neuronal response after repetitive stimulation. This modeling approach allowed us to systematically test the impact of conductance interactions on the firing patterns. We found that the expression of multiple firing patterns can be reproduced by changes in the balance between two currents (L-type calcium and potassium inward rectifier conductances). By investigating a possible generalization of the firing state switch, we found that the switch can also occur by varying the balance of any hyperpolarizing and depolarizing conductances. This result extends the control of the firing switch to neuromodulators or to network effects such as synaptic inhibition. We observed that the switch between the different firing patterns occurs as a continuous function in the model, revealing a particular intermediate state called the accelerating mode. To characterize the functional effect of a firing switch on information transfer, we used correlation analysis between a model of peripheral nociceptive afference and the dDHN model. The simulation results indicate that the accelerating mode was the optimal firing state for information transfer.

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The number and distribution of bipolar to ganglion cell synapses in the inner plexiform layer of the anuran retina

Visual Neuroscience ◽

10.1017/s0952523800007744 ◽

1996 ◽

Vol 13 (6) ◽

pp. 1099-1107 ◽

Cited By ~ 6

Author(s):

Péter Buzás ◽

Sára Jeges ◽

Robert Gábriel

Keyword(s):

Ganglion Cell ◽

Cross Sections ◽

Information Transfer ◽

Ganglion Cells ◽

Receptive Fields ◽

Plexiform Layer ◽

Amacrine Cells ◽

Bipolar Cells ◽

Inner Plexiform Layer ◽

Flow Through

AbstractThe main route of information flow through the vertebrate retina is from the photoreceptors towards the ganglion cells whose axons form the optic nerve. Bipolar cells of the frog have been so far reported to contact mostly amacrine cells and the majority of input to ganglion cells comes from the amacrines. In this study, ganglion cells of frogs from two species (Bufo marinus, Xenopus laevis) were filled retrogradely with horseradish peroxidase. After visualization of the tracer, light-microscopic cross sections showed massive labeling of the somata in the ganglion cell layer as well as their dendrites in the inner plexiform layer. In cross sections, bipolar output and ganglion cell input synapses were counted in the electron microscope. Each synapse was assigned to one of the five equal sublayers (SLs) of the inner plexiform layer. In both species, bipolar cells were most often seen to form their characteristic synaptic dyads with two amacrine cells. In some cases, however, the dyads were directed to one amacrine and one ganglion cell dendrite. This type of synapse was unevenly distributed within the inner plexiform layer with the highest occurrence in SL2 both in Bufo and Xenopus. In addition, SL4 contained also a high number of this type of synapse in Xenopus. In both species, we found no or few bipolar to ganglion cell synapses in the marginal sublayers (SLs 1 and 5). In Xenopus, 22% of the bipolar cell output synapses went onto ganglion cells, whereas in Bufo this was only 10%. We conclude that direct bipolar to ganglion cell information transfer exists also in frogs although its occurrence is not as obvious and regular as in mammals. The characteristic distribution of these synapses, however, suggests that specific type of the bipolar and ganglion cells participate in this process. These contacts may play a role in the formation of simple ganglion cell receptive fields.

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Synaptic circuits for irradiance coding by intrinsically photosensitive retinal ganglion cells

10.1101/442954 ◽

2018 ◽

Cited By ~ 3

Author(s):

Shai Sabbah ◽

Carin Papendorp ◽

Elizabeth Koplas ◽

Marjo Beltoja ◽

Cameron Etebari ◽

...

Keyword(s):

Retinal Ganglion Cells ◽

Ganglion Cells ◽

Bipolar Cells ◽

Retinal Ganglion ◽

Electron Microscopic ◽

Synaptic Circuits ◽

Ribbon Synapses ◽

High Pass ◽

Excitatory Drive ◽

Rod Bipolar Cells

SummaryWe have explored the synaptic networks responsible for the unique capacity of intrinsically photosensitive retinal ganglion cells (ipRGCs) to encode overall light intensity. This luminance signal is crucial for circadian, pupillary and related reflexive responses light. By combined glutamate-sensor imaging and patch recording of postsynaptic RGCs, we show that the capacity for intensity-encoding is widespread among cone bipolar types, including OFF types.Nonetheless, the bipolar cells that drive ipRGCs appear to carry the strongest luminance signal. By serial electron microscopic reconstruction, we show that Type 6 ON cone bipolar cells are the dominant source of such input, with more modest input from Types 7, 8 and 9 and virtually none from Types 5i, 5o, 5t or rod bipolar cells. In conventional RGCs, the excitatory drive from bipolar cells is high-pass temporally filtered more than it is in ipRGCs. Amacrine-to-bipolar cell feedback seems to contribute surprisingly little to this filtering, implicating mostly postsynaptic mechanisms. Most ipRGCs sample from all bipolar terminals costratifying with their dendrites, but M1 cells avoid all OFF bipolar input and accept only ectopic ribbon synapses from ON cone bipolar axonal shafts. These are remarkable monad synapses, equipped with as many as a dozen ribbons and only one postsynaptic process.

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Bipolar input to melanopsin containing ganglion cells in primate retina

Visual Neuroscience ◽

10.1017/s095252381000026x ◽

2010 ◽

Vol 28 (1) ◽

pp. 39-50 ◽

Cited By ~ 38

Author(s):

ULRIKE GRÜNERT ◽

PATRICIA R. JUSUF ◽

SAMMY C.S. LEE ◽

DUNG THAN NGUYEN

Keyword(s):

Ganglion Cells ◽

Close Contact ◽

Dimensional Space ◽

Cell Types ◽

Bipolar Cells ◽

Light Responses ◽

Axon Terminals ◽

Ribbon Synapses ◽

Bipolar Type ◽

Rod Bipolar Cells

AbstractTwo morphological types of melanopsin-expressing ganglion cells have been described in primate retina. Both types show intrinsic light responses as well as rod- and cone-driven ON-type responses. Outer stratifying cells have their dendrites close to the inner nuclear layer (OFF sublamina); inner stratifying cells have their dendrites close to the ganglion cell layer (ON sublamina). Both inner and outer stratifying cells receive synaptic input via ribbon synapses, but the bipolar cell types providing this input have not been identified. Here, we addressed the question whether the diffuse (ON) cone bipolar type DB6 and/or rod bipolar cells contact melanopsin-expressing ganglion cells. Melanopsin containing ganglion cells in marmoset (Callithrix jacchus) and macaque (Macaca fascicularis) retinas were identified immunohistochemically; DB6 cells were labeled with antibodies against the carbohydrate epitope CD15, rod bipolar cells were labeled with antibodies against protein kinase C, and putative synapses between the two cells types were identified with antibodies against piccolo. For one inner cell, nearly all of the DB6 axon terminals that overlap with its dendrites in the two-dimensional space show areas of close contact. In vertical sections, the large majority of the areas of close contact also contain a synaptic punctum, suggesting that DB6 cells contact inner melanopsin cells. The output from DB6 cells accounts for about 30% of synapses onto inner melanopsin cells. Synaptic contacts between rod bipolar axons and inner dendrites were not observed. In the OFF sublamina, about 10% of the DB6 axons are closely associated with dendrites of outer cells, and in about a third of these areas, axonal en passant synapses are detected. This result suggests that DB6 cells may also provide input to outer melanopsin cells.

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Synchronized amplification of local information transmission by peripheral retinal input

eLife ◽

10.7554/elife.09266 ◽

2015 ◽

Vol 4 ◽

Cited By ~ 4

Author(s):

Pablo D Jadzinsky ◽

Stephen A Baccus

Keyword(s):

Information Transmission ◽

Sensory Input ◽

Time Window ◽

Ganglion Cells ◽

Sensory Information ◽

Bipolar Cells ◽

Dynamic Allocation ◽

Sensory Stimuli ◽

Retinal Input ◽

Expected Increase

Sensory stimuli have varying statistics influenced by both the environment and by active sensing behaviors that rapidly and globally change the sensory input. Consequently, sensory systems often adjust their neural code to the expected statistics of their sensory input to transmit novel sensory information. Here, we show that sudden peripheral motion amplifies and accelerates information transmission in salamander ganglion cells in a 50 ms time window. Underlying this gating of information is a transient increase in adaptation to contrast, enhancing sensitivity to a broader range of stimuli. Using a model and natural images, we show that this effect coincides with an expected increase in information in bipolar cells after a global image shift. Our findings reveal the dynamic allocation of energy resources to increase neural activity at times of expected high information content, a principle of adaptation that balances the competing requirements of conserving spikes and transmitting information.

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Synaptic connections of amacrine cells containing vesicular glutamate transporter 3 in baboon retinas

Visual Neuroscience ◽

10.1017/s0952523815000036 ◽

2015 ◽

Vol 32 ◽

Cited By ~ 7

Author(s):

DAVID W. MARSHAK ◽

ALICE Z. CHUANG ◽

DREW M. DOLINO ◽

ROY A. JACOBY ◽

WEILEY S. LIU ◽

...

Keyword(s):

Ganglion Cells ◽

Glutamate Transporter ◽

Plexiform Layer ◽

Amacrine Cells ◽

Bipolar Cells ◽

Inhibitory Synapses ◽

Inner Plexiform Layer ◽

Vesicular Glutamate Transporter ◽

Synaptic Connections ◽

Ribbon Synapses

AbstractThe goals of these experiments were to describe the morphology and synaptic connections of amacrine cells in the baboon retina that contain immunoreactive vesicular glutamate transporter 3 (vGluT3). These amacrine cells had the morphology characteristic of knotty bistratified type 1 cells, and their dendrites formed two plexuses on either side of the center of the inner plexiform layer. The primary dendrites received large synapses from amacrine cells, and the higher-order dendrites were both pre- and postsynaptic to other amacrine cells. Based on light microscopic immunolabeling results, these include AII cells and starburst cells, but not the polyaxonal amacrine cells tracer-coupled to ON parasol ganglion cells. The vGluT3 cells received input from ON bipolar cells at ribbon synapses and made synapses onto OFF bipolar cells, including the diffuse DB3a type. Many synapses from vGluT3 cells onto retinal ganglion cells were observed in both plexuses. At synapses where vGluT3 cells were presynaptic, two types of postsynaptic densities were observed; there were relatively thin ones characteristic of inhibitory synapses and relatively thick ones characteristic of excitatory synapses. In the light microscopic experiments with Neurobiotin-injected ganglion cells, vGluT3 cells made contacts with midget and parasol ganglion cells, including both ON and OFF types. Puncta containing immunoreactive gephyrin, an inhibitory synapse marker, were found at appositions between vGluT3 cells and each of the four types of labeled ganglion cells. The vGluT3 cells did not have detectable levels of immunoreactive γ-aminobutyric acid (GABA) or immunoreactive glycine transporter 1. Thus, the vGluT3 cells would be expected to have ON responses to light and make synapses onto neurons in both the ON and the OFF pathways. Taken with previous results, these findings suggest that vGluT3 cells release glycine at some of their output synapses and glutamate at others.

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Efficient stimulus-secretion coupling at ribbon synapses requires RIM-binding protein tethering of L-type Ca2+channels

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1702991114 ◽

2017 ◽

Vol 114 (38) ◽

pp. E8081-E8090 ◽

Cited By ~ 10

Author(s):

Fujun Luo ◽

Xinran Liu ◽

Thomas C. Südhof ◽

Claudio Acuna

Keyword(s):

Active Zone ◽

Neurotransmitter Release ◽

Information Transfer ◽

Bipolar Cells ◽

Mouse Retina ◽

Tight Coupling ◽

Ribbon Synapses ◽

Vesicle Exocytosis ◽

Stimulus Secretion Coupling

Fast neurotransmitter release from ribbon synapses via Ca2+-triggered exocytosis requires tight coupling of L-type Ca2+channels to release-ready synaptic vesicles at the presynaptic active zone, which is localized at the base of the ribbon. Here, we used genetic, electrophysiological, and ultrastructural analyses to probe the architecture of ribbon synapses by perturbing the function of RIM-binding proteins (RBPs) as central active-zone scaffolding molecules. We found that genetic deletion of RBP1 and RBP2 did not impair synapse ultrastructure of ribbon-type synapses formed between rod bipolar cells (RBCs) and amacrine type-2 (AII) cells in the mouse retina but dramatically reduced the density of presynaptic Ca2+channels, decreased and desynchronized evoked neurotransmitter release, and rendered evoked and spontaneous neurotransmitter release sensitive to the slow Ca2+buffer EGTA. These findings suggest that RBPs tether L-type Ca2+channels to the active zones of ribbon synapses, thereby synchronizing vesicle exocytosis and promoting high-fidelity information transfer in retinal circuits.

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Pre-Emphasis Pulse Design for Random-Access Memory

Electronics ◽

10.3390/electronics10121454 ◽

2021 ◽

Vol 10 (12) ◽

pp. 1454

Author(s):

Yoshihiro Sugiura ◽

Toru Tanzawa

Keyword(s):

Time Constant ◽

Random Access ◽

Memory Cell ◽

Random Access Memory ◽

Memory Access ◽

Access Time ◽

Access Memory ◽

Delay Times ◽

Cell Current ◽

The Impact

This paper describes how one can reduce the memory access time with pre-emphasis (PE) pulses even in non-volatile random-access memory. Optimum PE pulse widths and resultant minimum word-line (WL) delay times are investigated as a function of column address. The impact of the process variation in the time constant of WL, the cell current, and the resistance of deciding path on optimum PE pulses are discussed. Optimum PE pulse widths and resultant minimum WL delay times are modeled with fitting curves as a function of column address of the accessed memory cell, which provides designers with the ability to set the optimum timing for WL and BL (bit-line) operations, reducing average memory access time.

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The effect of water immersion on vection in virtual reality

Scientific Reports ◽

10.1038/s41598-020-80100-y ◽

2021 ◽

Vol 11 (1) ◽

Author(s):

Géraldine Fauville ◽

Anna C. M. Queiroz ◽

Erika S. Woolsey ◽

Jonathan W. Kelly ◽

Jeremy N. Bailenson

Keyword(s):

Virtual Reality ◽

Motion Sickness ◽

Water Immersion ◽

Sensory Information ◽

Future Research ◽

Visually Induced Motion Sickness ◽

Wide Range ◽

Induced Motion ◽

Ground Condition ◽

The Impact

AbstractResearch about vection (illusory self-motion) has investigated a wide range of sensory cues and employed various methods and equipment, including use of virtual reality (VR). However, there is currently no research in the field of vection on the impact of floating in water while experiencing VR. Aquatic immersion presents a new and interesting method to potentially enhance vection by reducing conflicting sensory information that is usually experienced when standing or sitting on a stable surface. This study compares vection, visually induced motion sickness, and presence among participants experiencing VR while standing on the ground or floating in water. Results show that vection was significantly enhanced for the participants in the Water condition, whose judgments of self-displacement were larger than those of participants in the Ground condition. No differences in visually induced motion sickness or presence were found between conditions. We discuss the implication of this new type of VR experience for the fields of VR and vection while also discussing future research questions that emerge from our findings.

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