Synaptic transmission at retinal ribbon synapses

Heidelberger, Ruth; Thoreson, Wallace B.; Witkovsky, Paul

doi:10.1016/j.preteyeres.2005.04.002

Cited by 209 publications

(250 citation statements)

References 359 publications

(576 reference statements)

Supporting

Mentioning

231

Contrasting

Order By: Relevance

“…5B). The integral of the deconvolved average AF response with 5 mM EGTA was best fit with two rather than three exponentials: 1 ϭ 27 ms, 2 (Fig. 5C, red trace).…”

Section: Resultsmentioning

confidence: 98%

See 1 more Smart Citation

Time course and calcium dependence of transmitter release at a single ribbon synapse

Goutman

Glowatzki

2007

Proc. Natl. Acad. Sci. U.S.A.

222

322

View full text Add to dashboard Cite

At the first synapse in the auditory pathway, the receptor potential of mechanosensory hair cells is converted into a firing pattern in auditory nerve fibers. For the accurate coding of timing and intensity of sound signals, transmitter release at this synapse must occur with the highest precision. To measure directly the transfer characteristics of the hair cell afferent synapse, we implemented simultaneous whole-cell recordings from mammalian inner hair cells (IHCs) and auditory nerve fiber terminals that typically receive input from a single ribbon synapse. During a 1-s IHC depolarization, the synaptic response depressed >90%, representing the main source for adaptation in the auditory nerve. Synaptic depression was slightly affected by ␣-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor desensitization; however, it was mostly caused by reduced vesicular release. When the transfer function between transmitter release and Ca 2؉ influx was tested at constant open probability for Ca 2؉ channels (potentials >0 mV), a super linear relation was found. This relation is presumed to result from the cooperative binding of three to four Ca 2؉ ions at the Ca 2؉ sensor. However, in the physiological range for receptor potentials (؊50 to ؊30 mV), the relation between Ca 2؉ influx and afferent activity was linear, assuring minimal distortion in the coding of sound intensity. Changes in Ca 2؉ influx caused an increase in release probability, but not in the average size of multivesicular synaptic events. By varying Ca 2؉ buffering in the IHC, we further investigate how Ca 2؉ channel and Ca 2؉ sensor at this synapse might relate.hearing ͉ exocytosis ͉ hair cell ͉ synaptic transmission ͉ auditory nerve fiber M echanosensory hair cells of the inner ear release neurotransmitter continuously and with high temporal precision onto dendrites of auditory nerve fibers (AFs) (1); therefore, availability of releasable synaptic vesicles is critical. Synaptic ribbons, presynaptic structures presenting a halo of tethered vesicles, also found in retinal photoreceptors and bipolar cells (2), are thought to facilitate accumulation of vesicles presynaptically (3). Postsynaptically, ␣-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptors mediate fast synaptic transmission (4). The response of the cochlea to sound has been investigated in great detail: prolonged sound stimulation produces an increase in the firing activity of the auditory nerve that adapts on a milliseconds time scale (5). However, direct demonstration of the synaptic processes underlying adaptation and sustained release is still missing. Heretofore, hair cell exocytosis has been measured by changes in membrane capacitance that sum activity from all of the dozens of ribbon synapses in each cell (3). Capacitance measurements therefore cannot distinguish properties of individual ribbons and are limited in temporal resolution, requiring extrapolation for the earliest components. Nor does this approach reveal what role postsynaptic desensitization might play.I...

show abstract

“…5B). The integral of the deconvolved average AF response with 5 mM EGTA was best fit with two rather than three exponentials: 1 ϭ 27 ms, 2 (Fig. 5C, red trace).…”

Section: Resultsmentioning

confidence: 98%

“…Synaptic ribbons, presynaptic structures presenting a halo of tethered vesicles, also found in retinal photoreceptors and bipolar cells (2), are thought to facilitate accumulation of vesicles presynaptically (3). Postsynaptically, ␣-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptors mediate fast synaptic transmission (4).…”

mentioning

confidence: 99%

Time course and calcium dependence of transmitter release at a single ribbon synapse

Goutman

Glowatzki

2007

Proc. Natl. Acad. Sci. U.S.A.

222

322

View full text Add to dashboard Cite

show abstract

“…e d u Abbreviations used in this paper: BC, bipolar cell; CaM, calmodulin; EPSC, excitatory postsynaptic current; ERG, electroretinogram; HC, horizontal cell; IRP, immediately releasable pool; MLCK, myosin light chain kinase; PPR, paired pulse ratio; RBC, rod BC; TIRFM, total internal reflection fluorescence microscopy. primed vesicles for release at the presynaptic membrane (Heidelberger et al, 2005;Snellman et al, 2011). Recent studies have shown that the interplay of vesicle release and replenishment at the ribbon are important in encoding luminance and contrast by cones (Jackman et al, 2009;Babai et al, 2010) and rod BCs (RBCs; Oesch and Diamond, 2011;Ke et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

Calmodulin enhances ribbon replenishment and shapes filtering of synaptic transmission by cone photoreceptors

Hook¹,

Parmelee²,

Chen³

et al. 2014

J Cell Biol

Self Cite

View full text Add to dashboard Cite

At the first synapse in the vertebrate visual pathway, light-evoked changes in photoreceptor membrane potential alter the rate of glutamate release onto second-order retinal neurons. This process depends on the synaptic ribbon, a specialized structure found at various sensory synapses, to provide a supply of primed vesicles for release. Calcium (Ca 2+ ) accelerates the replenishment of vesicles at cone ribbon synapses, but the mechanisms underlying this acceleration and its functional implications for vision are unknown. We studied vesicle replenishment using paired whole-cell recordings of cones and postsynaptic neurons in tiger salamander retinas and found that it involves two kinetic mechanisms, the faster of which was diminished by calmodulin (CaM) inhibitors. We developed an analytical model that can be applied to both conventional and ribbon synapses and showed that vesicle resupply is limited by a simple time constant,  = 1/(Ds), where D is the vesicle diffusion coefficient,  is the vesicle diameter,  is the vesicle density, and s is the probability of vesicle attachment. The combination of electrophysiological measurements, modeling, and total internal reflection fluorescence microscopy of single synaptic vesicles suggested that CaM speeds replenishment by enhancing vesicle attachment to the ribbon. Using electroretinogram and whole-cell recordings of light responses, we found that enhanced replenishment improves the ability of cone synapses to signal darkness after brief flashes of light and enhances the amplitude of responses to higherfrequency stimuli. By accelerating the resupply of vesicles to the ribbon, CaM extends the temporal range of synaptic transmission, allowing cones to transmit higher-frequency visual information to downstream neurons. Thus, the ability of the visual system to encode time-varying stimuli is shaped by the dynamics of vesicle replenishment at photoreceptor synaptic ribbons.

show abstract

“…Photoreceptors have an unusual type of synapse in their terminals, the ribbon synapse, which is structurally and functionally specialized for a large and tonic release of neurotransmitter (6)(7)(8)(9)(10). The synaptic ribbon is a plate-like structure that extends from the site of transmitter release into the synaptic terminal cytoplasm and has hundreds of synaptic vesicles tethered to it (11).…”

mentioning

confidence: 99%

Zebrafish larvae lose vision at night

Emran

Rihel²,

Adolph³

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

Darkness serves as a stimulus for vertebrate photoreceptors; they are actively depolarized in the dark and hyperpolarize in the light. Here, we show that larval zebrafish essentially turn off their visual system at night when they are not active. Electroretinograms recorded from larval zebrafish show large differences between day and night; the responses are normal in amplitude throughout the day but are almost absent after several hours of darkness at night. Behavioral testing also shows that larval zebrafish become unresponsive to visual stimuli at night. This phenomenon is largely circadian driven as fish show similar dramatic changes in visual responsiveness when maintained in continuous darkness, although light exposure at night partially restores the responses. Visual responsiveness is decreased at night by at least two mechanisms: photoreceptor outer segment activity decreases and synaptic ribbons in cone pedicles disassemble.photoreceptors | circadian rhythm | synaptic plasticity

show abstract

Synaptic transmission at retinal ribbon synapses

Cited by 209 publications

References 359 publications

Time course and calcium dependence of transmitter release at a single ribbon synapse

Time course and calcium dependence of transmitter release at a single ribbon synapse

Calmodulin enhances ribbon replenishment and shapes filtering of synaptic transmission by cone photoreceptors

Zebrafish larvae lose vision at night

Contact Info

Product

Resources

About