Coordinated multivesicular release at a mammalian ribbon synapse

Singer, Joshua H.; Lassová, Luisa; Vardi, Noga; Diamond, Jeffrey S.

doi:10.1038/nn1280

Cited by 208 publications

(279 citation statements)

References 46 publications

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“…In contrast, the RRP estimate from ⌬C m measurements in mouse inner hair cells is Ϸ53-64 SVs per synapse, whereas the morphologically docked SV pool contains only [16][17][18][19][20][21][22][23][24][25][26][27][28][29][30]. Some of this difference may be due to the fact that synaptic exocytosis had not been inhibited before fixation, which in frog saccular hair cells reduced the number of docked SVs per synapse from 43 to 32 (11).…”

Section: Discussionmentioning

confidence: 99%

Frequency selectivity of synaptic exocytosis in frog saccular hair cells

Rutherford

Roberts

2006

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

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The ability to respond selectively to particular frequency components of sensory inputs is fundamental to signal processing in the ear. The frog (Rana pipiens) sacculus, which is used for social communication and escape behaviors, is an exquisitely sensitive detector of sounds and ground-borne vibrations in the 5-to 200-Hz range, with most afferent axons having best frequencies between 40 and 60 Hz. We monitored the synaptic output of saccular sensory receptors (hair cells) by measuring the increase in membrane capacitance (⌬Cm) that occurs when synaptic vesicles fuse with the plasmalemma. Strong stepwise depolarization evoked an exocytic burst that lasted 10 ms and corresponded to the predicted capacitance of all docked vesicles at synapses, followed by a 20-ms delay before additional vesicle fusion. Experiments using weak stimuli, within the normal physiological range for these cells, revealed a sensitivity to the temporal pattern of membrane potential changes. Interrupting a weak depolarization with a properly timed hyperpolarization increased ⌬Cm. Small sinusoidal voltage oscillations (؎5 mV centered at ؊60 mV) evoked a ⌬Cm that corresponded to 95 vesicles per s at each synapse at 50 Hz but only 26 vesicles per s at 5 Hz and 27 vesicles per s at 200 Hz (perforated patch recordings). This frequency selectivity was absent for larger sinusoidal oscillations (؎10 mV centered at ؊55 mV) and was largest for hair cells with the smallest sinusoidal-stimulievoked Ca 2؉ currents. We conclude that frog saccular hair cells possess an intrinsic synaptic frequency selectivity that is saturated by strong stimuli.afferent ͉ synaptic vesicle pool ͉ ribbon synapse ͉ capacitance ͉ tuning T he auditory and vestibular systems in the ear and the related mechanosensory and electrosensory organs of the lateral line employ a remarkable variety of mechanical and neural mechanisms to distinguish frequency components of sensory signals from Ͻ10 Hz to nearly 100 kHz (1, 2). In each of these organs, a sensory stimulus passes through one or more stages of mechanical or electrical filtering (3), leading to graded changes in the sensory receptor cell's membrane potential, V m . Oscillatory sensory stimuli usually produce oscillations in V m , with the greatest amplitude occurring at a preferred frequency. Hair cells in the frog sacculus possess a broadly tuned electrical filter that causes V m to oscillate preferentially at frequencies between 35 and 75 Hz (4), as well as spontaneous oscillations of the mechanosensory apparatus at frequencies between 5 and 50 Hz (5).At the hair cells' output synapses, the information contained in V m is transmitted by a chemical neurotransmitter (glutamate) to postsynaptic terminals and encoded as a train of action potentials that travel to the brain. Each of these afferent synapses contains a presynaptic dense body [also known as the synaptic body (SB) or synaptic ribbon] (Fig. 1a) similar to ribbon synapses in the retina. As at other chemical synapses, V m controls calcium influx through voltage-gated cal...

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Section: Discussionmentioning

confidence: 99%

Frequency selectivity of synaptic exocytosis in frog saccular hair cells

Rutherford

Roberts

2006

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

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“…2D). Compound vesicles have been observed in non-neuronal secretory cells (e.g., Alvarez de Toledo and Fernandez, 1990) and could potentially underlie the multivesicular release reported in bipolar cells (Singer et al, 2004) and cochlear hair cells (Glowatzki and Fuchs, 2002;Edmonds et al, 2004). On the other hand, it is difficult to reconcile the fusion of compound vesicles with the rise in membrane capacitance evoked by the rapid, global elevation of calcium, which is best described by a smooth, single exponential function indicative of the fusion of a small, homogeneous class of vesicle (Heidelberger et al, 1994).…”

Section: Fusion Scenarios and Ribbon Functionmentioning

confidence: 99%

“…As with the Mb 1 bipolar cell, the intensity of the stimulus determines the relative ratios between the transient and sustained components. These two components share similar sensitivities to exogenous calcium buffers and may represent the fusion of vesicles located near calcium channels (Singer et al, 2004). Thus, there could potentially be release during the plateau phase, depending upon stimulation intensity.…”

Section: Relation Of Synaptic Release To the Underlying Light-evoked mentioning

confidence: 99%

Synaptic transmission at retinal ribbon synapses

Heidelberger

Thoreson

Witkovsky

2005

Progress in Retinal and Eye Research

209

231

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The molecular organization of ribbon synapses in photoreceptors and ON bipolar cells is reviewed in relation to the process of neurotransmitter release. The interactions between ribbon synapseassociated proteins, synaptic vesicle fusion machinery and the voltage-gated calcium channels that gate transmitter release at ribbon synapses are discussed in relation to the process of synaptic vesicle exocytosis. We describe structural and mechanistic specializations that permit the ON bipolar cell to release transmitter at a much higher rate than the photoreceptor does, under in vivo conditions. We also consider the modulation of exocytosis at photoreceptor synapses, with an emphasis on the regulation of calcium channels.

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“…At the EM level, the presynaptic elements are classical ribbon synapses (Kolb 1979;Sterling et al, 1988;Strettoi et al, 1990Strettoi et al, , 1992. The synaptic input is mediated by iGluRs of the AMPA-type (GluARs) (Singer and Diamond, 2003;Singer et al, 2004;Veruki et al, 2003 and immunocytochemical studies have identified the presence of GluA2/3 and GluA4 AMPA receptor subunits postsynaptically (Ghosh et al, 2001;Li et al, 2002). A recent study suggests that AII amacrines may also receive input at the arboreal dendrites from ribbon synapses of one type of ON-cone bipolar cell (Anderson et al, 2011).…”

Section: The Aii Amacrine Cell In the Mammalian Retinamentioning

confidence: 99%

Electrical synapses between AII amacrine cells in the retina: Function and modulation

Hartveit

Veruki

2012

Brain Research

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Adaptation enables the visual system to operate across a large range of background light intensities. There is evidence that one component of this adaptation is mediated by modulation of gap junctions functioning as electrical synapses, thereby tuning and functionally optimizing specific retinal microcircuits and pathways. The AII amacrine cell is an interneuron found in most mammalian retinas and plays a crucial role for processing visual signals in starlight, twilight and daylight. AII amacrine cells are connected to each other by gap junctions, potentially serving as a substrate for signal averaging and noise reduction, and there is evidence that the strength of electrical coupling is modulated by the level of background light. Whereas there is extensive knowledge concerning the retinal microcircuits that involve the AII amacrine cell, it is less clear which signaling pathways and intracellular transduction mechanisms are involved in modulating the junctional conductance between electrically coupled AII amacrine cells. Here we review the current state of knowledge, with a focus on recent evidence that suggests that the modulatory control involves activity-dependent changes in the phosphorylation of the gap junction channels between AII amacrine cells, potentially linked to their intracellular Ca 2+ dynamics.

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Coordinated multivesicular release at a mammalian ribbon synapse

Cited by 208 publications

References 46 publications

Frequency selectivity of synaptic exocytosis in frog saccular hair cells

Frequency selectivity of synaptic exocytosis in frog saccular hair cells

Synaptic transmission at retinal ribbon synapses

Electrical synapses between AII amacrine cells in the retina: Function and modulation

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