The diverse roles of ribbon synapses in sensory neurotransmission

Matthews, Gary; Fuchs, Paul

doi:10.1038/nrn2924

Cited by 334Neuroscience and Neuropharmacology ResearchCellular transport and secretionExtracellular vesicles in disease

The diverse roles of ribbon synapses in sensory neurotransmission

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Matthews, Gary, Fuchs, Paul·2010·Nature Reviews Neuroscience

DOI 10.1038/nrn2924PMC PMC3065184

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Abstract

Sensory synapses of the visual and auditory systems must faithfully encode a wide dynamic range of graded signals, and must be capable of sustained transmitter release over long periods of time. Functionally and morphologically, these sensory synapses are unique: their active zones are specialized in several ways for sustained, rapid vesicle exocytosis, but their most striking feature is an organelle called the synaptic ribbon, which is a proteinaceous structure that extends into the cytoplasm at the active zone and tethers a large pool of releasable vesicles. But precisely how does the ribbon function to support tonic release at these synapses? Recent genetic and biophysical advances have begun to open the 'black box' of the synaptic ribbon with some surprising findings and promise to resolve its function in vision and hearing.

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Ribbon synapses contain their characteristic synaptic ribbons in addition to standard active zones.
“Ribbon synapses contain their characteristic synaptic ribbons in addition to standard active zones, and the ribbons appear to function as accelerators in the recruitment of vesicles for exocytosis (Matthews and Fuchs, 2010).”
From The Presynaptic Active Zone (2012) · cites this paper as Matthews and Fuchs, 2010
The Abstract and Introduction describe synaptic ribbons as structures at the active zones of ribbon synapses. They do not say that ribbon synapses also contain separate, standard active zones; the Abstract instead describes their active zones as specialized. Page numbers were not provided in our copy. (LLM, conf=0.85)
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Synaptic ribbons appear to function as accelerators in the recruitment of vesicles for exocytosis.
“Ribbon synapses contain their characteristic synaptic ribbons in addition to standard active zones, and the ribbons appear to function as accelerators in the recruitment of vesicles for exocytosis (Matthews and Fuchs, 2010).”
From The Presynaptic Active Zone (2012) · cites this paper as Matthews and Fuchs, 2010

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Probing the Mechanism of Exocytosis at the Hair Cell Ribbon Synapse
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Diurnal Changes in Exocytosis and the Number of Synaptic Ribbons at Active Zones of an on -Type Bipolar Cell Terminal
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Vesicle association and exocytosis at ribbon and extraribbon sites in retinal bipolar cell presynaptic terminals
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Synaptic Ribbon Enables Temporal Precision of Hair Cell Afferent Synapse by Increasing the Number of Readily Releasable Vesicles: A Modeling Study
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Calcium- and Calmodulin-Dependent Inactivation of Calcium Channels in Inner Hair Cells of the Rat Cochlea
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Self-citation
Functional maturation of the exocytotic machinery at gerbil hair cell ribbon synapses
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Mobility and Turnover of Vesicles at the Synaptic Ribbon
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Self-citation
Syntaxin 3b is a t‐SNARE specific for ribbon synapses of the retina
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A theoretical study of calcium microdomains in turtle hair cells
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Vesicle Pool Size at the Salamander Cone Ribbon Synapse
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Miniature excitatory postsynaptic currents in bipolar cells of the tiger salamander retina
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Temperature enhances exocytosis efficiency at the mouse inner hair cell ribbon synapse
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Role of L-Type Ca2+Channels in Transmitter Release From Mammalian Inner Hair Cells I. Gross Sound-Evoked Potentials
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Syntaxin 3B is essential for the exocytosis of synaptic vesicles in ribbon synapses of the retina
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Active zone protein CAST is a component of conventional and ribbon synapses in mouse retina
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Vesicle recycling at ribbon synapses in the finely branched axon terminals of mouse retinal bipolar neurons
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Self-citation
Conical Electron Tomography of a Chemical Synapse: Polyhedral Cages Dock Vesicles to the Active Zone
Zampighi, G. A., Fain, N., Zampighi, L. M., Cantele, F., Lanzavecchia, S., & Wright, E. M. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.4639-07.2008 · Cited by 42 · see citing works
Mechanisms Contributing to Tonic Release at the Cone Photoreceptor Ribbon Synapse
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Quantitative Analysis of Synaptic Release at the Photoreceptor Synapse
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Glutamate release by the intact light-responsive photoreceptor layer of the Xenopus retina
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Nicotinamide Adenine Dinucleotide-Dependent Binding of the Neuronal Ca2+Sensor Protein GCAP2 to Photoreceptor Synaptic Ribbons
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Characterisation of bipolar cell synaptic transmission in goldfish retina using paired recordings
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Self-citation
The Neural Basis of Early Vision
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The Presynaptic Active Zone
Südhof, T. C. (2012) · Neuron · doi:10.1016/j.neuron.2012.06.012 · Cited by 1,062 · see citing works
Principles of Neural Design
Sterling, P., & Laughlin, S. (2015) · doi:10.7551/mitpress/9780262028707.001.0001 · Cited by 482 · see citing works
Hair Cell Transduction, Tuning, and Synaptic Transmission in the Mammalian Cochlea
Fettiplace, R. (2017) · Comprehensive physiology · doi:10.1002/cphy.c160049 · Cited by 376 · see citing works
Auditory neuropathy — neural and synaptic mechanisms
Moser, T., & Starr, A. (2016) · Nature Reviews Neurology · doi:10.1038/nrneurol.2016.10 · Cited by 364 · see citing works
Presynaptic calcium channels: specialized control of synaptic neurotransmitter release
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Sensory Processing at Ribbon Synapses in the Retina and the Cochlea
Moser, T., Grabner, C. P., & Schmitz, F. (2019) · Physiological Reviews · doi:10.1152/physrev.00026.2018 · Cited by 206 · see citing works
The Auditory Hair Cell Ribbon Synapse: From Assembly to Function
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Developmental refinement of hair cell synapses tightens the coupling of Ca2+ influx to exocytosis
Wong, A. B., Rutherford, M. A., Gabrielaitis, M., Pangršič, T., Göttfert, F., Frank, T., Michanski, S., Hell, S. W., Wolf, F., Wichmann, C., et al. (2014) · The EMBO Journal · doi:10.1002/embj.201387110 · Cited by 169 · see citing works
Disruption of the Presynaptic Cytomatrix Protein Bassoon Degrades Ribbon Anchorage, Multiquantal Release, and Sound Encoding at the Hair Cell Afferent Synapse
Jing, Z., Rutherford, M. A., Takago, H., Frank, T., Fejtová, A., Khimich, D., Moser, T., & Strenzke, N. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.3491-12.2013 · Cited by 167 · see citing works
Beyond plasticity: the dynamic impact of electrical synapses on neural circuits
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The Reduced Cochlear Output and the Failure to Adapt the Central Auditory Response Causes Tinnitus in Noise Exposed Rats
Rüttiger, L., Singer, W., Panford-Walsh, R., Matsumoto, M., Lee, S. C., Zuccotti, A., Zimmermann, U., Jaumann, M., Rohbock, K., Xiong, H., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0057247 · Cited by 155 · see citing works
How to make a synaptic ribbon: RIBEYE deletion abolishes ribbons in retinal synapses and disrupts neurotransmitter release
Maxeiner, S., Luo, F., Tan, A., Schmitz, F., & Südhof, T. C. (2016) · The EMBO Journal · doi:10.15252/embj.201592701 · Cited by 153 · see citing works
A new probe for super-resolution imaging of membranes elucidates trafficking pathways
Revelo, N. H., Kamin, D., Truckenbrodt, S., Wong, A. B., Reuter‐Jessen, K., Reisinger, E., Moser, T., & Rizzoli, S. O. (2014) · The Journal of Cell Biology · doi:10.1083/jcb.201402066 · Cited by 150 · see citing works
Developmental Profiling of Spiral Ganglion Neurons Reveals Insights into Auditory Circuit Assembly
Lu, C. C., Appler, J. M., Houseman, E. A., & Goodrich, L. V. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.2358-11.2011 · Cited by 142 · see citing works
A Mutation in CABP2 , Expressed in Cochlear Hair Cells, Causes Autosomal-Recessive Hearing Impairment
Schrauwen, I., Helfmann, S., Inagaki, A., Predoehl, F., Tabatabaiefar, M. A., Picher, M. M., Sommen, M., Seco, C. Z., Oostrik, J., Kremer, H., et al. (2012) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2012.08.018 · Cited by 135 · see citing works
A Synaptic Mechanism for Retinal Adaptation to Luminance and Contrast
Jarsky, T., Cembrowski, M. S., Logan, S. M., Kath, W. L., Riecke, H., Demb, J. B., & Singer, J. H. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.2631-11.2011 · Cited by 135 · see citing works
Cochlear hair cells: The sound‐sensing machines
Goutman, J. D., Elgoyhen, A. B., & Gómez‐Casati, M. E. (2015) · FEBS Letters · doi:10.1016/j.febslet.2015.08.030 · Cited by 127 · see citing works
Relating structure and function of inner hair cell ribbon synapses
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The SNARE complex in neuronal and sensory cells
Ramakrishnan, N. A., Drescher, M. J., & Drescher, D. G. (2012) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2012.03.009 · Cited by 123 · see citing works
Tonic signaling from O2 sensors sets neural circuit activity and behavioral state
Busch, K. E., Laurent, P., Soltész, Z., Murphy, R. J., Faivre, O., Hedwig, B., Thomas, M. V., Smith, H., & de Bono, M. (2012) · Nature Neuroscience · doi:10.1038/nn.3061 · Cited by 118 · see citing works
Synaptic Vesicle Clusters at Synapses: A Distinct Liquid Phase?
Milovanović, D., & Camilli, P. V. D. (2017) · Neuron · doi:10.1016/j.neuron.2017.02.013 · Cited by 117 · see citing works
miR-96 regulates the progression of differentiation in mammalian cochlear inner and outer hair cells
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Basic response properties of auditory nerve fibers: a review
Heil, P. F., & Peterson, A. J. (2015) · Cell and Tissue Research · doi:10.1007/s00441-015-2177-9 · Cited by 108 · see citing works
Disruption of adaptor protein 2μ (AP‐2μ) in cochlear hair cells impairs vesicle reloading of synaptic release sites and hearing
Jung, S., Maritzen, T., Wichmann, C., Jing, Z., Neef, A., Revelo, N. H., Al‐Moyed, H., Meese, S., Wojcik, S. M., Panou, I., et al. (2015) · The EMBO Journal · doi:10.15252/embj.201591885 · Cited by 107 · see citing works
Retinal Microvasculature and Visual Acuity in Eyes With Branch Retinal Vein Occlusion: Imaging Analysis by Optical Coherence Tomography Angiography
Wakabayashi, T., Sato, T., Hara-Ueno, C., Fukushima, Y., Sayanagi, K., Shiraki, N., Sawa, M., Ikuno, Y., Sakaguchi, H., & Nishida, K. (2017) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.16-21208 · Cited by 102 · see citing works
The presynaptic ribbon maintains vesicle populations at the hair cell afferent fiber synapse
Becker, L., Schnee, M. E., Niwa, M., Sun, W. W., Maxeiner, S., Talaei, S., Kachar, B., Rutherford, M. A., & Ricci, A. J. (2018) · eLife · doi:10.7554/elife.30241 · Cited by 97 · see citing works
Deletion of the Presynaptic Scaffold CAST Reduces Active Zone Size in Rod Photoreceptors and Impairs Visual Processing
Dieck, S. T., Specht, D., Strenzke, N., Hida, Y., Krishnamoorthy, V., Schmidt, K.-F., Inoue, E., Ishizaki, H., Tanaka, M., Miyoshi, J., et al. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.0752-12.2012 · Cited by 94 · see citing works
Molecular Remodeling of the Presynaptic Active Zone of Drosophila Photoreceptors via Activity-Dependent Feedback
Sugie, A., Hakeda‐Suzuki, S., Suzuki, E., Silies, M., Shimozono, M., Möhl, C., Suzuki, T., & Tavosanis, G. (2015) · Neuron · doi:10.1016/j.neuron.2015.03.046 · Cited by 89 · see citing works
Ephrin-A5/EphA4 signalling controls specific afferent targeting to cochlear hair cells
Defourny, J., Poirrier, A., Lallemend, F., Sánchez, S. M., Neef, J., Vanderhaeghen, P., Soriano, E., Peuckert, C., Kullander, K., Fritzsch, B., et al. (2013) · Nature Communications · doi:10.1038/ncomms2445 · Cited by 86 · see citing works
Retinal Glutamate Neurotransmission: From Physiology to Pathophysiological Mechanisms of Retinal Ganglion Cell Degeneration
Boccuni, I., & Fairless, R. (2022) · Life · doi:10.3390/life12050638 · Cited by 85 · see citing works
Sustaining rapid vesicular release at active zones: potential roles for vesicle tethering
Hallermann, S., & Silver, R. A. (2012) · Trends in Neurosciences · doi:10.1016/j.tins.2012.10.001 · Cited by 83 · see citing works
Identification and Immunocytochemical Characterization of Piccolino, a Novel Piccolo Splice Variant Selectively Expressed at Sensory Ribbon Synapses of the Eye and Ear
Regus‐Leidig, H., Ott, C., Löhner, M., Atorf, J., Fuchs, M., Sedmak, T., Kremers, J., Fejtová, A., Gundelfinger, E. D., & Brandstätter, J. H. (2013) · PLoS ONE · doi:10.1371/journal.pone.0070373 · Cited by 82 · see citing works
Synaptic Ribbons Influence the Size and Frequency of Miniature-like Evoked Postsynaptic Currents
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Lack of Brain-Derived Neurotrophic Factor Hampers Inner Hair Cell Synapse Physiology, But Protects against Noise-Induced Hearing Loss
Zuccotti, A., Kuhn, S. A. C., Johnson, S. L., Franz, C., Singer, W., Hecker, D., Geisler, H.-S., Köpschall, I., Rohbock, K., Gutsche, K., et al. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.1247-12.2012 · Cited by 82 · see citing works
Presynaptic maturation in auditory hair cells requires a critical period of sensory-independent spiking activity
Johnson, S. L., Kuhn, S. A. C., Franz, C., Ingham, N. J., Furness, D. N., Knipper, M., Steel, K. P., Adelman, J. P., Holley, M. C., & Marcotti, W. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1219578110 · Cited by 80 · see citing works
Is the din really harmless? Long-term effects of non-traumatic noise on the adult auditory system
Gourévitch, B., Edeline, J., Occelli, F., & Eggermont, J. J. (2014) · Nature reviews. Neuroscience · doi:10.1038/nrn3744 · Cited by 79 · see citing works
NGL-2 Regulates Pathway-Specific Neurite Growth and Lamination, Synapse Formation, and Signal Transmission in the Retina
Soto, F., Watkins, K. L., Johnson, R. E., Schottler, F., & Kerschensteiner, D. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.1521-13.2013 · Cited by 75 · see citing works
d-Galactose-induced oxidative stress and mitochondrial dysfunction in the cochlear basilar membrane: an in vitro aging model
Guo, B., Guo, Q., Wang, Z., Shao, J., Liu, K., Du, Z., & Gong, S.-S. (2020) · Biogerontology · doi:10.1007/s10522-020-09859-x · Cited by 74 · see citing works
Voltage- and calcium-gated ion channels of neurons in the vertebrate retina
Hook, M. J. V., Nawy, S., & Thoreson, W. B. (2019) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2019.05.001 · Cited by 74 · see citing works
Ribbon Synapses and Visual Processing in the Retina
Lagnado, L., & Schmitz, F. (2015) · Annual Review of Vision Science · doi:10.1146/annurev-vision-082114-035709 · Cited by 73 · see citing works
Molecular tuning of electroreception in sharks and skates
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Synaptic mitochondria regulate hair-cell synapse size and function
Wong, H.-T., Zhang, Q.-X., Beirl, A. J., Petralia, R. S., Wang, Y., & Kindt, K. S. (2019) · eLife · doi:10.7554/elife.48914 · Cited by 72 · see citing works
Synaptic Ribbons Require Ribeye for Electron Density, Proper Synaptic Localization, and Recruitment of Calcium Channels
Lv, C., Stewart, W. J., Akanyeti, O., Frederick, C., Zhu, J., Santos‐Sacchi, J., Sheets, L., Liao, J. C., & Zenisek, D. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.05.045 · Cited by 71 · see citing works
Neural Circuit Development in the Mammalian Cochlea
Bulankina, A. V., & Moser, T. (2012) · Physiology · doi:10.1152/physiol.00036.2011 · Cited by 70 · see citing works
Phase-Locking Precision Is Enhanced by Multiquantal Release at an Auditory Hair Cell Ribbon Synapse
Li, G., Cho, S., & von Gersdorff, H. (2014) · Neuron · doi:10.1016/j.neuron.2014.08.027 · Cited by 69 · see citing works
Cochlear NMDA Receptors as a Therapeutic Target of Noise-Induced Tinnitus
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Insights into electrosensory organ development, physiology and evolution from a lateral line-enriched transcriptome
Modrell, M. S., Lyne, M., Carr, A. R., Zakon, H. H., Buckley, D., Campbell, A. S., Davis, M. C., Micklem, G., & Baker, C. V. H. (2017) · eLife · doi:10.7554/elife.24197 · Cited by 67 · see citing works
Characterization of Cav1.4 Complexes (α11.4, β2, and α2δ4) in HEK293T Cells and in the Retina
Lee, A., Wang, S., Williams, B., Hagen, J., Scheetz, T. E., & Haeseleer, F. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.607465 · Cited by 66 · see citing works
Properties of Ribbon and Non-Ribbon Release from Rod Photoreceptors Revealed by Visualizing Individual Synaptic Vesicles
Chen, M., Hook, M. J. V., Zenisek, D., & Thoreson, W. B. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.3426-12.2013 · Cited by 66 · see citing works
Structure and function of a complex sensory synapse
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Spikes and ribbon synapses in early vision
Baden, T., Euler, T., Weckström, M., & Lagnado, L. (2013) · Trends in Neurosciences · doi:10.1016/j.tins.2013.04.006 · Cited by 63 · see citing works
Munc13-Independent Vesicle Priming at Mouse Photoreceptor Ribbon Synapses
Cooper, B. H., Hemmerlein, M., Ammermüller, J., Imig, C., Reim, K., Lipstein, N., Kalla, S., Kawabe, H., Brose, N., Brandstätter, J. H., et al. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.4240-11.2012 · Cited by 63 · see citing works
Cholinergic efferent synaptic transmission regulates the maturation of auditory hair cell ribbon synapses
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Nonlinear spatial encoding by retinal ganglion cells: when 1 + 1 ≠ 2
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Synaptojanin 1 Mutation in Parkinson’s Disease Brings Further Insight into the Neuropathological Mechanisms
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Nanoscale dynamics of synaptic vesicle trafficking and fusion at the presynaptic active zone
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Self-citation
The microtubule cytoskeleton at the synapse
Parato, J., & Bartolini, F. (2021) · Neuroscience Letters · doi:10.1016/j.neulet.2021.135850 · Cited by 60 · see citing works
The Coupling between Ca2+Channels and the Exocytotic Ca2+Sensor at Hair Cell Ribbon Synapses Varies Tonotopically along the Mature Cochlea
Johnson, S. L., Olt, J., Cho, S., von Gersdorff, H., & Marcotti, W. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.2867-16.2017 · Cited by 60 · see citing works
Enlargement of Ribbons in Zebrafish Hair Cells Increases Calcium Currents But Disrupts Afferent Spontaneous Activity and Timing of Stimulus Onset
Sheets, L., He, X. J., Olt, J., Schreck, M. R., Petralia, R. S., Wang, Y., Zhang, Q.-X., Beirl, A. J., Nicolson, T. A., Marcotti, W., et al. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.2878-16.2017 · Cited by 60 · see citing works
In vivo knockdown of Piccolino disrupts presynaptic ribbon morphology in mouse photoreceptor synapses
Regus‐Leidig, H., Fuchs, M., Löhner, M., Leist, S. R., Leal‐Ortiz, S., Chiodo, V. A., Hauswirth, W. W., Garner, C. C., & Brandstätter, J. H. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00259 · Cited by 59 · see citing works
Diversity matters — extending sound intensity coding by inner hair cells via heterogeneous synapses
Moser, T., Karagulyan, N., Neef, J., & Tobón, L. M. J. (2023) · The EMBO Journal · doi:10.15252/embj.2023114587 · Cited by 58 · see citing works
An amplitude code transmits information at a visual synapse
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Authors: Matthews, G., & Fuchs, P.
Affiliations: Stony Brook University (US)
Johns Hopkins University (US)
Corresponding author: Matthews, Gary
Fuchs, Paul
ORCID: Matthews, Gary
Fuchs, Paul
Venue: Nature Reviews Neuroscience
Publisher: Springer Science and Business Media LLC
Published: 2010-11-03
Volume: 11
Issue: 12
Pages: 812-822
ISSN: 1471-003X (ISSN-L)
1471-0048
DOI: 10.1038/nrn2924
PMC: PMC3065184
OpenAlex: W2070074690
Cited by: 334
References: 116
Citations by year: 2026: 16 · 2025: 17 · 2024: 18 · 2023: 11 · 2022: 28 · 2021: 24 · 2020: 25 · 2019: 24 · 2018: 19 · 2017: 24 · 2016: 16 · 2015: 24 · 2014: 23 · 2013: 25 · 2012: 25
FWCI: 1.88
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Nature reviews. Neuroscience (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health
National Eye Institute (R01EY003821)
National Institute on Deafness and Other Communication Disorders (P30DC005211, R01DC000276, R01DC001508)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
Keywords: ribbon synapses, auditory synapses, synaptic ribbons, active zone, vesicle exocytosis, graded signaling, dynamic range, sustained drug release
MeSH terms: Animals, Models, Biological, Synaptic Transmission, Sensory Receptor Cells, Sensation, Synapses, Calcium Channels, L-Type

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