eLife (Jan 2018)
The synaptic ribbon is critical for sound encoding at high rates and with temporal precision
- Philippe Jean,
- David Lopez de la Morena,
- Susann Michanski,
- Lina María Jaime Tobón,
- Rituparna Chakrabarti,
- Maria Magdalena Picher,
- Jakob Neef,
- SangYong Jung,
- Mehmet Gültas,
- Stephan Maxeiner,
- Andreas Neef,
- Carolin Wichmann,
- Nicola Strenzke,
- Chad Grabner,
- Tobias Moser
Affiliations
- Philippe Jean
- ORCiD
- Institute for Auditory Neuroscience and InnerEarLab, University Medical Center Göttingen, Göttingen, Germany; Collaborative Research Center, University of Göttingen, Göttingen, Germany; Göttingen Graduate School for Neurosciences and Molecular Biosciences, University of Göttingen, Göttingen, Germany; InnerEarLab, Department of Otolaryngology, University Medical Center Göttingen, Göttingen, Germany
- David Lopez de la Morena
- ORCiD
- Institute for Auditory Neuroscience and InnerEarLab, University Medical Center Göttingen, Göttingen, Germany; Göttingen Graduate School for Neurosciences and Molecular Biosciences, University of Göttingen, Göttingen, Germany; InnerEarLab, Department of Otolaryngology, University Medical Center Göttingen, Göttingen, Germany
- Susann Michanski
- ORCiD
- Collaborative Research Center, University of Göttingen, Göttingen, Germany; InnerEarLab, Department of Otolaryngology, University Medical Center Göttingen, Göttingen, Germany; Molecular Architecture of Synapses Group, Institute for Auditory Neuroscience, University Medical Center Göttingen, Göttingen, Germany; Institute for Biostructural Imaging of Neurodegeneration, University Medical Center Göttingen, Göttingen, Germany
- Lina María Jaime Tobón
- ORCiD
- Institute for Auditory Neuroscience and InnerEarLab, University Medical Center Göttingen, Göttingen, Germany; Collaborative Research Center, University of Göttingen, Göttingen, Germany; Göttingen Graduate School for Neurosciences and Molecular Biosciences, University of Göttingen, Göttingen, Germany; InnerEarLab, Department of Otolaryngology, University Medical Center Göttingen, Göttingen, Germany; Synaptic Nanophysiology Group, Max Planck Institute for Biophysical Chemistry, Göttingen, Germany; Auditory Neuroscience Group, Max Planck Institute for Experimental Medicine, Göttingen, Germany
- Rituparna Chakrabarti
- Collaborative Research Center, University of Göttingen, Göttingen, Germany; Göttingen Graduate School for Neurosciences and Molecular Biosciences, University of Göttingen, Göttingen, Germany; InnerEarLab, Department of Otolaryngology, University Medical Center Göttingen, Göttingen, Germany; Molecular Architecture of Synapses Group, Institute for Auditory Neuroscience, University Medical Center Göttingen, Göttingen, Germany; Institute for Biostructural Imaging of Neurodegeneration, University Medical Center Göttingen, Göttingen, Germany
- Maria Magdalena Picher
- ORCiD
- Institute for Auditory Neuroscience and InnerEarLab, University Medical Center Göttingen, Göttingen, Germany; Collaborative Research Center, University of Göttingen, Göttingen, Germany; InnerEarLab, Department of Otolaryngology, University Medical Center Göttingen, Göttingen, Germany
- Jakob Neef
- ORCiD
- Institute for Auditory Neuroscience and InnerEarLab, University Medical Center Göttingen, Göttingen, Germany; Collaborative Research Center, University of Göttingen, Göttingen, Germany; InnerEarLab, Department of Otolaryngology, University Medical Center Göttingen, Göttingen, Germany; Synaptic Nanophysiology Group, Max Planck Institute for Biophysical Chemistry, Göttingen, Germany; Auditory Neuroscience Group, Max Planck Institute for Experimental Medicine, Göttingen, Germany
- SangYong Jung
- Institute for Auditory Neuroscience and InnerEarLab, University Medical Center Göttingen, Göttingen, Germany; InnerEarLab, Department of Otolaryngology, University Medical Center Göttingen, Göttingen, Germany; Neuro Modulation and Neuro Circuitry Group, Singapore Bioimaging Consortium (SBIC), Biomedical Sciences Institutes, Singapore, Singapore
- Mehmet Gültas
- Department of Breeding Informatics, Georg-August-University Göttingen, Göttingen, Germany
- Stephan Maxeiner
- Institute for Anatomy and Cell Biology, University of the Saarland, Homburg, Germany
- Andreas Neef
- ORCiD
- Bernstein Group Biophysics of Neural Computation, Max Planck Institute for Dynamics and Self-Organization, Göttingen, Germany
- Carolin Wichmann
- ORCiD
- Collaborative Research Center, University of Göttingen, Göttingen, Germany; InnerEarLab, Department of Otolaryngology, University Medical Center Göttingen, Göttingen, Germany; Molecular Architecture of Synapses Group, Institute for Auditory Neuroscience, University Medical Center Göttingen, Göttingen, Germany; Institute for Biostructural Imaging of Neurodegeneration, University Medical Center Göttingen, Göttingen, Germany
- Nicola Strenzke
- Collaborative Research Center, University of Göttingen, Göttingen, Germany; InnerEarLab, Department of Otolaryngology, University Medical Center Göttingen, Göttingen, Germany; Auditory Systems Physiology Group, Department of Otolaryngology, University Medical Center Göttingen, Göttingen, Germany
- Chad Grabner
- Institute for Auditory Neuroscience and InnerEarLab, University Medical Center Göttingen, Göttingen, Germany; InnerEarLab, Department of Otolaryngology, University Medical Center Göttingen, Göttingen, Germany; Synaptic Nanophysiology Group, Max Planck Institute for Biophysical Chemistry, Göttingen, Germany
- Tobias Moser
- ORCiD
- Institute for Auditory Neuroscience and InnerEarLab, University Medical Center Göttingen, Göttingen, Germany; Collaborative Research Center, University of Göttingen, Göttingen, Germany; InnerEarLab, Department of Otolaryngology, University Medical Center Göttingen, Göttingen, Germany; Synaptic Nanophysiology Group, Max Planck Institute for Biophysical Chemistry, Göttingen, Germany; Auditory Neuroscience Group, Max Planck Institute for Experimental Medicine, Göttingen, Germany; Center for Nanoscale Microscopy and Molecular Physiology of the Brain, University Medical Center Göttingen, Göttingen, Germany
- DOI
- https://doi.org/10.7554/eLife.29275
- Journal volume & issue
-
Vol. 7
Abstract
We studied the role of the synaptic ribbon for sound encoding at the synapses between inner hair cells (IHCs) and spiral ganglion neurons (SGNs) in mice lacking RIBEYE (RBEKO/KO). Electron and immunofluorescence microscopy revealed a lack of synaptic ribbons and an assembly of several small active zones (AZs) at each synaptic contact. Spontaneous and sound-evoked firing rates of SGNs and their compound action potential were reduced, indicating impaired transmission at ribbonless IHC-SGN synapses. The temporal precision of sound encoding was impaired and the recovery of SGN-firing from adaptation indicated slowed synaptic vesicle (SV) replenishment. Activation of Ca2+-channels was shifted to more depolarized potentials and exocytosis was reduced for weak depolarizations. Presynaptic Ca2+-signals showed a broader spread, compatible with the altered Ca2+-channel clustering observed by super-resolution immunofluorescence microscopy. We postulate that RIBEYE disruption is partially compensated by multi-AZ organization. The remaining synaptic deficit indicates ribbon function in SV-replenishment and Ca2+-channel regulation.
Keywords
