Central Vestibular Tuning Arises from Patterned Convergence of Otolith Afferents
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Abstract
As sensory information moves through the brain, higher-order areas exhibit more complex tuning than lower areas. Though models predict that complexity arises via convergent inputs from neurons with diverse response properties, in most vertebrate systems, convergence has only been inferred rather than tested directly. Here, we measure sensory computations in zebrafish vestibular neurons across multiple axes in vivo. We establish that whole-cell physiological recordings reveal tuning of individual vestibular afferent inputs and their postsynaptic targets. Strong, sparse synaptic inputs can be distinguished by their amplitudes, permitting analysis of afferent convergence in vivo. An independent approach, serial-section electron microscopy, supports the inferred connectivity. We find that afferents with similar or differing preferred directions converge on central vestibular neurons, conferring more simple or complex tuning, respectively. Together, these results provide a direct, quantifiable demonstration of feedforward input convergence in vivo.
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- Authors
- Liu, Z., Kimura, Y., Higashijima, S.-I., Hildebrand, D. G. C., Morgan, J. L., & Bagnall, M. W.
- Affiliations
- Washington University in St. Louis (US)
- National Institute for Basic Biology (JP)
- Rockefeller University (US)
- Corresponding author
- Bagnall, Martha W.
- ORCID
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2020-11
- Volume
- 108
- Issue
- 4
- Pages
- 748-762.e4
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC7704800
- OpenAlex
- W3086057402
- Cited by
- 50
- References
- 84
- Citations by year
- 2026: 6 · 2025: 11 · 2024: 12 · 2023: 6 · 2022: 10 · 2021: 5
- FWCI
- 2.02
- Type
- journal article
- Language
- en
- Update notices
- erratum (2021-03-03)
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Eye Institute
- National Institute on Deafness and Other Communication Disorders
- Topics
- Life Sciences › Neuroscience › Neurology › Vestibular and auditory disorders
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Keywords
- afferent convergence, otolith afferents, preferred direction, serial section electron microscopy, whole-cell recording, sensory processing
- MeSH terms
- Animals, Electric Stimulation, Evoked Potentials, Somatosensory, Microscopy, Electron, Neurons, Neurons, Afferent, Otolithic Membrane, Vestibular Nuclei, Zebrafish, Gene Knock-In Techniques
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