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Cited by 26Vestibular and auditory disordersMotor Control and AdaptationVisual perception and processing mechanisms

Functional architecture underlying binocular coordination of eye position and velocity in the larval zebrafish hindbrain

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Brysch, Christian, Leyden, Claire, Arrenberg, Aristides B.·2019·BMC Biology
DOI 10.1186/s12915-019-0720-yPMC PMC6936144

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Abstract

Background: The oculomotor integrator (OI) in the vertebrate hindbrain transforms eye velocity input into persistent position coding output, which plays a crucial role in retinal image stability. For a mechanistic understanding of the integrator function and eye position control, knowledge about the tuning of the OI and other oculomotor nuclei is needed. Zebrafish are increasingly used to study integrator function and sensorimotor circuits, yet the precise neuronal tuning to motor variables remains uncharacterized. Results: Here, we recorded cellular calcium signals while evoking monocular and binocular optokinetic eye movements at different slow-phase eye velocities. Our analysis reveals the anatomical distributions of motoneurons and internuclear neurons in the nucleus abducens as well as those of oculomotor neurons in caudally adjacent hindbrain volumes. Each neuron is tuned to eye position and/or velocity to variable extents and is only activated after surpassing particular eye position and velocity thresholds. While the abducens (rhombomeres 5/6) mainly codes for eye position, in rhombomeres 7/8, a velocity-to-position coding gradient exists along the rostro-caudal axis, which likely corresponds to the oculomotor structures storing velocity and position, and is in agreement with a feedforward mechanism of persistent activity generation. Position encoding neurons are recruited at eye position thresholds distributed across the behaviourally relevant dynamic range, while velocity-encoding neurons have more centred firing thresholds for velocity. In the abducens, neurons coding exclusively for one eye intermingle with neurons coding for both eyes. Many of these binocular neurons are preferentially active during conjugate eye movements and less active during monocular eye movements. This differential recruitment during monocular versus conjugate tasks represents a functional diversification in the final common motor pathway. Conclusions: We localized and functionally characterized the repertoire of oculomotor neurons in the zebrafish hindbrain. Our findings provide evidence for a mixed but task-specific binocular code and suggest that generation of persistent activity is organized along the rostro-caudal axis in the hindbrain.

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  • Together, these subnetworks could provide for maintenance of conjugate and disconjugate eye movements.

    “Together, these subnetworks could provide for maintenance of conjugate and disconjugate eye movements56–58.”

    From Predicting modular functions and neural coding of behavior from a synaptic wiring diagram (2024) · cites this paper as [57]

  • This extension is consistent with a previous observation that VPNI function was only partially abolished by sizable inactivation of R7/R8 and with previous reports of eye position signals in R4-R6 neurons that are not from ABD neurons.

    “This extension is consistent with a previous observation that VPNI function was only partially abolished by sizable inactivation of R7/R8 (ref. 55) and with previous reports of eye position signals in R4–R6 neurons that are not from ABD neurons50,57.”

    From Predicting modular functions and neural coding of behavior from a synaptic wiring diagram (2024) · cites this paper as [57]

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Authors
Brysch, C., Leyden, C., & Arrenberg, A. B.
Affiliations
University of Tübingen (DE)
Corresponding author
Arrenberg, Aristides B.
ORCID
Arrenberg, Aristides B.
Venue
BMC Biology
Publisher
Springer Science and Business Media LLC
Published
2019-12
Volume
17
Issue
1
Pages
110-110
ISSN
1741-7007 (ISSN-L)
DOI
10.1186/s12915-019-0720-y
PMC
PMC6936144
OpenAlex
W2997235851
Cited by
26
References
83
Citations by year
2026: 5 · 2025: 1 · 2024: 2 · 2023: 4 · 2022: 4 · 2021: 6 · 2020: 2 · 2019: 1 · 2018: 1
FWCI
1.43
Type
journal article
Language
en
Open access
Licence
Locations
  • BMC Biology (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders
  • Deutsche Forschungsgemeinschaft (EXC307, INST 37/967-1 FUGG)
  • Ministerium für Wissenschaft, Forschung und Kunst Baden-Württemberg (Juniorprofessor programme)
Topics
  • Life Sciences › Neuroscience › Neurology › Vestibular and auditory disorders
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
Keywords
binocular coordination, optokinetic eye movements, oculomotor neurons, motor neurons, persistent activity, conjugate eye movements, rhombomeres, zebrafish, calcium imaging
MeSH terms
Animals, Eye Movements, Rhombencephalon, Zebrafish, Vision, Binocular

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