A Structural and Genotypic Scaffold Underlying Temporal Integration
Open accessAbstract
The accumulation and storage of information over time, temporal integration, is key to numerous behaviors. Many oculomotor tasks depend on integration of eye-velocity signals to eye-position commands, a transformation achieved by a hindbrain cell group termed the velocity-to-position neural integrator (VPNI). Although the VPNI's coding properties have been well characterized, its mechanism of function remains poorly understood because few links exist between neuronal activity, structure, and genotypic identity. To fill this gap, we used calcium imaging and single-cell electroporation during oculomotor behaviors to map VPNI neural activity in zebrafish onto a hindbrain scaffold consisting of alternating excitatory and inhibitory parasagittal stripes. Three distinct classes of VPNI cells were identified. One glutamatergic class was medially located along a stripe associated with the alx transcription factor; these cells had ipsilateral projections terminating near abducens motoneurons and collateralized extensively within the ipsilateral VPNI in a manner consistent with integration through recurrent excitation. A second glutamatergic class was more laterally located along a stripe associated with transcription factor dbx1b; these glutamatergic cells had contralateral projections collateralizing near abducens motoneurons, consistent with a role in disconjugate eye movements. A third class, immunohistochemically suggested to be GABAergic, was located primarily in the dbx1b stripe and also had contralateral projections terminating near abducens motoneurons; these cells collateralized extensively in the dendritic field of contralateral VPNI neurons, consistent with a role in coordinating activity between functionally opposing populations. This mapping between VPNI activity, structure, and genotype may provide a blueprint for understanding the mechanisms governing temporal integration.
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The imaged volume includes neurons involved in eye movements.
“The imaged volume includes neurons involved in eye movements16,21,22,28.”
From Predicting modular functions and neural coding of behavior from a synaptic wiring diagram (2024) · cites this paper as [21]
Within the oculomotor integrator, broad physiological and coarse anatomical evidence implicates recurrent excitatory interactions in generating attractor dynamics.
“Within the oculomotor integrator, there is broad physiological18–20 and coarse anatomical21 evidence implicating recurrent excitatory interactions in generating attractor dynamics.”
From Predicting modular functions and neural coding of behavior from a synaptic wiring diagram (2024) · cites this paper as [21]
In R7/R8, the former VPNI cells have somata primarily within a medial glutamatergic parasagittal stripe associated with the Alx transcription factor, and the latter with a more lateral GABAergic parasagittal stripe associated with the Abx1b transcription factor.
“In R7/R8, the former were found to have somata primarily within a medial glutamatergic parasagittal stripe associated with the Alx transcription factor and the latter with a more lateral GABAergic parasagittal stripe associated with the Abx1b transcription factor21,95,96.”
From Predicting modular functions and neural coding of behavior from a synaptic wiring diagram (2024) · cites this paper as [21]
Prior work has identified two major classes of VPNI cells: those with ipsilateral recurrent excitatory projections and those with inhibitory contralateral projections.
“Prior work has identified two major classes of VPNI cells, those with ipsilateral recurrent excitatory projections and those with inhibitory contralateral projections21,49.”
From Predicting modular functions and neural coding of behavior from a synaptic wiring diagram (2024) · cites this paper as [21]
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- Authors
- Lee, M. M., Arrenberg, A. B., & Aksay, E. R. F.
- Affiliations
- Weill Cornell Medicine (US)
- University of Freiburg (DE)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2015-05-20
- Volume
- 35
- Issue
- 20
- Pages
- 7903-7920
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC4438132
- OpenAlex
- W1870345950
- Cited by
- 27
- References
- 62
- Citations by year
- 2026: 1 · 2025: 2 · 2024: 2 · 2023: 2 · 2022: 1 · 2021: 2 · 2020: 1 · 2019: 6 · 2018: 2 · 2017: 5 · 2016: 3
- FWCI
- 2.00
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Science Foundation (1208088)
- Simons Foundation
- Deutsche Forschungsgemeinschaft (EXC307, (EXC 294))
- National Institutes of Health
- National Eye Institute (R01EY021581)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Neurology › Vestibular and auditory disorders
- Keywords
- temporal integration, oculomotor control, hindbrain, glutamatergic neurons, GABAergic neurons, abducens motoneurons, recurrent excitation, disconjugate eye movements, zebrafish, single-cell electroporation, calcium imaging
- MeSH terms
- Animals, Eye Movements, Eye Proteins, Female, Genotype, Male, Motor Neurons, Rhombencephalon, Transcription Factors, Zebrafish, Homeodomain Proteins, Zebrafish Proteins, GABAergic Neurons
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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