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Brain-wide neuronal dynamics during motor adaptation in zebrafish

Author

Listed:
  • Misha B. Ahrens

    (Harvard University, 16 Divinity Avenue, Cambridge, Massachusetts 02138, USA
    Computational and Biological Learning Laboratory, Cambridge University, Trumpington Street, Cambridge CB2 1PZ, UK)

  • Jennifer M. Li

    (Harvard University, 16 Divinity Avenue, Cambridge, Massachusetts 02138, USA)

  • Michael B. Orger

    (Champalimaud Neuroscience Programme, Champalimaud Centre for the Unknown, Avenida Brasília, Doca de Pedrouços, 1400-038 Lisboa, Portugal)

  • Drew N. Robson

    (Harvard University, 16 Divinity Avenue, Cambridge, Massachusetts 02138, USA)

  • Alexander F. Schier

    (Harvard University, 16 Divinity Avenue, Cambridge, Massachusetts 02138, USA)

  • Florian Engert

    (Harvard University, 16 Divinity Avenue, Cambridge, Massachusetts 02138, USA)

  • Ruben Portugues

    (Harvard University, 16 Divinity Avenue, Cambridge, Massachusetts 02138, USA)

Abstract

A fundamental question in neuroscience is how entire neural circuits generate behaviour and adapt it to changes in sensory feedback. Here we use two-photon calcium imaging to record the activity of large populations of neurons at the cellular level, throughout the brain of larval zebrafish expressing a genetically encoded calcium sensor, while the paralysed animals interact fictively with a virtual environment and rapidly adapt their motor output to changes in visual feedback. We decompose the network dynamics involved in adaptive locomotion into four types of neuronal response properties, and provide anatomical maps of the corresponding sites. A subset of these signals occurred during behavioural adjustments and are candidates for the functional elements that drive motor learning. Lesions to the inferior olive indicate a specific functional role for olivocerebellar circuitry in adaptive locomotion. This study enables the analysis of brain-wide dynamics at single-cell resolution during behaviour.

Suggested Citation

  • Misha B. Ahrens & Jennifer M. Li & Michael B. Orger & Drew N. Robson & Alexander F. Schier & Florian Engert & Ruben Portugues, 2012. "Brain-wide neuronal dynamics during motor adaptation in zebrafish," Nature, Nature, vol. 485(7399), pages 471-477, May.
    • Handle: RePEc:nat:nature:v:485:y:2012:i:7399:d:10.1038_nature11057
    DOI: 10.1038/nature11057
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    Cited by:

    1. Jeffrey P Nguyen & Ashley N Linder & George S Plummer & Joshua W Shaevitz & Andrew M Leifer, 2017. "Automatically tracking neurons in a moving and deforming brain," PLOS Computational Biology, Public Library of Science, vol. 13(5), pages 1-19, May.
    2. Shivesh Chaudhary & Sihoon Moon & Hang Lu, 2022. "Fast, efficient, and accurate neuro-imaging denoising via supervised deep learning," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    3. Johannes Friedrich & Weijian Yang & Daniel Soudry & Yu Mu & Misha B Ahrens & Rafael Yuste & Darcy S Peterka & Liam Paninski, 2017. "Multi-scale approaches for high-speed imaging and analysis of large neural populations," PLOS Computational Biology, Public Library of Science, vol. 13(8), pages 1-24, August.
    4. Roy Harpaz & Minh Nguyet Nguyen & Armin Bahl & Florian Engert, 2021. "Precise visuomotor transformations underlying collective behavior in larval zebrafish," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    5. Ziyue Wang & Xiang Fei & Xiaotong Liu & Yanjie Wang & Yue Hu & Wanling Peng & Ying-wei Wang & Siyu Zhang & Min Xu, 2022. "REM sleep is associated with distinct global cortical dynamics and controlled by occipital cortex," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    6. Dániel L. Barabási & Gregor F. P. Schuhknecht & Florian Engert, 2024. "Functional neuronal circuits emerge in the absence of developmental activity," Nature Communications, Nature, vol. 15(1), pages 1-14, December.

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