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A synaptic corollary discharge signal suppresses midbrain visual processing during saccade-like locomotion

Author

Listed:
  • Mir Ahsan Ali

    (University of Freiburg)

  • Katharina Lischka

    (University of Freiburg)

  • Stephanie J. Preuss

    (Max Planck Institute for Medical Research
    Springer Nature Group)

  • Chintan A. Trivedi

    (Max Planck Institute for Medical Research
    University College London)

  • Johann H. Bollmann

    (University of Freiburg
    Max Planck Institute for Medical Research
    Bernstein Center Freiburg, University of Freiburg)

Abstract

In motor control, the brain not only sends motor commands to the periphery, but also generates concurrent internal signals known as corollary discharge (CD) that influence sensory information processing around the time of movement. CD signals are important for identifying sensory input arising from self-motion and to compensate for it, but the underlying mechanisms remain unclear. Using whole-cell patch clamp recordings from neurons in the zebrafish optic tectum, we discovered an inhibitory synaptic signal, temporally locked to spontaneous and visually driven locomotion. This motor-related inhibition was appropriately timed to counteract visually driven excitatory input arising from the fish’s own motion, and transiently suppressed tectal spiking activity. High-resolution calcium imaging revealed localized motor-related signals in the tectal neuropil and the upstream torus longitudinalis, suggesting that CD enters the tectum via this pathway. Together, our results show how visual processing is suppressed during self-motion by motor-related phasic inhibition. This may help explain perceptual saccadic suppression observed in many species.

Suggested Citation

  • Mir Ahsan Ali & Katharina Lischka & Stephanie J. Preuss & Chintan A. Trivedi & Johann H. Bollmann, 2023. "A synaptic corollary discharge signal suppresses midbrain visual processing during saccade-like locomotion," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43255-6
    DOI: 10.1038/s41467-023-43255-6
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    References listed on IDEAS

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    1. Satoru K. Miura & Massimo Scanziani, 2022. "Publisher Correction: Distinguishing externally from saccade-induced motion in visual cortex," Nature, Nature, vol. 611(7934), pages 5-5, November.
    2. Satoru K. Miura & Massimo Scanziani, 2022. "Distinguishing externally from saccade-induced motion in visual cortex," Nature, Nature, vol. 610(7930), pages 135-142, October.
    3. Tuan Leng Tay & Olaf Ronneberger & Soojin Ryu & Roland Nitschke & Wolfgang Driever, 2011. "Comprehensive catecholaminergic projectome analysis reveals single-neuron integration of zebrafish ascending and descending dopaminergic systems," Nature Communications, Nature, vol. 2(1), pages 1-12, September.
    4. David L. McLean & Jingyi Fan & Shin-ichi Higashijima & Melina E. Hale & Joseph R. Fetcho, 2007. "A topographic map of recruitment in spinal cord," Nature, Nature, vol. 446(7131), pages 71-75, March.
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    Cited by:

    1. Guy Amichay & Liang Li & Máté Nagy & Iain D. Couzin, 2024. "Revealing the mechanism and function underlying pairwise temporal coupling in collective motion," Nature Communications, Nature, vol. 15(1), pages 1-11, December.

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