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The stimulus-evoked population response in visual cortex of awake monkey is a propagating wave

Author

Listed:
  • Lyle Muller

    (Unité des Neurosciences, Information et Complexité (UNIC), UPR-3293, CNRS, 1 Avenue de la Terrasse)

  • Alexandre Reynaud

    (Institut de Neurosciences de la Timone (INT), CNRS and Aix-Marseille Université, UMR 7289, Campus Santé Timone, 27 boulevard Jean Moulin)

  • Frédéric Chavane

    (Institut de Neurosciences de la Timone (INT), CNRS and Aix-Marseille Université, UMR 7289, Campus Santé Timone, 27 boulevard Jean Moulin)

  • Alain Destexhe

    (Unité des Neurosciences, Information et Complexité (UNIC), UPR-3293, CNRS, 1 Avenue de la Terrasse)

Abstract

Propagating waves occur in many excitable media and were recently found in neural systems from retina to neocortex. While propagating waves are clearly present under anaesthesia, whether they also appear during awake and conscious states remains unclear. One possibility is that these waves are systematically missed in trial-averaged data, due to variability. Here we present a method for detecting propagating waves in noisy multichannel recordings. Applying this method to single-trial voltage-sensitive dye imaging data, we show that the stimulus-evoked population response in primary visual cortex of the awake monkey propagates as a travelling wave, with consistent dynamics across trials. A network model suggests that this reliability is the hallmark of the horizontal fibre network of superficial cortical layers. Propagating waves with similar properties occur independently in secondary visual cortex, but maintain precise phase relations with the waves in primary visual cortex. These results show that, in response to a visual stimulus, propagating waves are systematically evoked in several visual areas, generating a consistent spatiotemporal frame for further neuronal interactions.

Suggested Citation

  • Lyle Muller & Alexandre Reynaud & Frédéric Chavane & Alain Destexhe, 2014. "The stimulus-evoked population response in visual cortex of awake monkey is a propagating wave," Nature Communications, Nature, vol. 5(1), pages 1-14, May.
    • Handle: RePEc:nat:natcom:v:5:y:2014:i:1:d:10.1038_ncomms4675
    DOI: 10.1038/ncomms4675
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    Cited by:

    1. Adeeti Aggarwal & Connor Brennan & Jennifer Luo & Helen Chung & Diego Contreras & Max B. Kelz & Alex Proekt, 2022. "Visual evoked feedforward–feedback traveling waves organize neural activity across the cortical hierarchy in mice," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    2. Georgios Spyropoulos & Matteo Saponati & Jarrod Robert Dowdall & Marieke Louise Schölvinck & Conrado Arturo Bosman & Bruss Lima & Alina Peter & Irene Onorato & Johanna Klon-Lipok & Rasmus Roese & Serg, 2022. "Spontaneous variability in gamma dynamics described by a damped harmonic oscillator driven by noise," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    3. Anirban Das & Alec G. Sheffield & Anirvan S. Nandy & Monika P. Jadi, 2024. "Brain-state mediated modulation of inter-laminar dependencies in visual cortex," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    4. Yifan Gu & Yang Qi & Pulin Gong, 2019. "Rich-club connectivity, diverse population coupling, and dynamical activity patterns emerging from local cortical circuits," PLOS Computational Biology, Public Library of Science, vol. 15(4), pages 1-34, April.
    5. Rory G Townsend & Pulin Gong, 2018. "Detection and analysis of spatiotemporal patterns in brain activity," PLOS Computational Biology, Public Library of Science, vol. 14(12), pages 1-29, December.
    6. James Rankin & Frédéric Chavane, 2017. "Neural field model to reconcile structure with function in primary visual cortex," PLOS Computational Biology, Public Library of Science, vol. 13(10), pages 1-30, October.
    7. David M Alexander & Tonio Ball & Andreas Schulze-Bonhage & Cees van Leeuwen, 2019. "Large-scale cortical travelling waves predict localized future cortical signals," PLOS Computational Biology, Public Library of Science, vol. 15(11), pages 1-34, November.
    8. Dominik P. Koller & Michael Schirner & Petra Ritter, 2024. "Human connectome topology directs cortical traveling waves and shapes frequency gradients," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    9. Gabriel B. Benigno & Roberto C. Budzinski & Zachary W. Davis & John H. Reynolds & Lyle Muller, 2023. "Waves traveling over a map of visual space can ignite short-term predictions of sensory input," Nature Communications, Nature, vol. 14(1), pages 1-14, December.

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