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Perception's shadow: long-distance synchronization of human brain activity

Author

Listed:
  • Eugenio Rodriguez

    (Laboratoire de Neurosciences Cognitives et Imagerie Cérbréale (LENA))

  • Nathalie George

    (Laboratoire de Neurosciences Cognitives et Imagerie Cérbréale (LENA))

  • Jean-Philippe Lachaux

    (Laboratoire de Neurosciences Cognitives et Imagerie Cérbréale (LENA))

  • Jacques Martinerie

    (Laboratoire de Neurosciences Cognitives et Imagerie Cérbréale (LENA))

  • Bernard Renault

    (Laboratoire de Neurosciences Cognitives et Imagerie Cérbréale (LENA))

  • Francisco J. Varela

    (Laboratoire de Neurosciences Cognitives et Imagerie Cérbréale (LENA))

Abstract

Transient periods of synchronization of oscillating neuronal discharges in the frequency range 30–80 Hz (gamma oscillations) have been proposed to act as an integrative mechanism that may bring a widely distributed set of neurons together into a coherent ensemble that underlies a cognitive act1,2,3,4. Results of several experiments in animals provide support for this idea (see, for example, refs 4,5,6,7,8,9,10). In humans, gamma oscillations have been described both on the scalp11,12,13,14,15,16 (measured by electroencephalography and magnetoencephalography) and in intracortical recordings17, but no direct participation of synchrony in a cognitive task has been demonstrated so far. Here we record electrical brain activity from subjects who are viewing ambiguous visual stimuli (perceived either as faces or as meaningless shapes). We show for the first time, to our knowledge, that only face perception induces a long-distance pattern of synchronization, corresponding to the moment of perception itself and to the ensuing motor response. A period of strong desynchronization marks the transition between the moment of perception and the motor response. We suggest that this desynchronization reflects a process of active uncoupling of the underlying neural ensembles that is necessary to proceed from one cognitive state to another3.

Suggested Citation

  • Eugenio Rodriguez & Nathalie George & Jean-Philippe Lachaux & Jacques Martinerie & Bernard Renault & Francisco J. Varela, 1999. "Perception's shadow: long-distance synchronization of human brain activity," Nature, Nature, vol. 397(6718), pages 430-433, February.
    • Handle: RePEc:nat:nature:v:397:y:1999:i:6718:d:10.1038_17120
    DOI: 10.1038/17120
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    Citations

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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. Christian G Fink & Victoria Booth & Michal Zochowski, 2011. "Cellularly-Driven Differences in Network Synchronization Propensity Are Differentially Modulated by Firing Frequency," PLOS Computational Biology, Public Library of Science, vol. 7(5), pages 1-14, May.
    3. Yuichi Katori & Kazuhiro Sakamoto & Naohiro Saito & Jun Tanji & Hajime Mushiake & Kazuyuki Aihara, 2011. "Representational Switching by Dynamical Reorganization of Attractor Structure in a Network Model of the Prefrontal Cortex," PLOS Computational Biology, Public Library of Science, vol. 7(11), pages 1-17, November.
    4. Hu, Xueyan & Ding, Qianming & Wu, Yong & Huang, Weifang & Yang, Lijian & Jia, Ya, 2024. "Dynamical rewiring promotes synchronization in memristive FitzHugh-Nagumo neuronal networks," Chaos, Solitons & Fractals, Elsevier, vol. 184(C).
    5. Andreas Wilmer & Marc de Lussanet & Markus Lappe, 2012. "Time-Delayed Mutual Information of the Phase as a Measure of Functional Connectivity," PLOS ONE, Public Library of Science, vol. 7(9), pages 1-22, September.
    6. François O David & Etienne Hugues & Tristan Cenier & Nicolas Fourcaud-Trocmé & Nathalie Buonviso, 2009. "Specific Entrainment of Mitral Cells during Gamma Oscillation in the Rat Olfactory Bulb," PLOS Computational Biology, Public Library of Science, vol. 5(10), pages 1-19, October.
    7. Muto, Makoto & Saiki, Yoshitaka, 2024. "Synchronization analysis between exchange rates on the basis of purchasing power parity using the Hilbert transform," The North American Journal of Economics and Finance, Elsevier, vol. 74(C).
    8. Wu, Huagan & Bian, Yixuan & Zhang, Yunzhen & Guo, Yixuan & Xu, Quan & Chen, Mo, 2023. "Multi-stable states and synchronicity of a cellular neural network with memristive activation function," Chaos, Solitons & Fractals, Elsevier, vol. 177(C).
    9. Jajcay, Nikola, 2018. "Spatial and temporal scales of atmospheric dynamics," Thesis Commons ar8ks_v1, Center for Open Science.
    10. Wu, Yong & Ding, Qianming & Huang, Weifang & Hu, Xueyan & Ye, Zhiqiu & Jia, Ya, 2024. "Dynamic modulation of external excitation enhance synchronization in complex neuronal network," Chaos, Solitons & Fractals, Elsevier, vol. 183(C).
    11. Cao, Haoyu & Yang, Zhiyin & Liu, Zonghua, 2023. "Remote synchronization in multi-layered community networks with star-like topology," Chaos, Solitons & Fractals, Elsevier, vol. 166(C).
    12. Shilpa Chakravartula & Premananda Indic & Bala Sundaram & Timothy Killingback, 2017. "Emergence of local synchronization in neuronal networks with adaptive couplings," PLOS ONE, Public Library of Science, vol. 12(6), pages 1-16, June.

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