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Waves traveling over a map of visual space can ignite short-term predictions of sensory input

Author

Listed:
  • Gabriel B. Benigno

    (Western University
    Western University
    Western University)

  • Roberto C. Budzinski

    (Western University
    Western University
    Western University)

  • Zachary W. Davis

    (The Salk Institute for Biological Studies)

  • John H. Reynolds

    (The Salk Institute for Biological Studies)

  • Lyle Muller

    (Western University
    Western University
    Western University)

Abstract

Recent analyses have found waves of neural activity traveling across entire visual cortical areas in awake animals. These traveling waves modulate the excitability of local networks and perceptual sensitivity. The general computational role of these spatiotemporal patterns in the visual system, however, remains unclear. Here, we hypothesize that traveling waves endow the visual system with the capacity to predict complex and naturalistic inputs. We present a network model whose connections can be rapidly and efficiently trained to predict individual natural movies. After training, a few input frames from a movie trigger complex wave patterns that drive accurate predictions many frames into the future solely from the network’s connections. When the recurrent connections that drive waves are randomly shuffled, both traveling waves and the ability to predict are eliminated. These results suggest traveling waves may play an essential computational role in the visual system by embedding continuous spatiotemporal structures over spatial maps.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39076-2
    DOI: 10.1038/s41467-023-39076-2
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    References listed on IDEAS

    as
    1. 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.
    2. Zachary W. Davis & Gabriel B. Benigno & Charlee Fletterman & Theo Desbordes & Christopher Steward & Terrence J. Sejnowski & John Reynolds & Lyle Muller, 2021. "Spontaneous traveling waves naturally emerge from horizontal fiber time delays and travel through locally asynchronous-irregular states," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    3. Kazutaka Takahashi & Sanggyun Kim & Todd P. Coleman & Kevin A. Brown & Aaron J. Suminski & Matthew D. Best & Nicholas G. Hatsopoulos, 2015. "Large-scale spatiotemporal spike patterning consistent with wave propagation in motor cortex," Nature Communications, Nature, vol. 6(1), pages 1-11, November.
    4. Aidan J. Horner & James A. Bisby & Daniel Bush & Wen-Jing Lin & Neil Burgess, 2015. "Evidence for holistic episodic recollection via hippocampal pattern completion," Nature Communications, Nature, vol. 6(1), pages 1-11, November.
    5. 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.
    6. Zachary W. Davis & Lyle Muller & Julio Martinez-Trujillo & Terrence Sejnowski & John H. Reynolds, 2020. "Spontaneous travelling cortical waves gate perception in behaving primates," Nature, Nature, vol. 587(7834), pages 432-436, November.
    7. Evan S Schaffer & Srdjan Ostojic & L F Abbott, 2013. "A Complex-Valued Firing-Rate Model That Approximates the Dynamics of Spiking Networks," PLOS Computational Biology, Public Library of Science, vol. 9(10), pages 1-11, October.
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