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Orthogonalization of spontaneous and stimulus-driven activity by hierarchical neocortical areal network in primates

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  • Teppei Matsui

    (The University of Tokyo
    Doshisha University
    Kyushu University
    Japan Science and Technology Agency)

  • Takayuki Hashimoto

    (The University of Tokyo
    Kyushu University
    The University of Tokyo)

  • Tomonari Murakami

    (The University of Tokyo
    Kyushu University
    The University of Tokyo)

  • Masato Uemura

    (The University of Tokyo
    Kyushu University
    The University of Tokyo
    Kansai Medical University)

  • Kohei Kikuta

    (The University of Tokyo
    The University of Tokyo)

  • Toshiki Kato

    (The University of Tokyo
    The University of Tokyo)

  • Kenichi Ohki

    (The University of Tokyo
    Kyushu University
    The University of Tokyo
    The University of Tokyo)

Abstract

How biological neural networks reliably process information in the presence of spontaneous activity remains controversial. In mouse primary visual cortex (V1), stimulus-evoked and spontaneous activity show orthogonal (dissimilar) patterns, which is advantageous for separating sensory signals from internal noise. However, studies in carnivore and primate V1, which have functional columns, have reported high similarity between stimulus-evoked and spontaneous activity. Thus, the mechanism of signal-noise separation in the columnar visual cortex may be different from that in rodents. To address this issue, we compared spontaneous and stimulus-evoked activity in marmoset V1 and higher visual areas. In marmoset V1, spontaneous and stimulus-evoked activity showed similar patterns as expected. However, in marmoset higher visual areas, spontaneous and stimulus-evoked activity were progressively orthogonalized along the cortical hierarchy, eventually reaching levels comparable to those in mouse V1. These results suggest that orthogonalization of spontaneous and stimulus-evoked activity is a general principle of cortical computation.

Suggested Citation

  • Teppei Matsui & Takayuki Hashimoto & Tomonari Murakami & Masato Uemura & Kohei Kikuta & Toshiki Kato & Kenichi Ohki, 2024. "Orthogonalization of spontaneous and stimulus-driven activity by hierarchical neocortical areal network in primates," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-54322-x
    DOI: 10.1038/s41467-024-54322-x
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    References listed on IDEAS

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    1. József Fiser & Chiayu Chiu & Michael Weliky, 2004. "Small modulation of ongoing cortical dynamics by sensory input during natural vision," Nature, Nature, vol. 431(7008), pages 573-578, September.
    2. Kenichi Ohki & Sooyoung Chung & Yeang H. Ch'ng & Prakash Kara & R. Clay Reid, 2005. "Functional imaging with cellular resolution reveals precise micro-architecture in visual cortex," Nature, Nature, vol. 433(7026), pages 597-603, February.
    3. Stefano Recanatesi & Gabriel Koch Ocker & Michael A Buice & Eric Shea-Brown, 2019. "Dimensionality in recurrent spiking networks: Global trends in activity and local origins in connectivity," PLOS Computational Biology, Public Library of Science, vol. 15(7), pages 1-29, July.
    4. J. L. Vincent & G. H. Patel & M. D. Fox & A. Z. Snyder & J. T. Baker & D. C. Van Essen & J. M. Zempel & L. H. Snyder & M. Corbetta & M. E. Raichle, 2007. "Intrinsic functional architecture in the anaesthetized monkey brain," Nature, Nature, vol. 447(7140), pages 83-86, May.
    5. Satoru Kondo & Takashi Yoshida & Kenichi Ohki, 2016. "Mixed functional microarchitectures for orientation selectivity in the mouse primary visual cortex," Nature Communications, Nature, vol. 7(1), pages 1-16, December.
    6. Tal Kenet & Dmitri Bibitchkov & Misha Tsodyks & Amiram Grinvald & Amos Arieli, 2003. "Spontaneously emerging cortical representations of visual attributes," Nature, Nature, vol. 425(6961), pages 954-956, October.
    7. Lawrence H. Snyder & Kenneth L. Grieve & Peter Brotchie & Richard A. Andersen, 1998. "Separate body- and world-referenced representations of visual space in parietal cortex," Nature, Nature, vol. 394(6696), pages 887-891, August.
    8. Tsai-Wen Chen & Trevor J. Wardill & Yi Sun & Stefan R. Pulver & Sabine L. Renninger & Amy Baohan & Eric R. Schreiter & Rex A. Kerr & Michael B. Orger & Vivek Jayaraman & Loren L. Looger & Karel Svobod, 2013. "Ultrasensitive fluorescent proteins for imaging neuronal activity," Nature, Nature, vol. 499(7458), pages 295-300, July.
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