Excitatory Neuronal Hubs Configure Multisensory Integration of Slow Waves in Association Cortex

Satoshi Kuroki, Takamasa Yoshida, Hidekazu Tsutsui, Mizuho Iwama, Reiko Ando, Takayuki Michikawa, Atsushi Miyawaki, Toshio Ohshima, Shigeyoshi Itohara

    Research output: Contribution to journalArticle

    6 Citations (Scopus)

    Abstract

    Multisensory integration (MSI) is a fundamental emergent property of the mammalian brain. During MSI, perceptual information encoded in patterned activity is processed in multimodal association cortex. The systems-level neuronal dynamics that coordinate MSI, however, are unknown. Here, we demonstrate intrinsic hub-like network activity in the association cortex that regulates MSI. We engineered calcium reporter mouse lines based on the fluorescence resonance energy transfer sensor yellow cameleon (YC2.60) expressed in excitatory or inhibitory neurons. In medial and parietal association cortex, we observed spontaneous slow waves that self-organized into hubs defined by long-range excitatory and local inhibitory circuits. Unlike directional source/sink-like flows in sensory areas, medial/parietal excitatory and inhibitory hubs had net-zero balanced inputs. Remarkably, multisensory stimulation triggered rapid phase-locking mainly of excitatory hub activity persisting for seconds after the stimulus offset. Therefore, association cortex tends to form balanced excitatory networks that configure slow-wave phase-locking for MSI. Video Abstract [Figure presented] Kuroki et al. performed cell-type-specific, wide-field FRET-based calcium imaging to visualize cortical network activity induced by multisensory inputs. They observed phase-locking of cortical slow waves in excitatory neuronal hubs in association cortical areas that may underlie multisensory integration.

    Original languageEnglish
    Pages (from-to)2809-2817
    Number of pages9
    JournalCell Reports
    Volume22
    Issue number11
    DOIs
    Publication statusPublished - 2018 Mar 13

    Fingerprint

    Calcium
    Fluorescence Resonance Energy Transfer
    Parietal Lobe
    Neurons
    Brain
    Imaging techniques
    Networks (circuits)
    Sensors
    yellow cameleon

    Keywords

    • association cortex
    • cortical slow waves
    • excitatory neuron
    • fluorescence resonance energy transfer
    • inhibitory neuron
    • mouse
    • multisensory integration
    • phase locking
    • spontaneous activity
    • wide-field calcium imaging

    ASJC Scopus subject areas

    • Biochemistry, Genetics and Molecular Biology(all)

    Cite this

    Kuroki, S., Yoshida, T., Tsutsui, H., Iwama, M., Ando, R., Michikawa, T., ... Itohara, S. (2018). Excitatory Neuronal Hubs Configure Multisensory Integration of Slow Waves in Association Cortex. Cell Reports, 22(11), 2809-2817. https://doi.org/10.1016/j.celrep.2018.02.056

    Excitatory Neuronal Hubs Configure Multisensory Integration of Slow Waves in Association Cortex. / Kuroki, Satoshi; Yoshida, Takamasa; Tsutsui, Hidekazu; Iwama, Mizuho; Ando, Reiko; Michikawa, Takayuki; Miyawaki, Atsushi; Ohshima, Toshio; Itohara, Shigeyoshi.

    In: Cell Reports, Vol. 22, No. 11, 13.03.2018, p. 2809-2817.

    Research output: Contribution to journalArticle

    Kuroki, S, Yoshida, T, Tsutsui, H, Iwama, M, Ando, R, Michikawa, T, Miyawaki, A, Ohshima, T & Itohara, S 2018, 'Excitatory Neuronal Hubs Configure Multisensory Integration of Slow Waves in Association Cortex', Cell Reports, vol. 22, no. 11, pp. 2809-2817. https://doi.org/10.1016/j.celrep.2018.02.056
    Kuroki S, Yoshida T, Tsutsui H, Iwama M, Ando R, Michikawa T et al. Excitatory Neuronal Hubs Configure Multisensory Integration of Slow Waves in Association Cortex. Cell Reports. 2018 Mar 13;22(11):2809-2817. https://doi.org/10.1016/j.celrep.2018.02.056
    Kuroki, Satoshi ; Yoshida, Takamasa ; Tsutsui, Hidekazu ; Iwama, Mizuho ; Ando, Reiko ; Michikawa, Takayuki ; Miyawaki, Atsushi ; Ohshima, Toshio ; Itohara, Shigeyoshi. / Excitatory Neuronal Hubs Configure Multisensory Integration of Slow Waves in Association Cortex. In: Cell Reports. 2018 ; Vol. 22, No. 11. pp. 2809-2817.
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