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A modality-independent proto-organization of human multisensory areas

Author

Listed:
  • Francesca Setti

    (MoMiLab, IMT School for Advanced Studies Lucca)

  • Giacomo Handjaras

    (MoMiLab, IMT School for Advanced Studies Lucca)

  • Davide Bottari

    (MoMiLab, IMT School for Advanced Studies Lucca)

  • Andrea Leo

    (University of Pisa)

  • Matteo Diano

    (University of Turin)

  • Valentina Bruno

    (University of Turin)

  • Carla Tinti

    (University of Turin)

  • Luca Cecchetti

    (MoMiLab, IMT School for Advanced Studies Lucca)

  • Francesca Garbarini

    (University of Turin)

  • Pietro Pietrini

    (MoMiLab, IMT School for Advanced Studies Lucca)

  • Emiliano Ricciardi

    (MoMiLab, IMT School for Advanced Studies Lucca)

Abstract

The processing of multisensory information is based upon the capacity of brain regions, such as the superior temporal cortex, to combine information across modalities. However, it is still unclear whether the representation of coherent auditory and visual events requires any prior audiovisual experience to develop and function. Here we measured brain synchronization during the presentation of an audiovisual, audio-only or video-only version of the same narrative in distinct groups of sensory-deprived (congenitally blind and deaf) and typically developed individuals. Intersubject correlation analysis revealed that the superior temporal cortex was synchronized across auditory and visual conditions, even in sensory-deprived individuals who lack any audiovisual experience. This synchronization was primarily mediated by low-level perceptual features, and relied on a similar modality-independent topographical organization of slow temporal dynamics. The human superior temporal cortex is naturally endowed with a functional scaffolding to yield a common representation across multisensory events.

Suggested Citation

  • Francesca Setti & Giacomo Handjaras & Davide Bottari & Andrea Leo & Matteo Diano & Valentina Bruno & Carla Tinti & Luca Cecchetti & Francesca Garbarini & Pietro Pietrini & Emiliano Ricciardi, 2023. "A modality-independent proto-organization of human multisensory areas," Nature Human Behaviour, Nature, vol. 7(3), pages 397-410, March.
  • Handle: RePEc:nat:nathum:v:7:y:2023:i:3:d:10.1038_s41562-022-01507-3
    DOI: 10.1038/s41562-022-01507-3
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    References listed on IDEAS

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    1. Alexander G. Huth & Wendy A. de Heer & Thomas L. Griffiths & Frédéric E. Theunissen & Jack L. Gallant, 2016. "Natural speech reveals the semantic maps that tile human cerebral cortex," Nature, Nature, vol. 532(7600), pages 453-458, April.
    2. Matthew F. Glasser & Timothy S. Coalson & Emma C. Robinson & Carl D. Hacker & John Harwell & Essa Yacoub & Kamil Ugurbil & Jesper Andersson & Christian F. Beckmann & Mark Jenkinson & Stephen M. Smith , 2016. "A multi-modal parcellation of human cerebral cortex," Nature, Nature, vol. 536(7615), pages 171-178, August.
    3. Velia Cardin & Eleni Orfanidou & Jerker Rönnberg & Cheryl M. Capek & Mary Rudner & Bencie Woll, 2013. "Dissociating cognitive and sensory neural plasticity in human superior temporal cortex," Nature Communications, Nature, vol. 4(1), pages 1-5, June.
    4. Giada Lettieri & Giacomo Handjaras & Emiliano Ricciardi & Andrea Leo & Paolo Papale & Monica Betta & Pietro Pietrini & Luca Cecchetti, 2019. "Emotionotopy in the human right temporo-parietal cortex," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
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    Cited by:

    1. Maria Zimmermann & Rhodri Cusack & Marina Bedny & Marcin Szwed, 2024. "Auditory areas are recruited for naturalistic visual meaning in early deaf people," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    2. Wenbo Li & Yang Liu, 2024. "The influence of visual and auditory environments in parks on visitors’ landscape preference, emotional state, and perceived restorativeness," Palgrave Communications, Palgrave Macmillan, vol. 11(1), pages 1-18, December.

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