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Immediate neural impact and incomplete compensation after semantic hub disconnection

Author

Listed:
  • Zsuzsanna Kocsis

    (University of Iowa
    Newcastle University Medical School
    Carnegie Mellon University)

  • Rick L. Jenison

    (University of Wisconsin)

  • Peter N. Taylor

    (Newcastle University
    Queen Square)

  • Ryan M. Calmus

    (University of Iowa
    Newcastle University Medical School)

  • Bob McMurray

    (University of Iowa)

  • Ariane E. Rhone

    (University of Iowa)

  • McCall E. Sarrett

    (Gonzaga University)

  • Carolina Deifelt Streese

    (University of Iowa)

  • Yukiko Kikuchi

    (Newcastle University Medical School)

  • Phillip E. Gander

    (University of Iowa
    University of Iowa
    University of Iowa)

  • Joel I. Berger

    (University of Iowa)

  • Christopher K. Kovach

    (University of Iowa)

  • Inyong Choi

    (University of Iowa)

  • Jeremy D. Greenlee

    (University of Iowa)

  • Hiroto Kawasaki

    (University of Iowa)

  • Thomas E. Cope

    (Cambridge University
    Cambridge University)

  • Timothy D. Griffiths

    (Newcastle University Medical School)

  • Matthew A. Howard

    (University of Iowa)

  • Christopher I. Petkov

    (University of Iowa
    Newcastle University Medical School)

Abstract

The human brain extracts meaning using an extensive neural system for semantic knowledge. Whether broadly distributed systems depend on or can compensate after losing a highly interconnected hub is controversial. We report intracranial recordings from two patients during a speech prediction task, obtained minutes before and after neurosurgical treatment requiring disconnection of the left anterior temporal lobe (ATL), a candidate semantic knowledge hub. Informed by modern diaschisis and predictive coding frameworks, we tested hypotheses ranging from solely neural network disruption to complete compensation by the indirectly affected language-related and speech-processing sites. Immediately after ATL disconnection, we observed neurophysiological alterations in the recorded frontal and auditory sites, providing direct evidence for the importance of the ATL as a semantic hub. We also obtained evidence for rapid, albeit incomplete, attempts at neural network compensation, with neural impact largely in the forms stipulated by the predictive coding framework, in specificity, and the modern diaschisis framework, more generally. The overall results validate these frameworks and reveal an immediate impact and capability of the human brain to adjust after losing a brain hub.

Suggested Citation

  • Zsuzsanna Kocsis & Rick L. Jenison & Peter N. Taylor & Ryan M. Calmus & Bob McMurray & Ariane E. Rhone & McCall E. Sarrett & Carolina Deifelt Streese & Yukiko Kikuchi & Phillip E. Gander & Joel I. Ber, 2023. "Immediate neural impact and incomplete compensation after semantic hub disconnection," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-42088-7
    DOI: 10.1038/s41467-023-42088-7
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    References listed on IDEAS

    as
    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. E. A. Solomon & J. E. Kragel & M. R. Sperling & A. Sharan & G. Worrell & M. Kucewicz & C. S. Inman & B. Lega & K. A. Davis & J. M. Stein & B. C. Jobst & K. A. Zaghloul & S. A. Sheth & D. S. Rizzuto & , 2017. "Widespread theta synchrony and high-frequency desynchronization underlies enhanced cognition," Nature Communications, Nature, vol. 8(1), pages 1-14, December.
    3. Thomas E. Cope & E. Sohoglu & W. Sedley & K. Patterson & P. S. Jones & J. Wiggins & C. Dawson & M. Grube & R. P. Carlyon & T. D. Griffiths & Matthew H. Davis & James B. Rowe, 2017. "Evidence for causal top-down frontal contributions to predictive processes in speech perception," Nature Communications, Nature, vol. 8(1), pages 1-16, December.
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