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Greater TMS-evoked frontoparietal effective connectivity is correlated with better cognitive performance

View ORCID ProfileTimothy P. Morris, Maria Redondo-Camos, Gabriele Cattaneo, Didac Macia, Javier Solana-Sanchez, Goretti Espanya-Irla, Selma Delgado-Gallén, Vanessa Alviarez-Schulze, Catherine Pachón-Garcia, View ORCID ProfileEmiliano Santarnecchi, Ehsan Tadayon, Recep Ozdemir, Jose Ma Tormos Muñoz, David Batres-Faz, Alvaro Pascual-Leone, Mouhsin M. Shafi
doi: https://doi.org/10.1101/2020.08.03.234518
Timothy P. Morris
1Berenson-Allen Center for Noninvasive Brain Stimulation, Department of Neurology, Beth Israel Deaconess Medical Center and Harvard Medical School, Boston, United States
2Guttmann Brain Health Institute, Institut Guttmann, Institut Universitari de Neurorehabilitació Adscrit a la UAB, Badalona, Spain
3Center for Cognitive and Brain Health, Northeastern University, Boston, United States
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  • ORCID record for Timothy P. Morris
Maria Redondo-Camos
2Guttmann Brain Health Institute, Institut Guttmann, Institut Universitari de Neurorehabilitació Adscrit a la UAB, Badalona, Spain
4Universitat Autònoma de Barcelona, Bellaterra, Spain
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Gabriele Cattaneo
2Guttmann Brain Health Institute, Institut Guttmann, Institut Universitari de Neurorehabilitació Adscrit a la UAB, Badalona, Spain
4Universitat Autònoma de Barcelona, Bellaterra, Spain
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Didac Macia
6Departament de Medicina, Facultat de Medicina i Ciències de la Salut i Institut de Neurociències, Universitat de Barcelona, Barcelona, Spain
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Javier Solana-Sanchez
2Guttmann Brain Health Institute, Institut Guttmann, Institut Universitari de Neurorehabilitació Adscrit a la UAB, Badalona, Spain
4Universitat Autònoma de Barcelona, Bellaterra, Spain
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Goretti Espanya-Irla
2Guttmann Brain Health Institute, Institut Guttmann, Institut Universitari de Neurorehabilitació Adscrit a la UAB, Badalona, Spain
4Universitat Autònoma de Barcelona, Bellaterra, Spain
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Selma Delgado-Gallén
2Guttmann Brain Health Institute, Institut Guttmann, Institut Universitari de Neurorehabilitació Adscrit a la UAB, Badalona, Spain
4Universitat Autònoma de Barcelona, Bellaterra, Spain
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Vanessa Alviarez-Schulze
2Guttmann Brain Health Institute, Institut Guttmann, Institut Universitari de Neurorehabilitació Adscrit a la UAB, Badalona, Spain
4Universitat Autònoma de Barcelona, Bellaterra, Spain
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Catherine Pachón-Garcia
2Guttmann Brain Health Institute, Institut Guttmann, Institut Universitari de Neurorehabilitació Adscrit a la UAB, Badalona, Spain
4Universitat Autònoma de Barcelona, Bellaterra, Spain
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Emiliano Santarnecchi
1Berenson-Allen Center for Noninvasive Brain Stimulation, Department of Neurology, Beth Israel Deaconess Medical Center and Harvard Medical School, Boston, United States
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Ehsan Tadayon
1Berenson-Allen Center for Noninvasive Brain Stimulation, Department of Neurology, Beth Israel Deaconess Medical Center and Harvard Medical School, Boston, United States
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Recep Ozdemir
1Berenson-Allen Center for Noninvasive Brain Stimulation, Department of Neurology, Beth Israel Deaconess Medical Center and Harvard Medical School, Boston, United States
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Jose Ma Tormos Muñoz
2Guttmann Brain Health Institute, Institut Guttmann, Institut Universitari de Neurorehabilitació Adscrit a la UAB, Badalona, Spain
4Universitat Autònoma de Barcelona, Bellaterra, Spain
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David Batres-Faz
2Guttmann Brain Health Institute, Institut Guttmann, Institut Universitari de Neurorehabilitació Adscrit a la UAB, Badalona, Spain
6Departament de Medicina, Facultat de Medicina i Ciències de la Salut i Institut de Neurociències, Universitat de Barcelona, Barcelona, Spain
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Alvaro Pascual-Leone
2Guttmann Brain Health Institute, Institut Guttmann, Institut Universitari de Neurorehabilitació Adscrit a la UAB, Badalona, Spain
5Hinda and Arthur Marcus Institute for Aging Research and Center for Memory Health, Hebrew SeniorLife, Department of Neurology, Harvard Medical School, Boston, United States
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Mouhsin M. Shafi
1Berenson-Allen Center for Noninvasive Brain Stimulation, Department of Neurology, Beth Israel Deaconess Medical Center and Harvard Medical School, Boston, United States
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  • For correspondence: mshafi@bidmc.harvard.edu
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Abstract

Fronto-parietal activity has been related to fluid intelligence and flexible cognitive control. However, causal insights on this relation are lacking. We used real-time integration of MRI-guided TMS and EEG to characterize the spatial and temporal properties of signal propagation between these two regions and relate them to cognitive performance.

31 healthy adults (55 ±6 years, 20 female) underwent TMS-EEG and a full cognitive assessment. Local and propagated current from 5 source space-reconstructed scouts ipsilateral to two stimulation sites (pre frontal cortex (PFC) and inferior parietal lobule (IPL)) was quantified in two-time windows (15-40ms and 40-80ms) and related to domain-general (global cognition) and domain-specific (memory, working memory, reasoning, flexibility, lexical access and visuo-spatial) cognitive functions.

TMS-evoked activity from stimulation of the PFC and the IPL resulted in local and distributed activity across frontoparietal regions. TMS-evoked activity in local regions was not correlated with cognitive functions. In response to TMS of the PFC, propagated current to the distal superior parietal scout in the first 15-40ms was significantly associated with global cognition (β = 2.63, SE = .898, p = .008, R2 = .31). Similarly, following TMS of the IPL, propagation to the middle prefrontal gyrus scout (15-40ms) was significantly associated with global cognition (β = 2.67, SE = 1.289, p = .025, R2 = .27). In an exploratory step, domain-specific correlations were seen in the PFC condition.

Locally evoked activity measured via source space reconstruction from TMS of two association hubs is not associated with cognitive functions. However, the propagation of the TMS pulse through frontoparietal connections is associated with overall cognitive ability. These associations are driven by a number of cognitive domains in the PFC stimulation condition.

Competing Interest Statement

Dr. A. Pascual-Leone serves on the scientific advisory boards for Starlab Neuroscience, Neuroelectrics, Magstim, Magventure, and Nexstim; is co-founder of Linus Health; and is listed as an inventor on several issued and pending patents on the real-time integration of transcranial magnetic stimulation with electroencephalography and magnetic resonance imaging. All other authors disclose no conflicts of interest including no financial, personal, or other relationships with other people or organizations that could inappropriately influence this work

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted August 04, 2020.
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Greater TMS-evoked frontoparietal effective connectivity is correlated with better cognitive performance
Timothy P. Morris, Maria Redondo-Camos, Gabriele Cattaneo, Didac Macia, Javier Solana-Sanchez, Goretti Espanya-Irla, Selma Delgado-Gallén, Vanessa Alviarez-Schulze, Catherine Pachón-Garcia, Emiliano Santarnecchi, Ehsan Tadayon, Recep Ozdemir, Jose Ma Tormos Muñoz, David Batres-Faz, Alvaro Pascual-Leone, Mouhsin M. Shafi
bioRxiv 2020.08.03.234518; doi: https://doi.org/10.1101/2020.08.03.234518
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Greater TMS-evoked frontoparietal effective connectivity is correlated with better cognitive performance
Timothy P. Morris, Maria Redondo-Camos, Gabriele Cattaneo, Didac Macia, Javier Solana-Sanchez, Goretti Espanya-Irla, Selma Delgado-Gallén, Vanessa Alviarez-Schulze, Catherine Pachón-Garcia, Emiliano Santarnecchi, Ehsan Tadayon, Recep Ozdemir, Jose Ma Tormos Muñoz, David Batres-Faz, Alvaro Pascual-Leone, Mouhsin M. Shafi
bioRxiv 2020.08.03.234518; doi: https://doi.org/10.1101/2020.08.03.234518

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