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Asymmetric Signaling Across the Hierarchy of Cytoarchitecture within the Human Connectome

View ORCID ProfileLinden Parkes, Jason Z Kim, Jennifer Stiso, View ORCID ProfileMonica E Calkins, View ORCID ProfileMatthew Cieslak, Raquel E Gur, View ORCID ProfileRuben C Gur, View ORCID ProfileTyler M Moore, Mathieu Ouellet, View ORCID ProfileDavid R Roalf, View ORCID ProfileRussell T Shinohara, Daniel H Wolf, View ORCID ProfileTheodore D Satterthwaite, View ORCID ProfileDani S Bassett
doi: https://doi.org/10.1101/2022.05.13.491642
Linden Parkes
1Department of Bioengineering, School of Engineering & Applied Science, University of Pennsylvania, Philadelphia, PA, 19104 USA
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  • For correspondence: lindenmp@seas.upenn.edu
Jason Z Kim
1Department of Bioengineering, School of Engineering & Applied Science, University of Pennsylvania, Philadelphia, PA, 19104 USA
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Jennifer Stiso
1Department of Bioengineering, School of Engineering & Applied Science, University of Pennsylvania, Philadelphia, PA, 19104 USA
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Monica E Calkins
2Department of Psychiatry, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA
3Lifespan Brain Institute, University of Pennsylvania & Children’s Hospital of Philadelphia, Philadelphia, USA
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Matthew Cieslak
2Department of Psychiatry, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA
3Lifespan Brain Institute, University of Pennsylvania & Children’s Hospital of Philadelphia, Philadelphia, USA
4Center for Biomedical Image Computing and Analytics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104 USA
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Raquel E Gur
2Department of Psychiatry, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA
3Lifespan Brain Institute, University of Pennsylvania & Children’s Hospital of Philadelphia, Philadelphia, USA
5Department of Neurology, Perelman School of Medicine, Philadelphia, PA 19104 USA
6Department of Radiology, Perelman School of Medicine, Philadelphia, PA 19104 USA
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Ruben C Gur
2Department of Psychiatry, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA
3Lifespan Brain Institute, University of Pennsylvania & Children’s Hospital of Philadelphia, Philadelphia, USA
5Department of Neurology, Perelman School of Medicine, Philadelphia, PA 19104 USA
6Department of Radiology, Perelman School of Medicine, Philadelphia, PA 19104 USA
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Tyler M Moore
2Department of Psychiatry, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA
3Lifespan Brain Institute, University of Pennsylvania & Children’s Hospital of Philadelphia, Philadelphia, USA
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Mathieu Ouellet
7Department of Electrical & Systems Engineering, School of Engineering & Applied Science, University of Pennsylvania, Philadelphia, PA 19104 USA
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David R Roalf
2Department of Psychiatry, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA
3Lifespan Brain Institute, University of Pennsylvania & Children’s Hospital of Philadelphia, Philadelphia, USA
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Russell T Shinohara
4Center for Biomedical Image Computing and Analytics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104 USA
8Penn Statistics in Imaging and Visualization Center, Department of Biostatistics, Epidemiology, and Informatics, University of Pennsylvania, Perelman School of Medicine, Philadelphia, Pennsylvania
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Daniel H Wolf
2Department of Psychiatry, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA
4Center for Biomedical Image Computing and Analytics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104 USA
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Theodore D Satterthwaite
2Department of Psychiatry, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA
3Lifespan Brain Institute, University of Pennsylvania & Children’s Hospital of Philadelphia, Philadelphia, USA
4Center for Biomedical Image Computing and Analytics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104 USA
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Dani S Bassett
1Department of Bioengineering, School of Engineering & Applied Science, University of Pennsylvania, Philadelphia, PA, 19104 USA
2Department of Psychiatry, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA
5Department of Neurology, Perelman School of Medicine, Philadelphia, PA 19104 USA
9Department of Electrical & Systems Engineering, School of Engineering & Applied Science, University of Pennsylvania, Philadelphia, PA, 19104 USA
10Department of Physics & Astronomy, College of Arts & Sciences, University of Pennsylvania, Philadelphia, PA, 19104 USA
11Santa Fe Institute, Santa Fe, NM 87501 USA
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Abstract

Cortical variations in cytoarchitecture form a sensory-fugal axis that systematically shapes regional profiles of extrinsic connectivity. Additionally, this axis is thought to guide signal propagation and integration across the cortical hierarchy. While human neuroimaging work has shown that this axis constrains local properties of the human connectome, it remains unclear whether it also shapes the asymmetric signaling that arises from higher-order connectome topology. Here, we used network control theory to examine the amount of energy required to propagate dynamics across the sensory-fugal axis. Our results revealed an asymmetry in this energy indicating that bottom-up transitions were easier to complete compared to top-down transitions. Supporting analyses demonstrated that this asymmetry was underpinned by a connectome topology that is wired to support efficient bottom-up signaling. Finally, we found that this asymmetry correlated with changes in intrinsic neuronal timescales and lessened throughout youth. Our results show that cortical variation in cytoarchitecture may guide the formation of macroscopic connectome topology.

Competing Interest Statement

R.T.S. receives consulting compensation from Octave Bioscience and compensation for reviewership duties from the American Medical Association

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 4.0 International license.
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Posted May 13, 2022.
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Asymmetric Signaling Across the Hierarchy of Cytoarchitecture within the Human Connectome
Linden Parkes, Jason Z Kim, Jennifer Stiso, Monica E Calkins, Matthew Cieslak, Raquel E Gur, Ruben C Gur, Tyler M Moore, Mathieu Ouellet, David R Roalf, Russell T Shinohara, Daniel H Wolf, Theodore D Satterthwaite, Dani S Bassett
bioRxiv 2022.05.13.491642; doi: https://doi.org/10.1101/2022.05.13.491642
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Asymmetric Signaling Across the Hierarchy of Cytoarchitecture within the Human Connectome
Linden Parkes, Jason Z Kim, Jennifer Stiso, Monica E Calkins, Matthew Cieslak, Raquel E Gur, Ruben C Gur, Tyler M Moore, Mathieu Ouellet, David R Roalf, Russell T Shinohara, Daniel H Wolf, Theodore D Satterthwaite, Dani S Bassett
bioRxiv 2022.05.13.491642; doi: https://doi.org/10.1101/2022.05.13.491642

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