Asymmetric signaling across the hierarchy of cytoarchitecture within the human connectome

Author:

Parkes Linden1ORCID,Kim Jason Z.1ORCID,Stiso Jennifer1,Calkins Monica E.23,Cieslak Matthew234ORCID,Gur Raquel E.2356ORCID,Gur Ruben C.2356ORCID,Moore Tyler M.23ORCID,Ouellet Mathieu7ORCID,Roalf David R.23,Shinohara Russell T.48,Wolf Daniel H.24ORCID,Satterthwaite Theodore D.234ORCID,Bassett Dani S.12579ORCID

Affiliation:

1. Department of Bioengineering, School of Engineering and Applied Science, University of Pennsylvania, Philadelphia, PA 19104, USA.

2. Department of Psychiatry, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.

3. Lifespan Brain Institute, University of Pennsylvania and Children’s Hospital of Philadelphia, Philadelphia, PA 19104, USA.

4. Center for Biomedical Image Computing and Analytics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.

5. Department of Neurology, Perelman School of Medicine, Philadelphia, PA 19104, USA.

6. Department of Radiology, Perelman School of Medicine, Philadelphia, PA 19104, USA.

7. Department of Electrical and Systems Engineering, School of Engineering and Applied Science, University of Pennsylvania, Philadelphia, PA 19104, USA.

8. Penn Statistics in Imaging and Visualization Center, Department of Biostatistics, Epidemiology, and Informatics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.

9. Department of Physics and Astronomy, College of Arts and Sciences, University of Pennsylvania, Philadelphia, PA 19104, USA.

Abstract

Cortical variations in cytoarchitecture form a sensory-fugal axis that shapes regional profiles of extrinsic connectivity and is thought to guide signal propagation and integration across the cortical hierarchy. While 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 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. Supporting analyses demonstrated that asymmetries were underpinned by a connectome topology that is wired to support efficient bottom-up signaling. Lastly, we found that asymmetries correlated with differences in communicability and intrinsic neuronal time scales and lessened throughout youth. Our results show that cortical variation in cytoarchitecture may guide the formation of macroscopic connectome topology.

Publisher

American Association for the Advancement of Science (AAAS)

Subject

Multidisciplinary

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