Network structure-function coupling and neurocognition in cerebral small vessel disease

Jonathan Tay; Marco Düring; Esther M C van Leijsen; Mayra I Bergkamp; David G Norris; Frank-Erik de Leeuw; Hugh S Markus; Anil M Tuladhar

doi:10.1016/j.nicl.2023.103421

Network structure-function coupling and neurocognition in cerebral small vessel disease

Neuroimage Clin. 2023:38:103421. doi: 10.1016/j.nicl.2023.103421. Epub 2023 Apr 28.

Authors

Jonathan Tay¹, Marco Düring², Esther M C van Leijsen³, Mayra I Bergkamp⁴, David G Norris⁵, Frank-Erik de Leeuw⁴, Hugh S Markus¹, Anil M Tuladhar⁶

Affiliations

¹ Stroke Research Group, Department of Clinical Neurosciences, University of Cambridge, Cambridge, UK.
² Medical Image Analysis Center (MIAC AG) and qbig, Department of Biomedical Engineering, University of Basel, Basel, Switzerland.
³ Netherlands Court of Audit, The Hague, the Netherlands.
⁴ Department of Neurology, Donders Center for Medical Neurosciences, Radboud University Nijmegen Medical Centre, Nijmegen, the Netherlands.
⁵ Centre for Cognitive Neuroimaging, Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen, the Netherlands.
⁶ Department of Neurology, Donders Center for Medical Neurosciences, Radboud University Nijmegen Medical Centre, Nijmegen, the Netherlands. Electronic address: Anil.Tuladhar@radboudumc.nl.

Abstract

Background: Cerebral small vessel disease is a leading cause of cognitive decline and vascular dementia. Small vessel disease pathology changes structural brain networks, but its impact on functional networks remains poorly understood. Structural and functional networks are closely coupled in healthy individuals, and decoupling is associated with clinical symptoms in other neurological conditions. We tested the hypothesis that structural-functional network coupling is related to neurocognitive outcomes in 262 small vessel disease patients.

Methods: Participants underwent multimodal magnetic resonance imaging and cognitive assessment in 2011 and 2015. Structural connectivity networks were reconstructed using probabilistic diffusion tractography, while functional connectivity networks were estimated from resting-state functional magnetic resonance imaging. Structural and functional networks were then correlated to calculate a measure of structural-functional network coupling for each participant.

Results: Lower whole-brain coupling was associated with reduced processing speed and greater apathy both cross-sectionally and longitudinally. In addition, coupling within the cognitive control network was associated with all cognitive outcomes, suggesting that neurocognitive outcomes in small vessel disease may be related to the functioning of this intrinsic connectivity network.

Conclusions: Our work demonstrates the influence of structural-functional connectivity network decoupling in small vessel disease symptomatology. Cognitive control network function may be investigated in future studies.

Keywords: Cognition; MRI; Network analysis; Small vessel disease.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Brain
Cerebral Small Vessel Diseases* / complications
Cerebral Small Vessel Diseases* / diagnostic imaging
Cerebral Small Vessel Diseases* / pathology
Cognition
Cognitive Dysfunction* / complications
Cognitive Dysfunction* / etiology
Humans
Magnetic Resonance Imaging

Grants and funding

DH_/Department of Health/United Kingdom