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Distance from main arteries influences microstructural and functional brain tissue characteristics

V. Weiss, V. Kokošová, Z. Valenta, I. Doležalová, M. Baláž, S. Mangia, S. Michaeli, L. Vojtíšek, I. Nestrašil, R. Herzig, P. Filip

. 2024 ; 285 (-) : 120502. [pub] 20231214

Language English Country United States

Document type Journal Article

Persistent link   https://www.medvik.cz/link/bmc24007737

Grant support
P41 EB027061 NIBIB NIH HHS - United States

Given the substantial dependence of neurons on continuous supply of energy, the distribution of major cerebral arteries opens a question whether the distance from the main supply arteries constitutes a modulating factor for the microstructural and functional properties of brain tissue. To tackle this question, multimodal MRI acquisitions of 102 healthy volunteers over the full adult age span were utilised. Relaxation along a fictitious field in the rotating frame of rank n = 4 (RAFF4), adiabatic T1ρ, T2ρ, and intracellular volume fraction (fICVF) derived from diffusion-weighted imaging were implemented to quantify microstructural (cellularity, myelin density, iron concentration) tissue characteristics and degree centrality and fractional amplitude of low-frequency fluctuations to probe for functional metrics. Inverse correlation of arterial distance with robust homogeneity was detected for T1ρ, T2ρ and RAFF4 for cortical grey matter and white matter, showing substantial complex microstructural differences between brain tissue close and farther from main arterial trunks. Albeit with wider variability, functional metrics pointed to increased connectivity and neuronal activity in areas farther from main arteries. Surprisingly, multiple of these microstructural and functional distance-based gradients diminished with higher age, pointing to uniformization of brain tissue with ageing. All in all, this pilot study provides a novel insight on brain regionalisation based on artery distance, which merits further investigation to validate its biological underpinnings.

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$a Given the substantial dependence of neurons on continuous supply of energy, the distribution of major cerebral arteries opens a question whether the distance from the main supply arteries constitutes a modulating factor for the microstructural and functional properties of brain tissue. To tackle this question, multimodal MRI acquisitions of 102 healthy volunteers over the full adult age span were utilised. Relaxation along a fictitious field in the rotating frame of rank n = 4 (RAFF4), adiabatic T1ρ, T2ρ, and intracellular volume fraction (fICVF) derived from diffusion-weighted imaging were implemented to quantify microstructural (cellularity, myelin density, iron concentration) tissue characteristics and degree centrality and fractional amplitude of low-frequency fluctuations to probe for functional metrics. Inverse correlation of arterial distance with robust homogeneity was detected for T1ρ, T2ρ and RAFF4 for cortical grey matter and white matter, showing substantial complex microstructural differences between brain tissue close and farther from main arterial trunks. Albeit with wider variability, functional metrics pointed to increased connectivity and neuronal activity in areas farther from main arteries. Surprisingly, multiple of these microstructural and functional distance-based gradients diminished with higher age, pointing to uniformization of brain tissue with ageing. All in all, this pilot study provides a novel insight on brain regionalisation based on artery distance, which merits further investigation to validate its biological underpinnings.
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$a Valenta, Zdeněk $u Department of Statistical Modelling, Institute of Computer Science of the Czech Academy of Sciences, Prague, Czech Republic
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$a Baláž, Marek $u First Department of Neurology, Faculty of Medicine, Masaryk University and University Hospital of St. Anne, Brno, Czech Republic
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$a Filip, Pavel $u Center for Magnetic Resonance Research (CMRR), University of Minnesota, Minneapolis, MN, United States of America; Department of Neurology, Charles University, First Faculty of Medicine and General University Hospital, Prague, Czech Republic. Electronic address: pvlfilip@gmail.com
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