Developmental coupling of cerebral blood flow and fMRI fluctuations in youth

Erica B. Baller; Alessandra M. Valcarcel; Azeez Adebimpe; Aaron Alexander-Bloch; Zaixu Cui; Ruben C. Gur; Raquel E. Gur; Bart L. Larsen; Kristin A. Linn; Carly M. O'Donnell; Adam R. Pines; Armin Raznahan; David R. Roalf; Valerie J. Sydnor; Tinashe M. Tapera; M. Dylan Tisdall; Simon Vandekar; Cedric H. Xia; John A. Detre; Russell T. Shinohara; Theodore D. Satterthwaite

doi:10.1016/j.celrep.2022.110576

Developmental coupling of cerebral blood flow and fMRI fluctuations in youth

Erica B. Baller, Alessandra M. Valcarcel, Azeez Adebimpe, Aaron Alexander-Bloch, Zaixu Cui, Ruben C. Gur, Raquel E. Gur, Bart L. Larsen, Kristin A. Linn, Carly M. O'Donnell, Adam R. Pines, Armin Raznahan, David R. Roalf, Valerie J. Sydnor, Tinashe M. Tapera, M. Dylan Tisdall, Simon Vandekar, Cedric H. Xia, John A. Detre, Russell T. ShinoharaTheodore D. Satterthwaite

Research output: Contribution to journal › Article › peer-review

25 Scopus citations

Abstract

The functions of the human brain are metabolically expensive and reliant on coupling between cerebral blood flow (CBF) and neural activity, yet how this coupling evolves over development remains unexplored. Here, we examine the relationship between CBF, measured by arterial spin labeling, and the amplitude of low-frequency fluctuations (ALFF) from resting-state magnetic resonance imaging across a sample of 831 children (478 females, aged 8–22 years) from the Philadelphia Neurodevelopmental Cohort. We first use locally weighted regressions on the cortical surface to quantify CBF-ALFF coupling. We relate coupling to age, sex, and executive functioning with generalized additive models and assess network enrichment via spin testing. We demonstrate regionally specific changes in coupling over age and show that variations in coupling are related to biological sex and executive function. Our results highlight the importance of CBF-ALFF coupling throughout development; we discuss its potential as a future target for the study of neuropsychiatric diseases.

Original language	English (US)
Article number	110576
Journal	Cell reports
Volume	38
Issue number	13
DOIs	https://doi.org/10.1016/j.celrep.2022.110576
State	Published - Mar 29 2022
Externally published	Yes

Bibliographical note

Publisher Copyright:
© 2022 The Authors

Keywords

CP: Neuroscience
adolescence
amplitude of low-frequency fluctuations
cerebral blood flow
development
executive function
frontoparietal
neurovascular coupling
sex differences

PubMed: MeSH publication types

Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

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10.1016/j.celrep.2022.110576

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Baller, E. B., Valcarcel, A. M., Adebimpe, A., Alexander-Bloch, A., Cui, Z., Gur, R. C., Gur, R. E., Larsen, B. L., Linn, K. A., O'Donnell, C. M., Pines, A. R., Raznahan, A., Roalf, D. R., Sydnor, V. J., Tapera, T. M., Tisdall, M. D., Vandekar, S., Xia, C. H., Detre, J. A., ... Satterthwaite, T. D. (2022). Developmental coupling of cerebral blood flow and fMRI fluctuations in youth. Cell reports, 38(13), Article 110576. https://doi.org/10.1016/j.celrep.2022.110576

Baller, EB, Valcarcel, AM, Adebimpe, A, Alexander-Bloch, A, Cui, Z, Gur, RC, Gur, RE, Larsen, BL, Linn, KA, O'Donnell, CM, Pines, AR, Raznahan, A, Roalf, DR, Sydnor, VJ, Tapera, TM, Tisdall, MD, Vandekar, S, Xia, CH, Detre, JA, Shinohara, RT & Satterthwaite, TD 2022, 'Developmental coupling of cerebral blood flow and fMRI fluctuations in youth', Cell reports, vol. 38, no. 13, 110576. https://doi.org/10.1016/j.celrep.2022.110576

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abstract = "The functions of the human brain are metabolically expensive and reliant on coupling between cerebral blood flow (CBF) and neural activity, yet how this coupling evolves over development remains unexplored. Here, we examine the relationship between CBF, measured by arterial spin labeling, and the amplitude of low-frequency fluctuations (ALFF) from resting-state magnetic resonance imaging across a sample of 831 children (478 females, aged 8–22 years) from the Philadelphia Neurodevelopmental Cohort. We first use locally weighted regressions on the cortical surface to quantify CBF-ALFF coupling. We relate coupling to age, sex, and executive functioning with generalized additive models and assess network enrichment via spin testing. We demonstrate regionally specific changes in coupling over age and show that variations in coupling are related to biological sex and executive function. Our results highlight the importance of CBF-ALFF coupling throughout development; we discuss its potential as a future target for the study of neuropsychiatric diseases.",

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AU - Valcarcel, Alessandra M.

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AU - Cui, Zaixu

AU - Gur, Ruben C.

AU - Gur, Raquel E.

AU - Larsen, Bart L.

AU - Linn, Kristin A.

AU - O'Donnell, Carly M.

AU - Pines, Adam R.

AU - Raznahan, Armin

AU - Roalf, David R.

AU - Sydnor, Valerie J.

AU - Tapera, Tinashe M.

AU - Tisdall, M. Dylan

AU - Vandekar, Simon

AU - Xia, Cedric H.

AU - Detre, John A.

AU - Shinohara, Russell T.

AU - Satterthwaite, Theodore D.

PY - 2022/3/29

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N2 - The functions of the human brain are metabolically expensive and reliant on coupling between cerebral blood flow (CBF) and neural activity, yet how this coupling evolves over development remains unexplored. Here, we examine the relationship between CBF, measured by arterial spin labeling, and the amplitude of low-frequency fluctuations (ALFF) from resting-state magnetic resonance imaging across a sample of 831 children (478 females, aged 8–22 years) from the Philadelphia Neurodevelopmental Cohort. We first use locally weighted regressions on the cortical surface to quantify CBF-ALFF coupling. We relate coupling to age, sex, and executive functioning with generalized additive models and assess network enrichment via spin testing. We demonstrate regionally specific changes in coupling over age and show that variations in coupling are related to biological sex and executive function. Our results highlight the importance of CBF-ALFF coupling throughout development; we discuss its potential as a future target for the study of neuropsychiatric diseases.

AB - The functions of the human brain are metabolically expensive and reliant on coupling between cerebral blood flow (CBF) and neural activity, yet how this coupling evolves over development remains unexplored. Here, we examine the relationship between CBF, measured by arterial spin labeling, and the amplitude of low-frequency fluctuations (ALFF) from resting-state magnetic resonance imaging across a sample of 831 children (478 females, aged 8–22 years) from the Philadelphia Neurodevelopmental Cohort. We first use locally weighted regressions on the cortical surface to quantify CBF-ALFF coupling. We relate coupling to age, sex, and executive functioning with generalized additive models and assess network enrichment via spin testing. We demonstrate regionally specific changes in coupling over age and show that variations in coupling are related to biological sex and executive function. Our results highlight the importance of CBF-ALFF coupling throughout development; we discuss its potential as a future target for the study of neuropsychiatric diseases.

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Developmental coupling of cerebral blood flow and fMRI fluctuations in youth

Abstract

Bibliographical note

Keywords

PubMed: MeSH publication types

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