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Edited by Marcus E. Raichle, Washington University in St. Louis, St. Louis, MO, and approved December 5, 2017 (received for review June 28, 2017)
Significance
Functional MRI has been widely used to assess the functional architecture of the brain based on detecting changes in neural activity in gray matter via blood oxygenation level-dependent (BOLD) effects. However, the existence and possible relevance of BOLD signals in white matter remain controversial. We demonstrate that BOLD signals in functional cortical volumes are strongly correlated with signals in specific, segmented white matter tracts in a resting state, and the correlations can be modulated by specific functional loadings. We therefore show that current concepts of functional connectivity based on synchronous BOLD correlations may be extended to include white matter and that changes in neural activity are encoded in BOLD variations throughout the brain.
Abstract
Functional MRI based on blood oxygenation level-dependent (BOLD) contrast is well established as a neuroimaging technique for detecting neural activity in the cortex of the human brain. While detection and characterization of BOLD signals, as well as their electrophysiological and hemodynamic/metabolic origins, have been extensively studied in gray matter (GM), the detection and interpretation of BOLD signals in white matter (WM) remain controversial. We have previously observed that BOLD signals in a resting state reveal structure-specific anisotropic temporal correlations in WM and that external stimuli alter these correlations and permit visualization of task-specific fiber pathways, suggesting variations in WM BOLD signals are related to neural activity. In this study, we provide further strong evidence that BOLD signals in WM reflect neural activities both in a resting state and under functional loading. We demonstrate that BOLD signal waveforms in stimulus-relevant WM pathways are synchronous with the applied stimuli but with various degrees of time delay and that signals in WM pathways exhibit clear task specificity. Furthermore, resting-state signal fluctuations in WM tracts show significant correlations with specific parcellated GM volumes. These observations support the notion that neural activities are encoded in WM circuits similarly to cortical responses.
Footnotes
- ↵1To whom correspondence should be addressed. Email: zhaohua.ding{at}vanderbilt.edu.
Author contributions: Z.D., L.E.C., and J.C.G. designed research; Z.D., Y.H., and S.K.B. performed research; Y.H., Y.G., B.P.R., and A.T.N. analyzed data; and Z.D. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1711567115/-/DCSupplemental.
Published under the PNAS license.
References
Detection of neural activity in brain white matter
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