Direct, intraoperative observation of ~0.1Hz hemodynamic oscillations in awake human cortex: Implications for fMRI

Aleksandr Rayshubskiy, Teresa J. Wojtasiewicz, Charles B. Mikell, Matthew B. Bouchard, Dmitriy Timerman, Brett E. Youngerman, Robert A. McGovern, Marc L. Otten, Peter Canoll, Guy M. McKhann, Elizabeth M.C. Hillman

Research output: Contribution to journalArticlepeer-review

45 Scopus citations

Abstract

An almost sinusoidal, large amplitude ~. 0.1. Hz oscillation in cortical hemodynamics has been repeatedly observed in species ranging from mice to humans. However, the occurrence of 'slow sinusoidal hemodynamic oscillations' (SSHOs) in human functional magnetic resonance imaging (fMRI) studies is rarely noted or considered. As a result, little investigation into the cause of SSHOs has been undertaken, and their potential to confound fMRI analysis, as well as their possible value as a functional biomarker has been largely overlooked.Here, we report direct observation of large-amplitude, sinusoidal ~. 0.1. Hz hemodynamic oscillations in the cortex of an awake human undergoing surgical resection of a brain tumor. Intraoperative multispectral optical intrinsic signal imaging (MS-OISI) revealed that SSHOs were spatially localized to distinct regions of the cortex, exhibited wave-like propagation, and involved oscillations in the diameter of specific pial arterioles, indicating that the effect was not the result of systemic blood pressure oscillations. fMRI data collected from the same subject 4. days prior to surgery demonstrates that ~. 0.1. Hz oscillations in the BOLD signal can be detected around the same region. Intraoperative optical imaging data from a patient undergoing epilepsy surgery, in whom sinusoidal oscillations were not observed, is shown for comparison.This direct observation of the '0.1. Hz wave' in the awake human brain, using both intraoperative imaging and pre-operative fMRI, confirms that SSHOs occur in the human brain, and can be detected by fMRI. We discuss the possible physiological basis of this oscillation and its potential link to brain pathologies, highlighting its relevance to resting-state fMRI and its potential as a novel target for functional diagnosis and delineation of neurological disease.

Original languageEnglish (US)
Pages (from-to)323-331
Number of pages9
JournalNeuroImage
Volume87
DOIs
StatePublished - Feb 5 2014
Externally publishedYes

Bibliographical note

Funding Information:
We thank Drs. Catherine Schevon, Angela Lignelli-Dipple, Jack Grinband, Sameer Sheth, John Sheehy, Hani Malone, Daniel Stoyanov, Daniel Chow, Mariel Kozberg and Jason Berwick for helpful discussions; Drs. Michael Sisti and Jeffrey Bruce, Columbia University neurosurgery residents, and neurosurgical operating room staff for their help in collecting the data; Keith Yeager for machining assistance; and members of the Laboratory for Functional Optical Imaging for their support and helpful discussions. We acknowledge support from National Institutes of Health : UL1 RR024156 , National Center for Advancing Translational Sciences , Irving Institute CTSA , National Institute of Neurological Disorders and Stroke , 1R01NS063226 , 1R01NS076628 , and R21NS053684 (to E.M.C.H.); National Science Foundation Grants CAREER 0954796 (to E.M.C.H.); Graduate Fellowship (M.B.B.); National Defense Science and Engineering Graduate Fellowship (to M.B.B.), Doris Duke Foundation research fellowship (T.J.W.); the Human Frontier Science Program and the Kavli Foundation .

Keywords

  • 0.1Hz oscillation
  • Cerebral hemodynamics
  • FMRI
  • Intraoperative optical imaging
  • Resting state
  • Vasomotion

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