title: Direct, intraoperative observation of ~0.1 Hz hemodynamic oscillations in awake human cortex: implications for fMRI.
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.
authors.affiliation: Laboratory for Functional Optical Imaging, Department of Biomedical Engineering, Columbia University, USA.
authors.forename: Aleksandr
authors.initials: A
authors.lastname: Rayshubskiy
authors.affiliation: Department of Neurosurgery, Columbia University, USA.
authors.forename: Teresa J
authors.initials: TJ
authors.lastname: Wojtasiewicz
authors.affiliation: Department of Neurosurgery, Columbia University, USA.
authors.forename: Charles B
authors.initials: CB
authors.lastname: Mikell
authors.affiliation: Laboratory for Functional Optical Imaging, Department of Biomedical Engineering, Columbia University, USA.
authors.forename: Matthew B
authors.initials: MB
authors.lastname: Bouchard
authors.affiliation: Laboratory for Functional Optical Imaging, Department of Biomedical Engineering, Columbia University, USA.
authors.forename: Dmitriy
authors.initials: D
authors.lastname: Timerman
authors.affiliation: Department of Neurosurgery, Columbia University, USA.
authors.forename: Brett E
authors.initials: BE
authors.lastname: Youngerman
authors.affiliation: Department of Neurosurgery, Columbia University, USA.
authors.forename: Robert A
authors.initials: RA
authors.lastname: McGovern
authors.affiliation: Department of Neurosurgery, Columbia University, USA.
authors.forename: Marc L
authors.initials: ML
authors.lastname: Otten
authors.affiliation: Department of Pathology and Cell Biology, Columbia University, USA.
authors.forename: Peter
authors.initials: P
authors.lastname: Canoll
authors.affiliation: Department of Neurosurgery, Columbia University, USA.
authors.forename: Guy M
authors.initials: GM
authors.lastname: McKhann
authors.affiliation: Laboratory for Functional Optical Imaging, Department of Biomedical Engineering, Columbia University, USA; Department of Radiology, Columbia University, USA. Electronic address: eh2245@columbia.edu.
authors.forename: Elizabeth M C
authors.initials: EM
authors.lastname: Hillman
mesh_terms: D000328:Adult; D002540:Cerebral Cortex / Q000098:blood supply* / Q000502:physiology*; D002560:Cerebrovascular Circulation / Q000502:physiology; D005260:Female; D006439:Hemodynamics / Q000502:physiology*; D006801:Humans; D007091:Image Processing, Computer-Assisted; D064795:Intraoperative Neurophysiological Monitoring; D008279:Magnetic Resonance Imaging; D008297:Male; D061848:Optical Imaging / Q000379:methods; D014851:Wakefulness
keywords: 0.1Hz oscillation; Cerebral hemodynamics; Intraoperative optical imaging; Resting state; Vasomotion; fMRI