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, confirming 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.

Detailed view on slow sinusoidal, hemodynamic oscillations on the human brain cortex by Fourier transforming oxy/deoxy hyperspectral images

“…In contrast to Rayshubskiy et al (Rayshubskiy et al, 2014) who did not find strong HbR oscillations, we see strong HbR oscillations for all 4 patients (Figure 8). On average, the amplitude of the HbR SSHO is only 11% smaller than that of HbO SSHO.…”

“…Instead of applying a relatively wide bandpass filter, where all oscillations are aggregated (Bumstead et al, 2016; Gratton et al, 1998; Zuo et al, 2010), or only looking at only one frequency of 0.1 Hz (Rayshubskiy et al, 2014), a more detailed view on a SSHO can be acquired using a very small bandwidth ( $\Delta f$ around 0.002 Hz) as with a Fourier transform. In this way, it becomes clear that different but also overlapping SSHO‐regions can be observed with slightly different SSHO frequencies.…”

“…Instead of cross‐correlating signals to image wave propagation (Rayshubskiy et al, 2014), we used the phase part of the Fourier transform to estimate the SSHO phase variation within a region. The phase was continuous within a SSHO‐region, indicating that the phase can be determined robustly across the region.…”

“…Although our analysis gives new insight in the characteristics of SSHOs (distinct regions and various stable frequencies), several questions remain to be answered: It has been hypothesized that SSHOs are linked to pathology (Rayshubskiy et al, 2014) and that tissue in stress can produce SSHOs. We think that stress may indeed play a role, but it is a factor that is difficult to measure.…”

“…This method can be used to directly observe SSHOs on the human cortex itself. Due to the invasive character of having to remove the skull and dura, direct SSHO observations have been only sporadically described (Mitra, Ogawa, Hu, & Uǧurbil, 1997; Obrig et al, 2000; Rayshubskiy et al, 2014). …”