Neurovascular coupling alterations related to cognitive impairment in cerebral small vessel disease: A multiscale brain network perspective

Abstract

Evidence suggests that neurovascular coupling (NVC) dysfunction in cerebral small vessel disease (CSVD) may precede typical clinical and imaging manifestations. Here, we explored the underlying brain alterations of multiscale networks in CSVD patients related to cognitive impairment based on the method of NVC. We investigated 124 CSVD patients, including 70 patients with mild cognitive impairment (MCI) and 54 patients with no cognitive impairment (NCI). Functional MRI and arterial spin labeling were employed to estimate the coupling of spontaneous neuronal activity and cerebral blood perfusion based on the regional homogeneity and cerebral blood flow at the whole-brain, modular, and regional levels. We showed that the NVC of the dorsal attention network (DOR), ventral attention network (VEN) and default mode network (DMN) in the MCI were significantly lower than those in the NCI. The NVC of the DOR, VEN, and DMN in the NCI group exhibited correlations with the executive function. Furthermore, mediation effect of CSVD lesion load was observed for the association between NVC alterations and cognitive function. The abnormal NVC features achieved effective classification performance for MCI and NCI. These findings underscore the significance of specific modular and regional NVC dysfunction in the cognitive outcomes of CSVD. This study revealed the potential of NVC as a focal point for future research on cognitive impairment in CSVD, particularly from the perspective of multiscale brain network analysis.