Trade-offs among brain structural network characteristics across the cognitive decline process in cerebral small vessel disease.

OBJECTIVES

To investigate the potential trade-offs among brain structural network characteristics across different stages of cognitive impairment in cerebral small vessel disease (CSVD) based on diffusion tensor imaging (DTI).

METHODS

A total of 264 CSVD patients, including 95 patients with non-cognitive impairment (NCI), 142 with mild cognitive impairment (MCI), 27 with vascular dementia (VaD), and 30 healthy controls (HC) underwent cognitive test and brain diffusion magnetic resonance imaging (MRI). The brain structural network was constructed using connections between 90 cortical and subcortical regions. Network characteristics, including sparsity, redundancy, global efficiency (Eg), and local efficiency (Eloc), were calculated.

RESULTS

Sparsity and redundancy significantly declined in the NCI group compared to the HC group. Eg was significantly reduced in the MCI group compared to the NCI group. All network characteristics declined in the VaD group compared to the MCI group. In the NCI group, both sparsity and redundancy were significantly positively correlated with Montreal Cognitive Assessment (MoCA). In the MCI group, there was significant positive correlation between Eg and MoCA. In the VaD group, there was significant negative correlation between Eloc and MoCA. When controlling for sparsity, Eloc exhibited a significant negative correlation with Eg in all three CSVD groups, while redundancy displayed a significant negative correlation with Eg specifically in MCI group.

CONCLUSION

Our study provides evidence for the heterogeneous alterations in brain structural network across different stages of cognitive impairment in CSVD. The disconnection of brain structural network at NCI stage is mainly the loss of redundant connections. The decline of Eg is the vital factor for cognitive impairment at MCI stage. The decline of all network characteristics is the prominent manifestation at VaD stage. Throughout the cognitive decline process in CSVD, there are trade-offs among the brain network wiring cost, integration, and segregation.