Faded Critical Dynamics in Adult Moyamoya Disease Revealed by EEG and fMRI

Criticality is considered a dynamic signature of healthy brain activity that can be measured on the short-term timescale with neural avalanches and long-term timescale with long-range temporal correlation (LRTC). It is unclear how the brain dynamics change in adult moyamoya disease (MMD). We used BOLD-fMRI for LRTC analysis from 16 hemorrhagic (H(MMD)) and 34 ischemic (I(MMD)) patients and 25 healthy controls. Afterwards, they were examined by EEG recordings in the eyes-closed (EC), eyes-open (EO), and working memory (WM) states. The EEG data of 11 H(MMD) and 13 I(MMD) patients and 21 healthy controls were in good quality for analysis. Regarding the 4 metrics of neural avalanches (e.g., size (α), duration (β), κ value, and branching parameter (σ)), both MMD subtypes exhibited subcritical states in the EC state. When switching to the WM state, H(MMD) remained inactive, while I(MMD) surpassed controls and became supercritical (p < 0.05). Regarding LRTC, the amplitude envelope in the EC state was more analogous to random noise in the MMD patients than in controls. During state transitions, LRTC decreased sharply in the controls but remained chaotic in the MMD individuals (p < 0.05). The spatial LRTC reduction distribution based on both EEG and fMRI in the EC state implied that, compared with controls, the two MMD subtypes might exhibit mutually independent but partially overlapping patterns. The regions showing decreased LRTC in both EEG and fMRI were the left supplemental motor area of H(MMD) and right pre-/postcentral gyrus and right inferior temporal gyrus of I(MMD). This study not only sheds light on the decayed critical dynamics of MMD in both the resting and task states for the first time but also proposes several EEG and fMRI features to identify its two subtypes.