Abstract
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 moyamoya disease (MMD). We used BOLD-fMRI for LRTC analysis from 16 hemorrhagic (HMMD) and 35 ischemic (IMMD) patients, and 26 healthy controls. Besides, 11 HMMD, 13 IMMD, and 21 controls of the cohort completed EEG experiments in the eyes-closed (EC), eyes-open (EO), and working-memory (WM) states. Regarding 4 metrics of neural avalanches, both MMD subtypes exhibited subcritical states in the EC state. When switching to the WM state, HMMD remained inactive, while IMMD 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 (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 exhibited mutually independent but overlapping patterns. The regions showing decreased LRTC in both EEG and fMRI were the left supplemental motor area and dorsolateral prefrontal cortex (DLPFC) of HMMD, and right pre-/postcentral gyrus, right DLPFC, and right inferior temporal gyrus of IMMD. This study not only sheds light on decayed critical dynamics of MMD for the first time, but also confirms different neurophysiological processes of its two subtypes. Funding Statement: National Natural Science Foundation of China under Grant no. 81801155 (to Yu Lei), 81771237 (to Yuxiang Gu), and 81761128011 (to Yuguo Yu), Shanghai Science and Technology Committee support under Grant no. 18511102800 (to Yuxiang Gu) and 16JC1420100 (to Ying Mao), Shanghai Health and Family Planning Commission support under Grant no. 2017BR022 (to Yuxiang Gu), Shanghai Municipal Science and Technology 795 Major Project under Grant no. 2018SHZDZX01 (to Yuguo Yu), program for the Professor of Special Appointment (Eastern Scholar) under Grant no. SHH1140004 (to Yuguo Yu) at Shanghai Institutions of Higher Learning, and Fundamental Research Funds for the Central Universities under Grant no. lzujbky-2015-119 (to Lianchun Yu). Declaration of Interests: The authors declare no competing financial interests. Ethics Approval Statement: This study was approved by the Institutional Review Board in our hospital, and conducted in accordance with the Declaration of Helsinki. Informed consent was signed by all subjects of this study.
Highlights
Moyamoya disease (MMD) is a chronic cerebrovascular disease characterized by progressive stenosis and occlusion of the terminal portion of the bilateral internal carotid arteries and their main branches
Among the subjects who were selected for the EEG analysis, differences of the demographics and cognitive and task performances among the three groups were not significant (p > 0:05)
The criticality theory provides a novel insight into the neuronal dynamics underlying brain disorders
Summary
Moyamoya disease (MMD) is a chronic cerebrovascular disease characterized by progressive stenosis and occlusion of the terminal portion of the bilateral internal carotid arteries and their main branches. According to one published fMRI study of ours, a dynamic measurement of entropy was proposed as an index of the critical dynamics to describe quantitatively the spatiotemporal changes of neural communication in adult MMD [26]. It found that critical dynamics faded in the diseased brain and with disease progression. The other is to investigate whether the two subtypes with a similar extent of cognitive impairment exhibit different neuronal dynamics and generate several features for future rapid and bedside identification of acute cerebral ischemia and hemorrhage
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