Age-related unstable transient states and imbalanced activation proportion of brain networks in people with autism spectrum disorder: A resting-state fMRI study using coactivation pattern analyses

Yunge Zhang; Lin Lin; Dongyue Zhou; Yang Song; Abigail Stein; Shuqin Zhou; Huashuai Xu; Wei Zhao; Fengyu Cong; Jin Sun; Huanjie Li; Fei Du

doi:10.1162/netn_a_00396

Age-related unstable transient states and imbalanced activation proportion of brain networks in people with autism spectrum disorder: A resting-state fMRI study using coactivation pattern analyses

Netw Neurosci. 2024 Dec 10;8(4):1173-1191. doi: 10.1162/netn_a_00396. eCollection 2024.

Authors

Yunge Zhang^{1

2}, Lin Lin², Dongyue Zhou^{2

3}, Yang Song¹, Abigail Stein⁴, Shuqin Zhou⁴, Huashuai Xu², Wei Zhao⁵, Fengyu Cong^{2

6

7}, Jin Sun⁸, Huanjie Li^{1

2}, Fei Du^{4

9}

Affiliations

¹ Central Hospital of Dalian University of Technology, Dalian, China.
² School of Biomedical Engineering, Faculty of Medicine, Dalian University of Technology, Dalian, China.
³ Department of Cognitive Neuroscience, Donders Institute for Brain, Cognition, and Behaviour, Radboud University Medical Centre, Nijmegen, The Netherlands.
⁴ McLean Imaging Center, McLean Hospital, Harvard Medical School, Belmont, MA, USA.
⁵ School of Software, Henan Polytechnic University, Jiaozuo, China.
⁶ Faculty of Information Technology, University of Jyväskylä, Jyväskylä, Finland.
⁷ Key Laboratory of Social Computing and Cognitive Intelligence (Dalian University of Technology), Ministry of Education, Dalian, China.
⁸ Dalian Woman and Children's Medical Group, Dalian, China.
⁹ Psychotic Disorders Division, McLean Hospital, Harvard Medical School, Belmont, MA, USA.

Abstract

The atypical static brain functions related to the executive control network (ECN), default mode network (DMN), and salience network (SN) in people with autism spectrum disorder (ASD) has been widely reported. However, their transient functions in ASD are not clear. We aim to identify transient network states (TNSs) using coactivation pattern (CAP) analysis to characterize the age-related atypical transient functions in ASD. CAP analysis was performed on a resting-state fMRI dataset (78 ASD and 78 healthy control (CON) juveniles, 54 ASD and 54 CON adults). Six TNSs were divided into the DMN-TNSs, ECN-TNSs, and SN-TNSs. The DMN-TNSs were major states with the highest stability and proportion, and the ECN-TNSs and SN-TNSs were minor states. Age-related abnormalities on spatial stability and TNS proportion were found in ASD. The spatial stability of DMN-TNSs was found increasing with age in CON, but was not found in ASD. A lower proportion of DMN-TNSs was found in ASD compared with CON of the same age, and ASD juveniles had a higher proportion of SN-TNSs while ASD adults had a higher proportion of ECN-TNSs. The abnormalities on spatial stability and TNS proportion were related to social deficits. Our results provided new evidence for atypical transient brain functions in people with ASD.

Keywords: Autism spectrum disorder; Coactivation pattern; Default model network; Resting-state functional MRI; Triple network model.

Plain language summary

This article reveals the age-related atypical transient brain functions in autistic people. The default mode network dominates major states during rest, while the executive control network and salience network dominates minor states. Major states have more a stable coactivation patterns and higher proportion than minor states. The spatial stability would increase with age in healthy controls but not in autistic people. Meanwhile, autistic people spend less time on major states but more time on minor states. In addition, the unstable transient states and imbalanced activation proportion of brain networks are correlated with the social deficits. Although this work is limited by that single scanning data of only involving male participants with normal intelligence, it provides new transient aspect for atypical brain function in autistic people.