Changes in Resting State Functional Connectivity Associated with Dynamic Adaptation of Wrist Movements

• Published in: The Journal of neuroscience 2023-05, Vol.43 (19), p.3520-3537
• Main Authors: Farrens, Andria J, Vahdat, Shahabeddin, Sergi, Fabrizio
• Format: Article
• Language: English
• Subjects: Adaptation; Behavior; Brain - diagnostic imaging; Brain mapping; Brain Mapping - methods; Cerebellum; Consolidation; Functional magnetic resonance imaging; Humans; Magnetic resonance imaging; Magnetic Resonance Imaging - methods; Motor task performance; Movement; Neural networks; Neuroimaging; Retention; Sensorimotor system; Wrist; Wrist - diagnostic imaging
• ISSN: 0270-6474; 1529-2401
• DOI: 10.1523/JNEUROSCI.1916-22.2023

Dynamic adaptation is an error-driven process of adjusting planned motor actions to changes in task dynamics (Shadmehr, 2017). Adapted motor plans are consolidated into memories that contribute to better performance on re-exposure. Consolidation begins within 15 min following training (Criscimagna-Hemminger and Shadmehr, 2008), and can be measured via changes in resting state functional connectivity (rsFC). For dynamic adaptation, rsFC has not been quantified on this timescale, nor has its relationship to adaptative behavior been established. We used a functional magnetic resonance imaging (fMRI)-compatible robot, the MR-SoftWrist (Erwin et al., 2017), to quantify rsFC specific to dynamic adaptation of wrist movements and subsequent memory formation in a mixed-sex cohort of human participants. We acquired fMRI during a motor execution and a dynamic adaptation task to localize brain networks of interest, and quantified rsFC within these networks in three 10-min windows occurring immediately before and after each task. The next day, we assessed behavioral retention. We used a mixed model of rsFC measured in each time window to identify changes in rsFC with task performance, and linear regression to identify the relationship between rsFC and behavior. Following the dynamic adaptation task, rsFC increased within the cortico-cerebellar network and decreased interhemispherically within the cortical sensorimotor network. Increases within the cortico-cerebellar network were specific to dynamic adaptation, as they were associated with behavioral measures of adaptation and retention, indicating that this network has a functional role in consolidation. Instead, decreases in rsFC within the cortical sensorimotor network were associated with motor control processes independent from adaptation and retention. Motor memory consolidation processes have been studied via functional magnetic resonance imaging (fMRI) by analyzing changes in resting state functional connectivity (rsFC) occurring more than 30 min after adaptation. However, it is unknown whether consolidation processes are detectable immediately (