Changes in resting state functional connectivity associated with dynamic adaptation of wrist movements.
Andria J FarrensShahabeddin VahdatFabrizio SergiPublished in: The Journal of neuroscience : the official journal of the Society for Neuroscience (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 minutes following training (Criscimagna-Hemminger & 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 an 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-minute 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. SIGNIFICANCE STATEMENT: Motor memory consolidation processes have been studied via fMRI by analyzing changes in resting state functional connectivity (rsFC) occurring more than 30 min after adaptation. However, it is unknown if consolidation processes are detectable immediately (<15 min) following dynamic adaptation. We used an fMRI-compatible wrist robot to localize brain regions involved in dynamic adaptation in the cortico-thalamic-cerebellar and cortical sensorimotor networks and quantified changes in rsFC within each network immediately after adaptation. Different patterns of change in rsFC were observed compared to studies conducted at longer latencies. Increases in rsFC in the cortico-cerebellar network were specific to adaptation and retention, while interhemispheric decreases in the cortical sensorimotor network were associated with alternate motor control processes but not with memory formation.