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Changes in Resting State Functional Connectivity Associated with Dynamic Adaptation of Wrist Movements
Journal of Neuroscience ( IF 5.3 ) Pub Date : 2023-05-10 , DOI: 10.1523/jneurosci.1916-22.2023
Andria J Farrens 1 , Shahabeddin Vahdat 2 , Fabrizio Sergi 3
Affiliation  

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.

SIGNIFICANCE STATEMENT 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 (<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 (CTC) and cortical sensorimotor networks and quantified changes in rsFC within each network immediately after adaptation. Different patterns of change in rsFC were observed compared with 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.



中文翻译:

与手腕运动动态适应相关的静息状态功能连接的变化

动态适应是一个错误驱动的过程,根据任务动态的变化调整计划的运动动作(沙德梅尔,2017)。适应的运动计划被整合到记忆中,有助于在重新暴露时获得更好的表现。训练后 15 分钟内开始巩固(Cricimagna-Hemminger 和 Shadmehr,2008),并且可以通过静息状态功能连接(rsFC)的变化来测量。对于动态适应,rsFC 尚未在该时间尺度上量化,也未建立其与适应行为的关系。我们使用了功能性磁共振成像 (fMRI) 兼容机器人 MR-SoftWrist (欧文等人,2017),量化混合性别人类参与者中手腕运动动态适应和随后记忆形成的 rsFC。我们在运动执行和动态适应任务期间获取了功能磁共振成像,以定位感兴趣的大脑网络,并在每个任务之前和之后立即发生的三个 10 分钟窗口中量化这些网络内的 rsFC。第二天,我们评估了行为保留。我们使用在每个时间窗口测量的 rsFC 混合模型来识别 rsFC 随任务表现的变化,并使用线性回归来识别 rsFC 和行为之间的关系。动态适应任务后,皮质小脑网络内的 rsFC 增加,皮质感觉运动网络内的半球间减少。皮质小脑网络内的增加是动态适应所特有的,因为它们与适应和保留的行为测量相关,表明该网络在巩固中具有功能性作用。相反,皮质感觉运动网络内 rsFC 的减少与独立于适应和保留的运动控制过程相关。

意义声明通过功能磁共振成像 (fMRI),通过分析适应后 30 分钟以上发生的静息态功能连接 (rsFC) 的变化,研究了运动记忆巩固过程。然而,尚不清楚动态适应后是否可以立即(<15 分钟)检测到巩固过程。我们使用兼容 fMRI 的腕部机器人来定位参与皮质-丘脑-小脑 (CTC) 和皮质感觉运动网络动态适应的大脑区域,并在适应后立即量化每个网络内 rsFC 的变化。与在较长潜伏期进行的研究相比,观察到 rsFC 的不同变化模式。皮质小脑网络中 rsFC 的增加与适应和保留有关,而皮质感觉运动网络中半球间的减少与交替运动控制过程相关,但与记忆形成无关。

更新日期:2023-05-11
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