Department of Biomedical Engineering, University of Delaware, Newark, Delaware 19713.
Department of Applied Physiology and Kinesiology, University of Florida, Gainesville, Florida 32611.
J Neurosci. 2023 May 10;43(19):3520-3537. doi: 10.1523/JNEUROSCI.1916-22.2023. Epub 2023 Mar 28.
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 (<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.
动态适应是一种调整计划运动动作以适应任务动态变化的错误驱动过程（Shadmehr，2017）。适应的运动计划被整合到记忆中，有助于在重新暴露时表现更好。巩固过程在训练后 15 分钟内开始（Criscimagna-Hemminger 和 Shadmehr，2008），并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，尚未在这个时间尺度上量化 rsFC，也未确定其与适应性行为的关系。我们使用功能磁共振成像（fMRI）兼容的机器人，即 MR-SoftWrist（Erwin 等人，2017），来量化与手腕运动动态适应和随后记忆形成相关的 rsFC，并在混合性别人类参与者的两个任务期间获取 fMRI 来定位感兴趣的大脑网络，并在每个任务前后的三个 10 分钟窗口内量化这些网络中的 rsFC。第二天，我们评估了行为保留情况。我们使用在每个时间窗口中测量的 rsFC 的混合模型来识别与任务表现相关的 rsFC 变化，并使用线性回归来识别 rsFC 与行为之间的关系。在动态适应任务后，皮质-小脑网络内的 rsFC 增加，皮质感觉运动网络内的 rsFC 半球间减少。皮质-小脑网络内的增加是动态适应特有的，因为它们与适应和保留的行为测量相关，表明该网络在巩固过程中具有功能作用。相反，皮质感觉运动网络内 rsFC 的减少与适应和保留无关的运动控制过程相关。通过分析适应后超过 30 分钟发生的静息状态功能连接（rsFC）的变化，已经通过功能磁共振成像（fMRI）研究了运动记忆巩固过程。然而，尚不清楚巩固过程是否可以在动态适应后立即（<15 分钟）检测到。我们使用 fMRI 兼容的手腕机器人定位与皮质-丘脑-小脑（CTC）和皮质感觉运动网络中的动态适应相关的大脑区域，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 变化的不同模式。皮质-小脑网络中 rsFC 的增加是适应和保留特有的，而皮质感觉运动网络中半球间的减少与替代运动控制过程相关，但与记忆形成无关。
