Bangor Imaging Unit, Bangor University, Bangor, Wales LL57 2AS, United Kingdom.
Centre for Human Brain Health, School of Psychology, University of Birmingham, Birmingham, B15 2TT, United Kingdom.
J Neurosci. 2023 Mar 8;43(10):1742-1756. doi: 10.1523/JNEUROSCI.1628-22.2023. Epub 2023 Feb 1.
Performing sequences of movements from memory and adapting them to changing task demands is a hallmark of skilled human behavior, from handwriting to playing a musical instrument. Prior studies showed a fine-grained tuning of cortical primary motor, premotor, and parietal regions to motor sequences: from the low-level specification of individual movements to high-level sequence features, such as sequence order and timing. However, it is not known how tuning in these regions unfolds dynamically across planning and execution. To address this, we trained 24 healthy right-handed human participants (14 females, 10 males) to produce four five-element finger press sequences with a particular finger order and timing structure in a delayed sequence production paradigm entirely from memory. Local cortical fMRI patterns during preparation and production phases were extracted from separate No-Go and Go trials, respectively, to tease out activity related to these perimovement phases. During sequence planning, premotor and parietal areas increased tuning to movement order or timing, regardless of their combinations. In contrast, patterns reflecting the unique integration of sequence features emerged in these regions during execution only, alongside timing-specific tuning in the ventral premotor, supplementary motor, and superior parietal areas. This was in line with the participants' behavioral transfer of trained timing, but not of order to new sequence feature combinations. Our findings suggest a general informational state shift from high-level feature separation to low-level feature integration within cortical regions for movement execution. Recompiling sequence features trial-by-trial during planning may enable flexible last-minute adjustment before movement initiation. Musicians and athletes can modify the timing and order of movements in a sequence trial-by-trial, allowing for a vast repertoire of flexible behaviors. How does the brain put together these high-level sequence features into an integrated whole? We found that, trial-by-trial, the control of sequence features undergoes a state shift from separation during planning to integration during execution across a network of motor-related cortical areas. These findings have implications for understanding the hierarchical control of skilled movement sequences, as well as how information in brain areas unfolds across planning and execution.
从手写到演奏乐器，从记忆中执行动作序列并根据任务需求进行调整是人类熟练行为的标志。先前的研究表明，大脑初级运动皮层、运动前区和顶叶区域对运动序列进行了精细的调整：从单个运动的低水平特征到高水平序列特征，例如序列顺序和时间。然而，这些区域的调整在计划和执行过程中是如何动态展开的尚不清楚。为了解决这个问题，我们在延迟序列产生范式中训练了 24 名健康的右利手人类参与者（14 名女性，10 名男性），完全从记忆中产生四个具有特定手指顺序和时间结构的五个元素手指按压序列。在准备和产生阶段，从单独的 No-Go 和 Go 试验中提取局部皮质 fMRI 模式，以分别梳理与这些运动前阶段相关的活动。在序列规划期间，运动前区和顶叶区域增加了对运动顺序或时间的调整，无论它们的组合如何。相比之下，在执行过程中，仅在这些区域中才会出现反映序列特征独特整合的模式，同时在腹侧运动前区、补充运动区和上顶叶区中出现特定于时间的调整。这与参与者将训练有素的时间转移到新的序列特征组合上的行为一致，但顺序则不然。我们的发现表明，在运动执行过程中，皮质区域中的信息状态从高级特征分离转变为低级特征整合。在计划过程中逐次重新编译序列特征可能会在运动开始前允许进行灵活的最后一分钟调整。音乐家和运动员可以在序列试验中逐次修改运动的时间和顺序，从而实现灵活行为的广泛表现。大脑如何将这些高级序列特征组合成一个整体？我们发现，在逐次试验中，序列特征的控制在运动相关皮质区域网络中从规划期间的分离状态转变为执行期间的整合状态。这些发现对于理解熟练运动序列的层次控制以及大脑区域中的信息在计划和执行过程中的展开方式具有重要意义。
