Behavioral and neural markers of serial order and timing in skilled motor sequences during planning

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  • Myrto Mantziara

    Research areas

  • Motor sequence planning, serial order, timing, competitive queuing, PhD

Abstract

The ability to organize our movements in well-coordinated and functional sequences that are flexibly retrieved and generated from memory is a hallmark of the human behavioral repertoire. To achieve this skill, the brain utilizes the period before movement initiation to ‘set up’ and pre-pare the key higher-order properties of sequence representation, namely the order and timing of sequential movements. Previous neurophysiological research provides evidence for a parallel graded preactivation of upcoming movements offering support for a class of neural network models, termed competitive queuing (CQ). Timing has been modelled in this context as a key regulator of ordinal position of to-be-performed movements, whilst preparation time has been associated with improved subsequent performance. What remains unanswered is the role of prep-aration time and sequence timing in preorganizing the previously reported gradient of movements according to their position in the sequence during planning. By addressing that question, the pre-sent thesis aimed at disambiguating the representation of serial order and sequence timing during planning both with behavioral and neural measures. With a novel behavioral ‘delayed-production’ paradigm which utilized movement probes, this thesis first investigated the behavioral readout of the CQ mechanism prior to execution of well-learnt finger sequences and its modulation by prep-aration time or sequence timing (different speeds/temporal grouping). Subsequently, using movement decoding from non-invasive Electroencephalography (EEG) and concurrent Electro-myography (EMG), the parallel graded preactivation of upcoming movements and the potential impact of sequence timing, and specifically different speeds, on regulating the preactivations were further examined. The findings revealed that the preparatory CQ gradient acquired at the behavioral level represented the serial order of simultaneously prepared movements depending on their initial position in the sequence. The quality of movements’ organization expressed via the CQ gradient during planning was improved by more time to prepare the sequence, not its timing. The longer the preparation time the more the gradient was expanded refining the movements’ organization by their ordinal position. When more pronounced, i.e., featuring more distinct dif-ferences between positions, the gradient predicted better sequence performance, suggesting that this mechanism supports a more accurate sequence plan accounting for improved sequence execu-tion. The preparatory CQ gradient also reflected a fine-grained mechanism which determines the preparatory state of movements depending on whether a planned movement belongs to a se-quence or not, or whether a movement is planned as part of a sequence or not. In contrast to pre-vious findings, time-resolved EEG decoding showed that movement-related neural patterns were not preactivated in parallel before execution. Post hoc transformation of both the EEG and the EMG time series and timing analysis demonstrated that the EEG signal was scaled during se-quence planning according to the speed of the cued sequence. The timing of a movement unrelat-ed to the planned sequence was rehearsed during sequence planning at the same time as the se-quential movement in the first position. Both findings were not present at the neural periphery during sequence planning suggesting a high-level timing rehearsal of upcoming movements in the absence of overt motor behavior. Overall, these findings demonstrate that order and timing are controlled by different mechanisms during the planning of skilled motor sequences. This research has implications for understanding a modular control of motor sequence representation and the planning dynamics through different modalities and measures. Finally, these findings are dis-cussed in reference to skilled sequencing in movement disorders.

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Original languageEnglish
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Award date20 Jun 2022