Sequential Finger-tapping Learning Mediated by the Primary Motor Cortex and Fronto-parietal Network: A Combined MRI-MRS Study

Abstract

The primary motor cortex (M1) is crucial for motor learning. However, the interaction of the M1 with other brain areas during motor learning remains unclear. We hypothesized that the fronto-parietal execution network (FPN) provides the learning-related information that is crucial for flexible cognitive control required for practice. We assessed the network-level changes during sequential finger-tapping learning “as fast and as accurately as possible”, by combining magnetic resonance spectroscopy, task functional magnetic resonance imaging (fMRI), and resting-state fMRI methods using a 7T MR machine. An increase in the glutamate/GABA ratio in the right M1 was positively correlated with task performance improvement. There was a motor learning-related increase in preparatory activity in the fronto-parietal region, with an overlap between the FPN and sensorimotor network (SMN). The learning-related increments in M1-seeded functional connectivity with the FPN, but not the SMN, were positively correlated with changes in the glutamate/GABA ratio in M1. These connectivity changes were more prominent in the parietal region than in the frontal region. Our findings indicate that motor learning driven by cognitive control is associated with local variation in the excitatory-inhibitory balance in the M1 that reflects remote connectivity with the FPN, thereby representing the formation of declarative procedural skills.

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“…Additionally, the FPN to which the dlPFC belongs serves as a flexible hub to rapidly instantiate task states through interactions with other control and processing networks ( Marek and Dosenbach, 2018 ). This network is activated during motor sequence tasks and contributes to motor learning ( Maruyama et al, 2021 ). Simultaneous activation of the FPN and M1 during motor preparation was also found ( Maruyama et al, 2021 ).…”

“…This network is activated during motor sequence tasks and contributes to motor learning ( Maruyama et al, 2021 ). Simultaneous activation of the FPN and M1 during motor preparation was also found ( Maruyama et al, 2021 ). In addition, the FPN was also found to receive projections from the ARAS, which is primarily responsible for consciousness ( Jang et al, 2021 ).…”

“…In addition, the FPN may play a facilitating role in the motor cortex responsible for the current movement. In some sequential motor-learning tasks, the FPN and M1 contralateral to the movement side exhibit simultaneous activation during the preparation phase ( Maruyama et al, 2021 ). This is explained as internal reproduction and learning during the motor preparation phase.…”