NeuroImage (Aug 2024)
Macroscopic brain dynamics beyond contralateral primary motor cortex for movement prediction
Abstract
This study investigates the complex relationship between upper limb movement direction and macroscopic neural signals in the brain, which is critical for understanding brain-computer interfaces (BCI). Conventional BCI research has primarily focused on a local area, such as the contralateral primary motor cortex (M1), relying on the population-based decoding method with microelectrode arrays. In contrast, macroscopic approaches such as electroencephalography (EEG) and magnetoencephalography (MEG) utilize numerous electrodes to cover broader brain regions. This study probes the potential differences in the mechanisms of microscopic and macroscopic methods. It is important to determine which neural activities effectively predict movements. To investigate this, we analyzed MEG data from nine right-handed participants while performing arm-reaching tasks. We employed dynamic statistical parametric mapping (dSPM) to estimate source activity and built a decoding model composed of long short-term memory (LSTM) and a multilayer perceptron to predict movement trajectories. This model achieved a high correlation coefficient of 0.79 between actual and predicted trajectories. Subsequently, we identified brain regions sensitive to predicting movement direction using the integrated gradients (IG) method, which assesses the predictive contribution of each source activity. The resulting salience map demonstrated a distribution without significant differences across motor-related regions, including M1. Predictions based solely on M1 activity yielded a correlation coefficient of 0.42, nearly half as effective as predictions incorporating all source activities. This suggests that upper limb movements are influenced by various factors such as movement coordination, planning, body and target position recognition, and control, beyond simple muscle activity. All of the activities are needed in the decoding model using macroscopic signals. Our findings also revealed that contralateral and ipsilateral hemispheres contribute equally to movement prediction, implying that BCIs could potentially benefit patients with brain damage in the contralateral hemisphere by utilizing brain signals from the ipsilateral hemisphere. In conclusion, this study demonstrates that macroscopic activity from large brain regions significantly contributes to predicting upper limb movement. Non-invasive BCI systems would require a comprehensive collection of neural signals from multiple brain regions.
