Predicting motor learning performance from Electroencephalographic data

BackgroundResearch on the neurophysiological correlates of visuomotor integration and learning (VMIL) has largely focused on identifying learning-induced activity changes in cortical areas during motor execution. While such studies have generated valuable insights into the neural basis of VMIL, little is known about the processes that represent the current state of VMIL independently of motor execution. Here, we present empirical evidence that a subject’s performance in a 3D reaching task can be predicted on a trial-to-trial basis from pre-trial electroencephalographic (EEG) data. This evidence provides novel insights into the brain states that support successful VMIL.MethodsSix healthy subjects, attached to a seven degrees-of-freedom (DoF) robot with their right arm, practiced 3D reaching movements in a virtual space, while an EEG recorded their brain’s electromagnetic field. A random forest ensemble classifier was used to predict the next trial’s performance, as measured by the time needed to reach the goal, from pre-trial data using a leave-one-subject-out cross-validation procedure.ResultsThe learned models successfully generalized to novel subjects. An analysis of the brain regions, on which the models based their predictions, revealed areas matching prevalent motor learning models. In these brain areas, the α/μ frequency band (8–14 Hz) was found to be most relevant for performance prediction.ConclusionsVMIL induces changes in cortical processes that extend beyond motor execution, indicating a more complex role of these processes than previously assumed. Our results further suggest that the capability of subjects to modulate their α/μ bandpower in brain regions associated with motor learning may be related to performance in VMIL. Accordingly, training subjects in α/μ-modulation, e.g., by means of a brain-computer interface (BCI), may have a beneficial impact on VMIL.

[1]  D. Brooks,et al.  Motor sequence learning: a study with positron emission tomography , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[2]  Ron Kohavi,et al.  A Study of Cross-Validation and Bootstrap for Accuracy Estimation and Model Selection , 1995, IJCAI.

[3]  R. Shadmehr,et al.  Neural correlates of motor memory consolidation. , 1997, Science.

[4]  Eric Moulines,et al.  A blind source separation technique using second-order statistics , 1997, IEEE Trans. Signal Process..

[5]  M. Hallett,et al.  Frontal and parietal networks for conditional motor learning: a positron emission tomography study. , 1997, Journal of neurophysiology.

[6]  S. Kinomura,et al.  Activity in the parietal area during visuomotor learning with optical rotation , 1997, Neuroreport.

[7]  H. C. Diener,et al.  The Relevance of Sensory Input for the Cerebellar Control of Movements , 1997, NeuroImage.

[8]  S. Petersen,et al.  Changes in brain activity during motor learning measured with PET: effects of hand of performance and practice. , 1998, Journal of neurophysiology.

[9]  Kae Nakamura,et al.  Central mechanisms of motor skill learning , 2002, Current Opinion in Neurobiology.

[10]  M. Nitsche,et al.  Facilitation of Implicit Motor Learning by Weak Transcranial Direct Current Stimulation of the Primary Motor Cortex in the Human , 2003, Journal of Cognitive Neuroscience.

[11]  Richard A. Andersen,et al.  FMRI evidence for a 'parietal reach region' in the human brain , 2003, Experimental Brain Research.

[12]  Leo Breiman,et al.  Random Forests , 2001, Machine Learning.

[13]  R.M. Leahy,et al.  Electromagnetic brain imaging using BrainStorm , 2004, 2004 2nd IEEE International Symposium on Biomedical Imaging: Nano to Macro (IEEE Cat No. 04EX821).

[14]  U. Halsband,et al.  Motor learning in man: A review of functional and clinical studies , 2006, Journal of Physiology-Paris.

[15]  Cuntai Guan,et al.  Clinical study of neurorehabilitation in stroke using EEG-based motor imagery brain-computer interface with robotic feedback , 2010, 2010 Annual International Conference of the IEEE Engineering in Medicine and Biology.

[16]  J. Peters,et al.  Closing the sensorimotor loop: haptic feedback facilitates decoding of motor imagery , 2011, Journal of neural engineering.

[17]  Moritz Grosse-Wentrup,et al.  Using brain–computer interfaces to induce neural plasticity and restore function , 2011, Journal of neural engineering.

[18]  Bernhard Schölkopf,et al.  Closing the Sensorimotor Loop: Haptic Feedback Helps Decoding of Motor Imagery , 2011 .

[19]  Bernhard Schölkopf,et al.  A brain-robot interface for studying motor learning after stroke , 2012, 2012 IEEE/RSJ International Conference on Intelligent Robots and Systems.

[20]  C. Neuper,et al.  Relationship Between Electrical Brain Responses to Motor Imagery and Motor Impairment in Stroke , 2012, Stroke.

[21]  Simon B. Eickhoff,et al.  A quantitative meta-analysis and review of motor learning in the human brain , 2013, NeuroImage.