MEG-compatible pneumatic stimulator to elicit passive finger and toe movements

Magnetoencephalographic (MEG) signals recorded from the primary sensorimotor (SM1) cortex are coherent with kinematics of both active and passive finger movements. The coherence mainly reflects movement-related proprioceptive afference to the cortex. Here we describe a novel MEG-compatible stimulator to generate computer-controlled passive finger and toe movements that can be used as stimuli in functional brain-imaging experiments. The movements are produced by pneumatic artificial muscle (PAM), elastic actuator that shortens with increasing air pressure. To test the applicability of the stimulator to functional brain-imaging, 4-min trains of passive repetitive 5-mm flexion-extension movements of the right and left index finger and the right hallux were produced at 3Hz while the subject's brain activity was measured with whole-scalp MEG and finger or toe kinematics with an accelerometer. In all ten subjects studied, statistically significant coherence (up to 0.78) occurred between the accelerometer and MEG signals at the movement frequency or its first harmonic. Sources of coherent activity were in the contralateral hand or foot SM1 cortices. Movement-evoked fields elicited with intermittent movements of the right index finger (once every 3.2-4.0s; mean±SD peak response latency 88±25ms) were co-located with the respective coherent sources. We further moved the right index finger at 3, 6, and 12Hz (movement ranges 5, 3, and 2mm, respectively), and analyzed the first 1, 2, and 4-min epochs of data. One minute of data was sufficient to locate the left hand area of the SM1 cortex at all movement frequencies. Sound-induced spurious coherence was reliably ruled out in a control experiment. Our novel movement stimulator thus provides a robust and reliable tool to track proprioceptive afference to the cortex and to locate the SM1 cortex.

[1]  H Suzuki,et al.  Somatosensory evoked magnetic fields following passive finger movement. , 1997, Brain research. Cognitive brain research.

[2]  P. Matthews,et al.  The relative sensitivity to vibration of muscle receptors of the cat , 1967, The Journal of physiology.

[3]  Mathieu Bourguignon,et al.  Neuronal network coherent with hand kinematics during fast repetitive hand movements , 2012, NeuroImage.

[4]  Riitta Hari,et al.  Coherence between magnetoencephalography and hand-action-related acceleration, force, pressure, and electromyogram , 2013, NeuroImage.

[5]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[6]  C. Weiller,et al.  Passive finger movement evoked fields in magnetoencephalography , 2000, Experimental Brain Research.

[7]  S S Hsiao,et al.  Detection of vibration transmitted through an object grasped in the hand. , 1999, Journal of neurophysiology.

[8]  V. Caggiano,et al.  Proprioceptive Feedback and Brain Computer Interface (BCI) Based Neuroprostheses , 2012, PloS one.

[9]  Riitta Hari,et al.  Corticokinematic coherence mainly reflects movement-induced proprioceptive feedback , 2015, NeuroImage.

[10]  S. Taulu,et al.  Suppression of Interference and Artifacts by the Signal Space Separation Method , 2003, Brain Topography.

[11]  Hiroshi Shibasaki,et al.  Somatosensory evoked potentials following proprioceptive stimulation of finger in man , 1996, Experimental Brain Research.

[12]  Gabriela Scheler,et al.  Utilization of magnetoencephalography results to obtain favourable outcomes in epilepsy surgery. , 2004, Brain : a journal of neurology.

[13]  Riitta Hari,et al.  Functional motor-cortex mapping using corticokinematic coherence , 2011, NeuroImage.

[14]  Pavel Sovka,et al.  Approximation of statistical distribution of magnitude squared coherence estimated with segment overlapping , 2007, Signal Process..

[15]  M. Bourguignon,et al.  Corticokinematic coherence during active and passive finger movements , 2013, Neuroscience.

[16]  A M Amjad,et al.  A framework for the analysis of mixed time series/point process data--theory and application to the study of physiological tremor, single motor unit discharges and electromyograms. , 1995, Progress in biophysics and molecular biology.

[17]  Dimitrios Pantazis,et al.  Coherent neural representation of hand speed in humans revealed by MEG imaging , 2007, Proceedings of the National Academy of Sciences.

[18]  Tsunehiro Takeda,et al.  Sensory feedback contributes to early movement-evoked fields during voluntary finger movements in humans , 1997, Brain Research.

[19]  O Salonen,et al.  Three‐dimensional integration of brain anatomy and function to facilitate intraoperative navigation around the sensorimotor strip , 2001, Human brain mapping.

[20]  S. Kameyama,et al.  Neuromagnetic activation following active and passive finger movements , 2013, Brain and behavior.

[21]  R Kakigi,et al.  Somatosensory evoked magnetic fields and potentials following passive toe movement in humans. , 1997, Electroencephalography and clinical neurophysiology.

[22]  R. Hari,et al.  Magnetoencephalography in the study of human somatosensory cortical processing. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[23]  V. Jousmäki,et al.  Cortical Activation Associated with Passive Movements of the Human Index Finger: An MEG Study , 2002, NeuroImage.

[24]  V. Jousmäki,et al.  Comprehensive Functional Mapping Scheme for Non-Invasive Primary Sensorimotor Cortex Mapping , 2012, Brain Topography.

[25]  J E Desmedt,et al.  SEPs to finger joint input lack the N20-P20 response that is evoked by tactile inputs: contrast between cortical generators in areas 3b and 2 in humans. , 1991, Electroencephalography and clinical neurophysiology.

[26]  A. Friederici,et al.  Cortical Neuromagnetic Fields Evoked by Voluntary and Passive Hand Movements in Healthy Adults , 2003, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[27]  Suresh D Muthukumaraswamy,et al.  Functional properties of human primary motor cortex gamma oscillations. , 2010, Journal of neurophysiology.

[28]  W. Huk,et al.  Somatosensory evoked magnetic fields following passive movement compared with tactile stimulation of the index finger , 2002, Experimental Brain Research.