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Research Articles, Behavioral/Cognitive

Voluntary Motor Command Release Coincides with Restricted Sensorimotor Beta Rhythm Phases

Sara J Hussain, Mary K Vollmer, Iñaki Iturrate and Romain Quentin
Journal of Neuroscience 20 July 2022, 42 (29) 5771-5781; DOI: https://doi.org/10.1523/JNEUROSCI.1495-21.2022
Sara J Hussain
1Movement and Cognitive Rehabilitation Science Program, Department of Kinesiology and Health Education, University of Texas at Austin, Austin, Texas 78712
2Human Cortical Physiology and Neurorehabilitation Section, National Institute of Neurological Disorders and Stroke, Bethesda, Maryland 20892
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Mary K Vollmer
2Human Cortical Physiology and Neurorehabilitation Section, National Institute of Neurological Disorders and Stroke, Bethesda, Maryland 20892
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Iñaki Iturrate
2Human Cortical Physiology and Neurorehabilitation Section, National Institute of Neurological Disorders and Stroke, Bethesda, Maryland 20892
3Amazon EU, Spain
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Romain Quentin
2Human Cortical Physiology and Neurorehabilitation Section, National Institute of Neurological Disorders and Stroke, Bethesda, Maryland 20892
4MEL Group, EDUWELL Team, Lyon Neuroscience Research Center, Institut National de la Santé et de la Recherche Médicale U1028, Centre National de la Recherche Scientifique UMR5292, Université Claude Bernard Lyon 1, 69500 Bron, France
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  • Figure 1.
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    Figure 1.

    Experimental design and EEG analysis approach. a, Subjects viewed a series of pictures on a computer screen while they performed a self-paced finger movement task. Subjects were instructed to press a button using their left index finger when they wished to move to the next picture. EMG and EEG signals were recorded during the task. b, Before task performance, single-pulse TMS was used to determine each subject's corticomuscular conduction time by measuring the L FDI MEP onset latency. Corticomuscular conduction times were used to identify the time of motor command release from M1 preceding each finger movement. c, Flowchart depicting EEG processing steps.

  • Figure 2.
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    Figure 2.

    EMG and contralateral EEG data during individual finger movements recorded from a representative subject. a, b, Raw (colored) and bandpass-filtered (white) contralateral EEG data during individual finger movements. c, d, Time-domain representation of L FDI EMG data during individual finger movements. e, f, Time-frequency representation of L FDI EMG data during individual finger movements. Cooler and warmer colors indicate smaller and larger values, respectively. Note that color scaling was chosen to emphasize the onset of EMG activity. g, h, Raw power spectra (black), aperiodic fit of raw power spectra (gray), and fooof-modeled power spectra (colored). Black lines indicate MCRM1 time points, and gray lines indicate EMG onset time points (a–f). Left, contralateral mu; right, contralateral beta. Note the oscillatory activity present in all raw EEG traces (a, b) and power spectra (g, h) for mu and beta, respectively.

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    Figure 3.

    EMG and ipsilateral EEG data during individual finger movements recorded from a representative subject. a, b, Raw (colored) and bandpass-filtered (white) ipsilateral EEG data during individual finger movements. c, d, Time domain L FDI EMG data during individual finger movements. e, f, Time-frequency representation of L FDI EMG data during individual finger movements. Cooler and warmer colors indicate smaller and larger values, respectively. Note that color scaling was chosen to emphasize the onset of EMG activity. g, h, Raw power spectra (black), aperiodic fit of raw power spectra (gray), and fooof-modeled power spectra (colored). Black lines indicate MCRM1 time points and gray lines indicate EMG onset time points (a–f), Left, ipsilateral mu; right, ipsilateral beta. Note the oscillatory activity present in all raw EEG traces (a, b) and power spectra (g, h) for mu and beta, respectively.

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    Figure 4.

    Contralateral mu and beta phase angles during MCRM1. a, b, Variation in phase angles during MCRM1 at the individual subject level for contralateral mu (a) and beta (b) rhythms. Each dot reflects an individual subject's mean phase angle during MCRM1. Each circular line reflects an individual subject's phase angle SD during MCRM1. c, d, Mu (c) and beta (d) phase angles during MCRM1 along the oscillatory cycle and in phase space. Each dot indicates a single subject's mean phase angle during MCRM1. Phase angle histograms represent group-level distributions of mean phase angles during MCRM1. Radii values indicate the number of subjects showing mean phase angles within a given phase bin. The black square and horizontal line in d reflect the mean beta phase angle and the group-level SD. For c, the group mean and SD is not shown because of lack of significant deviations from uniformity. The asterisk reflects significance at p < 0.05.

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    Figure 5.

    Ipsilateral mu and beta phase angles during MCRM1. Variation in phase angles during MCRM1 at the individual subject level for ipsilateral mu (a) and beta (b). Each dot reflects an individual subject's mean phase angle during MCRM1. Each circular line reflects an individual subject's phase angle SD during MCRM1. c, d, Mu (c) and beta (d) phase angles during MCRM1 along the oscillatory cycle and in phase space. Each dot indicates a single subject's mean phase angle during MCRM1. Phase angle histograms represent group-level distributions of mean phase angles during MCRM1. Radii values indicate the number of subjects showing mean phase angles within a given phase bin. For c and d, group means and SDs are not shown because of lack of significant deviations from uniformity.

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    Table 1.

    Individual MEP latencies, center frequencies, and fooof model fits

    SubjectMEP latency (ms)Individual frequencies (Hz)Fooof fits (r2)
    ContralateralIpsilateralContralateralIpsilateral
    MuBetaMuBetaMuBetaMuBeta
    125.010.64 (1.18)20.16 (4.41)10.92 (1.15)22.54 (4.84)0.86 (0.13)0.74 (0.19)0.79 (0.15)0.77 (0.19)
    222.810.35 (1.10)20.61 (4.58)11.13 (1.23)21.40 (4.21)0.83 (0.10)0.79 (0.18)0.81 (0.20)0.83 (0.10)
    322.210.87 (1.32)20.62 (5.64)10.85 (1.13)21.58 (5.58)0.79 (0.15)0.79 (0.17)0.83 (0.15)0.84 (0.16)
    422.010.93 (1.06)20.68 (5.80)11.10 (1.13)22.45 (5.76)0.90 (0.11)0.82 (0.17)0.85 (0.10)0.77 (0.20)
    5—10.94 (1.04)22.35 (5.43)11.43 (1.05)22.59 (4.71)0.87 (0.11)0.87 (0.14)0.92 (0.09)0.90 (0.11)
    626.210.61 (1.11)22.31 (5.93)10.94 (1.10)22.38 (5.18)0.81 (0.13)0.79 (0.18)0.82 (0.11)0.83 (0.17)
    723.8————————
    822.611.67 (0.78)21.09 (5.04)——0.85 (0.10)0.80 (0.14)——
    920.4——11.29 (1.24)21.45 (5.57)——0.80 (0.15)0.76 (0.17)
    1026.810.55 (0.89)23.40 (6.50)10.12 (0.78)24.46 (5.97)0.86 (0.12)0.83 (0.14)0.87 (0.15)0.78 (0.17)
    11—11.67 (1.12)—11.81 (1.14)22.20 (5.78)0.88 (0.12)—0.89 (0.12)0.89 (0.08)
    1223.411.10 (1.08)21.44 (5.69)11.30 (1.23)21.16 (5.05)0.79 (0.15)0.78 (0.17)0.82 (0.14)0.77 (0.16)
    1323.211.27 (0.86)25.15 (4.90)11.04 (0.94)22.52 (5.67)0.86 (0.13)0.85 (0.16)0.83 (0.11)0.81 (0.19)
    1422.411.21 (1.07)20.72 (4.20)11.07 (0.87)20.99 (3.65)0.89 (0.12)0.88 (0.12)0.93 (0.10)0.89 (0.09)
    1523.410.69 (1.26)19.85 (5.31)11.33 (0.96)20.07 (5.11)0.86 (0.12)0.75 (0.17)0.86 (0.11)0.77 (0.14)
    1624.610.75 (1.04)21.91 (5.64)11.01 (1.18)21.96 (6.51)0.83 (0.12)0.80 (0.17)0.82 (0.16)0.73 (0.24)
    1721.610.62 (1.04)23.89 (5.43)10.41 (0.76)24.32 (5.51)0.88 (0.12)0.84 (0.16)0.85 (0.11)0.86 (0.13)
    1826.210.41 (1.32)22.25 (5.06)10.79 (0.95)21.58 (5.64)0.80 (0.17)0.81 (0.16)0.88 (0.09)0.87 (0.10)
    1925.011.37 (1.24)21.60 (6.58)11.84 (1.00)20.08 (6.58)0.82 (0.18)0.87 (0.11)0.86 (0.12)0.88 (0.12)
    2022.8—20.26 (4.23)—23.10 (5.79)—0.82 (0.16)—0.83 (0.13)
    2122.0——11.02 (1.22)23.88 (6.34)——0.84 (0.13)0.85 (0.13)
    Mean23.4910.9221.6611.0822.200.850.810.850.82
    SD1.730.411.440.421.260.030.040.040.05
    • For MEP latencies, dashes depict subjects for whom latencies could not be reliably identified. For all other columns, dashes depict subjects with fewer than 10 trials per hemisphere and frequency.

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    Table 2.

    Group-level coefficients of variation for center frequencies and the number of spectral peaks detected by the fooof algorithm

    Calculation methodCoefficient of variation of center frequenciesCoefficient of variation of number of detected peaks
    ContralateralIpsilateralContralateralIpsilateral
    MuBetaMuBetaMuBetaMuBeta
    Across time points within the same trial0.01 (0.004)0.03 (0.01)0.01 (0.004)0.03 (0.02)0.17 (0.06)0.16 (0.04)0.14 (0.04)0.15 (0.03)
    Across trials at MCRM1 time points0.10 (0.02)0.25 (0.03)0.10 (0.01)0.25 (0.06)0.37 (0.05)0.41 (0.04)0.34 (0.09)0.42 (0.09)
    • Coefficients of variation were calculated per trial at each time point within ± 5 ms of MCRM1 (top row) and across trials at MCRM1 (bottom row).

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The Journal of Neuroscience: 42 (29)
Journal of Neuroscience
Vol. 42, Issue 29
20 Jul 2022
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Voluntary Motor Command Release Coincides with Restricted Sensorimotor Beta Rhythm Phases
Sara J Hussain, Mary K Vollmer, Iñaki Iturrate, Romain Quentin
Journal of Neuroscience 20 July 2022, 42 (29) 5771-5781; DOI: 10.1523/JNEUROSCI.1495-21.2022

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Voluntary Motor Command Release Coincides with Restricted Sensorimotor Beta Rhythm Phases
Sara J Hussain, Mary K Vollmer, Iñaki Iturrate, Romain Quentin
Journal of Neuroscience 20 July 2022, 42 (29) 5771-5781; DOI: 10.1523/JNEUROSCI.1495-21.2022
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Keywords

  • electroencephalography
  • motor
  • movement
  • oscillations
  • sensorimotor rhythms

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