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Characterization of electrocorticogram high-gamma signal in response to varying upper extremity movement velocity

Abstract

The mechanism by which the human primary motor cortex (M1) encodes upper extremity movement kinematics is not fully understood. For example, human electrocorticogram (ECoG) signals have been shown to modulate with upper extremity movements; however, this relationship has not been explicitly characterized. To address this issue, we recorded high-density ECoG signals from patients undergoing epilepsy surgery evaluation as they performed elementary upper extremity movements while systematically varying movement speed and duration. Specifically, subjects performed intermittent pincer grasp/release, elbow flexion/extension, and shoulder flexion/extension at slow, moderate, and fast speeds. In all movements, bursts of power in the high-\(\gamma \) band (80–160 Hz) were observed in M1. In addition, the amplitude of these power bursts and the area of M1 with elevated high-\(\gamma \) activity were directly proportional to the movement speed. Likewise, the duration of elevated high-\(\gamma \) activity increased with movement duration. Based on linear regression, M1 high-\(\gamma \) power amplitude and duration covaried with movement speed and duration, respectively, with an average \(r^2\) of \(0.75 \pm 0.10\) and \(0.68 \pm 0.21\). These findings indicate that the encoding of upper extremity movement speed by M1 high-\(\gamma \) activity is primarily linear. Also, the fact that this activity remained elevated throughout a movement suggests that M1 does not merely generate transient instructions for a specific movement duration, but instead is responsible for the entirety of the movement. Finally, the spatial distribution of high-\(\gamma \) activity suggests the presence of a recruitment phenomenon in which higher speeds or increased muscle activity involve activation of larger M1 areas.

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Acknowledgements

We thank Angelica Nguyen for her assistance in setting up the experiments and Michael Chen and Aydin Kazgachi for their assistance in fabricating the gyroscopic instruments. This study was supported by the National Science Foundation (Award #1134575).

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Correspondence to Zoran Nenadic or An H. Do.

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Appendices

Appendix A: Figures for \(\overline{P}_\gamma \)

See Figs. 12, 13, 14, 15, 16, 17, 18, 19, 20 and 21.

Fig. 12
figure12

Spatial map of the M1 high-\(\gamma \) power underlying each movement speed–direction combination as well as the isometric flexion and extension epochs for Subject 1. Circles core electrodes

Fig. 13
figure13

Spatial map of the M1 high-\(\gamma \) power underlying each movement speed–direction combination as well as the isometric flexion and extension epochs for Subject 3. Circles core electrodes

Fig. 14
figure14

Spatial map of the M1 high-\(\gamma \) power underlying each movement speed–direction combination as well as the isometric flexion and extension epochs for Subject 4. Circles core electrodes

Fig. 15
figure15

Spatial map of the M1 high-\(\gamma \) power underlying each movement speed–direction combination as well as the isometric flexion and extension epochs for Subject 5. Circles core electrodes

Fig. 16
figure16

Spatial map of the M1 high-\(\gamma \) power underlying each movement speed–direction combination as well as the isometric flexion and extension epochs for Subject 6. Circles core electrodes

Fig. 17
figure17

Spatial map of the M1 high-\(\gamma \) power underlying each movement speed–direction combination as well as the isometric flexion and extension epochs for Subject 7. Circles core electrodes

Fig. 18
figure18

Spatial maps of the per-channel coefficient of determination (\(r^2\)) between \(\overline{P}_\gamma \) and \(\overline{\omega }\) aggregated across all movement events and speeds for Subjects 1 and 3. Circle core electrode. Triangle electrode with the highest \(r^2\) for each panel. The color of each symbol is consistent with the \(r^2\) value at the corresponding electrode

Fig. 19
figure19

\(r^2\) between \(\overline{P}_\gamma \) and \(\overline{\omega }\) for Subjects 4 and 5. Circle core electrode. Triangle electrode with the highest \(r^2\) for each panel

Fig. 20
figure20

\(r^2\) between \(\overline{P}_\gamma \) and \(\overline{\omega }\) for Subjects 6 and 7. Circle core electrode. Triangle electrode with the highest \(r^2\) for each panel

Fig. 21
figure21

Box and whisker graphs of \(\overline{\overline{P}}_{\gamma }\) for individual subjects. The vertical axes are normalized amplitudes (IMAD). NS non-significant (\(p>0.05\)); *\(p<0.05\); **\(p<0.01\)

Appendix B: Figures for \(D_M\)

See Figs. 22, 23, 24, 25, 26, 27, 28, 29, 30, 31, 32, 33, 34 and 35.

Fig. 22
figure22

The spatial distribution of \(D_M\) (in ms) for Subject 1. See Fig. 2 for definition

Fig. 23
figure23

The spatial distribution of \(D_M\) (in ms) for Subject 2

Fig. 24
figure24

The spatial distribution of \(D_M\) (in ms) for Subject 3

Fig. 25
figure25

The spatial distribution of \(D_M\) (in ms) for Subject 4

Fig. 26
figure26

The spatial distribution of \(D_M\) (in ms) for Subject 5

Fig. 27
figure27

The spatial distribution of \(D_M\) (in ms) for Subject 6

Fig. 28
figure28

The spatial distribution of \(D_M\) (in ms) for Subject 7

Fig. 29
figure29

Spatial maps of the per-channel coefficient of determination (\(r^2\)) between \(D_M\) and \(W_M\) aggregated across all movement events and speeds for Subjects 1 and 3. Circle core electrode. Triangle electrode with the highest \(r^2\) for each panel. The color of each symbol indicates the electrode’s \(r^2\) value

Fig. 30
figure30

Spatial maps of the per-channel coefficient of determination (\(r^2\)) between \(D_M\) and \(W_M\) aggregated across all movement events and speeds for Subjects 4 and 5. Circle core electrode. Triangle electrode with the highest \(r^2\) for each panel

Fig. 31
figure31

Spatial maps of the per-channel coefficient of determination (\(r^2\)) between \(D_M\) and \(W_M\) aggregated across all movement events and speeds for Subjects 6 and 7. Circle core electrode. Triangle electrode with the highest \(r^2\) for each panel

Fig. 32
figure32

Spatial map of the per-channel ratios \(D_M/W_M\) and \(D_I/W_I\) averaged across all movement speeds and events for Subjects 1 and 3. Circle core electrodes. Triangle electrodes with the highest averaged \(D_M/W_M\) for each specific movement and direction. The color of each symbol indicates the electrode’s \(D_M/W_M\) value

Fig. 33
figure33

Spatial map of the per-channel ratios \(D_M/W_M\) and \(D_I/W_I\) averaged across all movement speeds and events for Subjects 4 and 5. Circle core electrodes. Triangle electrodes with the highest averaged \(D_M/W_M\) for each specific movement and direction

Fig. 34
figure34

Spatial map of the per-channel ratios \(D_M/W_M\) and \(D_I/W_I\) averaged across all movement speeds and events for Subjects 6 and 7. Circle core electrodes. Triangle electrodes with the highest averaged \(D_M/W_M\) for each specific movement and direction

Fig. 35
figure35

Box and whisker graphs of \(D_M\) for individual subjects. The vertical axes are in ms

Appendix C: Figures for control experiments

See Figs. 36 and 37.

Fig. 36
figure36

Spatial map of the M1 high-\(\gamma \) power (\(\overline{P}_\gamma \)) underlying each “speed–direction” combination as well as the isometric “flexion” and “extension” epochs for Subject 5 in the control experiment (no actual movement or exertion of force)

Fig. 37
figure37

Spatial map of the M1 high-\(\gamma \) power (\(\overline{P}_\gamma \)) underlying each “speed–direction” combination as well as the isometric “flexion” and “extension” epochs for Subject 6 in the control experiment (no actual movement or exertion of force)

Appendix D: Tables for \(\overline{P}_\gamma \) and \(D_M\)

See Tables 4 and 5.

Table 4 \(r^2\) values of the electrode with the highest \(r^2\) (denoted in parentheses) for every subject, movement, and direction
Table 5 Distance (mm) between the core electrode and the electrode with the highest \(r^2\)

Appendix E: Determining envelope filter cutoffs

The corner frequency, \(f_c=2.5\) Hz, of the low-pass Butterworth filter used for \(\gamma \)-power envelope calculations (see Sect. 2.4.2) was chosen based on several factors. Namely its dominant time constant \(\tau _d=166\) ms is well matched to the duration of movements, as it takes 2–5 \(\tau _d\) to complete the fastest movements, and >8 \(\tau _d\) for slower ones (see Table 1). In addition, the main lobe of the filter’s impulse response is \(\sim \)400 ms, which is consistent with a typical duration of an integration window in ECoG-based BCI studies (Wang et al. 2013e). Finally, its zero-phase (acausal) nature ensures that the temporal relationship between the trajectory and \(\gamma \)-power bursts remains preserved, as can be seen in Fig. 40.

To verify the robustness of our results, we reanalyzed Subject 2’s data while perturbing the parameter \(f_c\). Specifically, brain maps of \(D_M/W_M\) as well as \(r^2\) between \(D_M\) and \(W_M\) were recomputed while varying the value of \(f_c\) from 2 to 5 Hz. Naturally, as \(f_c\) increased, the time constant, \(\tau _d\), decreased, thereby reducing the value of \(D_M\), and consequently the ratio, \(D_M/W_M\). However, this affected all electrodes in a similar manner and merely rescaled the \(D_M/W_M\) maps, as can be seen by comparing Figs. 6 and 38. On the other hand, the \(r^2\) maps remained essentially unchanged, as can be seen by comparing Figs.  10 and 39. This indicates that the goodness-of-fit of the linear model given by Eq. (4) did not change and remained high in the relevant areas, especially near the core electrode. At the same time, the \(r^2\) values between \(D_I\) and \(W_I\) remained low, suggesting an appropriate choice of thresholds for \(P_\gamma \) calculation (see Sect. 2.4.6).

Fig. 38
figure38

Spatial map of the per-channel ratios \(D_M/W_M\) and \(D_I/W_I\) averaged across all movement speeds and events for Subject 2 with the high-\(\gamma \) envelope filter set to 5 Hz. Circle core electrodes. Triangle electrodes with the highest averaged \(D_M/W_M\) for each specific movement and direction. The color of each symbol indicates the electrode’s \(D_M/W_M\) value. Compare to Fig. 6

Fig. 39
figure39

Spatial maps of the per-channel coefficient of determination (\(r^2\)) between \(D_M\) and \(W_M\) aggregated across all movement events and speeds for Subject 2 with the high-\(\gamma \) envelope filter set to 5 Hz. Circle core electrode. Triangle electrode with the highest \(r^2\) for each panel. The color of each symbol indicates the electrode’s \(r^2\) value. Compare to Fig. 10

Finally, Fig. 40 shows the evolution of \(P_\gamma \) as \(f_c\) varies from 2 to 40 Hz. Starting from \(f_c=10\) Hz, the period of elevated \(P_\gamma \) was no longer contiguous, which undermined the definition of \(D_M\) (see Sect. 2.4.3). At the same time, the amplitude of high-\(\gamma \) power bursts outside of movement periods increased, resulting in a significant loss of signal-to-noise ratio. This is not surprising since at \(f_c\ge 10\) Hz, the time constant of the filter (\(\tau _d\le 42\) ms) no longer matches the characteristic time scale of ECoG signals and is therefore highly suboptimal for analysis.

Fig. 40
figure40

Time movement velocity \(\omega \) and \(P_\gamma \) signal at electrode #24 during Subject 2’s PG experiment runs. Red dashed lines the local MAD (LMAD) thresholds estimated from local idling periods around each flexion or extension. Numbers denote the peak amplitudes during movement and local idling periods

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Wang, P.T., McCrimmon, C.M., King, C.E. et al. Characterization of electrocorticogram high-gamma signal in response to varying upper extremity movement velocity. Brain Struct Funct 222, 3705–3748 (2017). https://doi.org/10.1007/s00429-017-1429-8

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Keywords

  • Electrocorticography
  • Motor cortex
  • Kinematic
  • Movement speed
  • Movement duration