Existing motor state is favored at the expense of new movement during 13-35 Hz oscillatory synchrony in the human corticospinal system

Abstract

Oscillations in local field potentials in the beta-frequency band (13-35 Hz) are a pervasive feature of human and nonhuman primate motor cortical areas. However, the function of such synchronous activity across populations of neurons remains unknown. Here, we test the hypothesis that beta activity may promote existing motor set and posture while compromising processing related to new movements. Three experiments were performed. First, healthy subjects were instructed to make reaction time movements of the outstretched index finger in response to imperative cues triggered by transient increases in corticospinal synchrony, as evidenced by phasic elevations of beta-frequency band microtremor and intermuscular synchrony. Second, healthy subjects were instructed to resist a stretch to the index finger triggered in the same way. Finger acceleration in the reaction time task and transcortical components of the stretch reflex were measured and compared with those elicited by random cue or stretch presentation. Finally, we sought a correlation between finger acceleration in the reaction time task and cortical synchrony directly measured from the electrocorticogram in two patients undergoing functional neurosurgery. We demonstrate that movements are slowed and transcortical responses to stretch are potentiated during periods of elevated beta-band cortical synchrony. The results suggest that physiological periods of beta synchrony are associated with a cortical state in which postural set is reinforced, but the speed of new movements impaired. The findings are of relevance to Parkinson's disease, in which subcortical and cortical beta-band synchronization is exaggerated in the setting of increased tone and slowed movements.

Figure 1.

β-Frequency band microtremor in a single healthy subject. A, Spontaneous intertrial microtremor and EMG from both ipsilateral and contralateral EI and FDI showing lateralized bursts of microtremor (marked by horizontal bars). B, Finger acceleration in response to cues. The first movement was made in response to a visual cue presented at random (RC). The second movement was made in response to a cue triggered by a transient increase in the β-band microtremor (TC). The thin horizontal line represents the voltage threshold for triggering the cue (triggering was only possible >5 s after the last movement). C, D, Acceleration, FDI, and EI EMG during the periods between xy and ab for the RC and TC trials, respectively. Note the emergence of EMG bursts with an ∼50 ms period that are synchronized between the two muscles before the triggered cue. This synchronized EMG activity is reflected in the accelerometer signal. Cue presentation occurred 50 ms after β microtremor exceeded trigger levels (thin horizontal lines), with this delay being determined by the on-line electronic β bandpass filter. In contrast, before the RC, EMG is desynchronized, and there is little microtremor in the finger. Cue onset is given by the dashed vertical line.

Figure 2.

Intermuscular synchrony in a single healthy subject. PA was 18% less, on average, when cues were triggered (n = 146 movements) rather than randomly (n = 72) presented. A, B, Wavelet transformed microtremor power averaged around TCs and RCs, respectively. C, D, Averaged, time-evolved cross-correlation function between ipsilateral FDI and EI EMG at PTF (21 Hz; F1) in TC and RC trials. E, F, Two-dimensional cross-correlations (thick lines) at maxima in C and D at T1 and T2, respectively, with respective SEMs (thin lines). Ninety-five percent confidence limits are illustrated by the black horizontal lines on both the color plot scales and the two-dimensional correlations. Correlations with a Z score of >4.75 were considered significant [level determined after correction for multiple comparisons (129 lag points, 384 time points) by Bonferroni's method] [for previous use of this technique, see Roelfsema et al. (1997)]. This significance level was further verified using a shift control correlation in which no correlations were above this level. G, H, Individual and mean ±SEM peak intermuscular synchrony during periods of EMG activity before RC and TC presentation. Error bars represent SEM. ^**p = 0.04 (Wilcoxon signed ranks test).

Figure 3.

Behavioral data for both TCs and RCs in 10 healthy subjects. A, Individual mean PA. ^*p = 0.01. B, Individual mean RT. ns, Not significant (p = 0.74).

Figure 4.

Response to direct electrical stimulation of FDI. Shocks were either delivered triggered (TC) by bursts of β-frequency band microtremor or presented randomly (RC) in 10 healthy subjects. Individual mean PA in elicited twitches. ns, Not significant (p = 0.14).

Figure 5.

Relationship between ECoG over sensorimotor cortex and contralateral movement execution in two patients treated for chronic pain. A, Example of spontaneous β oscillations recorded from patient DF, which demonstrates their focal as indicated by arrow b or diffuse character where oscillations are present across all contacts, as in a and c. B, Postoperative skull x-rays from patients DF (top) and CO (bottom), respectively, with electrode position and contacts with maximal correlations labeled. C, D, ECoG from contacts 01 in patient DF and posterior contacts 01 in patient CO was decomposed into wavelet coefficients around the time of a randomly presented cue and Pearson's correlation estimated between ECoG β-frequency band power at each time point for each trial and the PA of the corresponding trial in patients DF (C) and CO (D). Correlation matrices thresholded at 99% significance level (r = -0.20 and r = 0.21, respectively). E, Correlation at T1, F1 (21 Hz), between log 10 wavelet power and PA. F, Correlation at T2, F2 (15 Hz), between log 10 wavelet power, and PA. G, Correlation at T1, F1 (21 Hz), between log 10 wavelet power and RT. H, Correlation at T2, F2 (15 Hz), between log 10 wavelet power and RT. The average reaction time was 275 ± 3 ms for patient DF and 483 ± 7 ms in patient CO.

Figure 6.

TS experiments. A, Average across all subjects of rectified β bandpass-filtered acceleration recorded with the ipsilateral (i) or contralateral (c) accelerometer during the 500 ms before RS or TS. Note the clear transient ipsilateral increase in the β-band microtremor before the TS. B, Averaged EMG responses from a single participant elicited by RS (n = 50 trials; top) and TS (n = 34 trials; bottom). Stretch onset is given by the thick vertical line. Stretch responses were divided into three components: M1 (32-50 ms), M2 (54-100 ms), and M3 (100-300 ms). Note that the transcortical M2 response was increased after TS compared with RS, whereas spinal M1 and late M3 responses remained unchanged. C, M1 and M2 responses (mean EMG minus background activity) for both TS and RS in 10 healthy participants. ns, Not significant (p = 0.326). ^*p = 0.003; two-tailed paired t tests.