Probing Corticospinal Control During Different Locomotor Tasks Using Detailed Time-Frequency Analysis of Electromyograms

Abstract

Locomotion relies on the fine-tuned coordination of different muscles which are controlled by particular neural circuits. Depending on the attendant conditions, walking patterns must be modified to optimally meet the demands of the task. Assessing neuromuscular control during dynamic conditions is methodologically highly challenging and prone to artifacts. Here we aim at assessing corticospinal involvement during different locomotor tasks using non-invasive surface electromyography. Activity in tibialis anterior (TA) and gastrocnemius medialis (GM) muscles was monitored by electromyograms (EMGs) in 27 healthy volunteers (11 female) during regular walking, walking while engaged in simultaneous cognitive dual tasks, walking with partial visual restriction, and skilled, targeted locomotion. Whereas EMG intensity of the TA and GM was considerably altered while walking with partial visual restriction and during targeted locomotion, dual-task walking induced only minor changes in total EMG intensity compared to regular walking. Targeted walking resulted in enhanced EMG intensity of GM in the frequency range associated with Piper rhythm synchronies. Likewise, targeted walking induced enhanced EMG intensity of TA at the Piper rhythm frequency around heelstrike, but not during the swing phase. Our findings indicate task- and phase-dependent modulations of neuromuscular control in distal leg muscles during various locomotor conditions in healthy subjects. Enhanced EMG intensity in the Piper rhythm frequency during targeted walking points toward enforced corticospinal drive during challenging locomotor tasks. These findings indicate that comprehensive time-frequency EMG analysis is able to gauge cortical involvement during different movement programs in a non-invasive manner and might be used as complementary diagnostic tool to assess baseline integrity of the corticospinal tract and to monitor changes in corticospinal drive as induced by neurorehabilitation interventions or during disease progression.

Targeted Walking in Incomplete Spinal Cord Injury: Role of Corticospinal Control

“…Of the measured muscles, TA is the only one exhibiting a two peak activity during one of the considered phases. Previous studies have shown differences in cortical contribution to the two peaks of TA activity during the swing phase 13,34 . Consequently, the two peak activity of TA during swing was analyzed in two separate windows.…”

“…iSCI or motor cortex lesions) [7][8][9][10] . Similarly, increased corticospinal control (input from cortical centers on spinal networks via the corticospinal tract) to locomotion has been shown in humans during anticipatory gait adaptations in visuo-motor targeted walking paradigms, in which foot placement is guided by randomized visual cues [11][12][13] . Targeted walking thus represents a suitable task for the assessment of corticospinal control of locomotion in humans.…”

“…EMG activity within the range of 20-60Hz (corticospinal drive frequencies) has been associated with corticospinal drive when investigated with corticomuscular and intermuscular coherence analysis [17][18][19][20] . Increased synchrony, suggesting common neural input, or shifts in relative intensity of EMGs to corticospinal drive frequencies, have been observed during voluntary gait pattern modifications 12,21 , including targeted treadmill walking 13 . In contrast, decreased synchrony has been observed during voluntary movement in various neurological disorders 22,23 , including iSCI 24 .…”

“…The EMG intensity of the filtered but non-normalized data of every step was decomposed into time and frequency components using a nonlinear wavelet transformation described in detail by von Tscharner 25 and applied to the analysis of dynamic movements in various settings 13,33 . Briefly, the wavelet transformation results in the EMG intensity (square root of power) of every step being distributed across nine frequency bands around center frequencies 7, 19, 38, 62, 92, 128, 170, 218 and 271 Hz.…”

“…Summation in each band separately results in a discrete wavelet intensity spectrum, which includes the intensity quantification of the chosen period of the gait cycle distributed across the nine frequency bands. In order to make wavelet spectra independent from EMG intensity and consequently allow the comparison between participants and the two walking conditions, relative intensity in each frequency band is calculated as a percentage of the total intensity (sum of intensity in all frequency bands).. A higher relative amount of EMG activity in the 38 Hz band has been associated to increased corticospinal control demands 13 . To compare frequency characteristics of specific muscle activity and not noise, wavelet spectra were calculated for windows of physiological muscle activity within stance (0-60%) and swing (60-100%), where muscles were active in both walking conditions.…”