Corticospinal Excitability Is Modulated as a Function of Postural Perturbation Predictability

Abstract

Recent studies demonstrated that the corticospinal pathway is one of the key nodes for the feedback control of human standing and that the excitability is flexibly changed according to the current state of posture. However, it has been unclear whether this pathway is also involved in a predictive control of human standing. Here, we investigated whether the corticospinal excitability of the soleus (SOL) and tibialis anterior (TA) muscles during standing would be modulated anticipatorily when perturbation was impending. We measured the motor-evoked potential (MEP) induced by transcranial magnetic stimulation over the motor cortex at six stimulus intensities. Three experimental conditions were set depending on predictabilities about perturbation occurrence and onset: No perturbation, No Cue, and Cue conditions. In the Cue condition, an acoustic signal was given as timing information of perturbation. The slope of the stimulus–response relation curve revealed that the TA-MEP was enhanced when postural perturbation was expected compared to when the perturbation was not expected (No Perturbation vs. No Cue, 0.023 ± 0.004 vs. 0.042 ± 0.007; No Perturbation vs. Cue, 0.023 ± 0.004 vs. 0.050 ± 0.009; Bonferroni correction, p = 0.01, respectively). In addition, two-way analysis of variance (intensity × condition) revealed the main effect of condition (F(1,13) = 6.31, p = 0.03) but not intensity and interaction when the MEP amplitude of the Cue and No Cue conditions was normalized by that in No Perturbation, suggesting the enhancement more apparent when timing information was given. The SOL-MEP was not modulated even when perturbation was expected, but it slightly reduced due to the timing information. The results of an additional experiment confirmed that the acoustic cue by itself did not affect the TA- and SOL-MEPs. Our findings suggest that a prediction of a future state of standing balance modulates the corticospinal excitability in the TA, and that the additional timing information facilitates this modulation. The corticospinal pathway thus appears to be involved in mechanisms of the predictive control as well as feedback control of standing posture.

Associations Between Types of Balance Performance in Healthy Individuals Across the Lifespan: A Systematic Review and Meta-Analysis

“…On the contrary, feedback control is characterized by the initiation of sufficient muscle responses after balance loss to compensate an unpredicted postural disturbance during one-legged standing and to avoid falling. In this respect, recent studies (Wälchli et al, 2017 ; Fujio et al, 2018 ) showed that the central nervous system differently prepares postural responses in expected compared to unexpected stance perturbations. For instance, Fujio et al ( 2018 ) examined motor-evoked potential (MEP) induced by transcranial magnetic stimulation during expected (via acoustic signal) and unexpected (no signal) perturbations, while standing on a moveable platform in healthy young adults (mean age: 27 ± 2 years).…”

“…In this respect, recent studies (Wälchli et al, 2017 ; Fujio et al, 2018 ) showed that the central nervous system differently prepares postural responses in expected compared to unexpected stance perturbations. For instance, Fujio et al ( 2018 ) examined motor-evoked potential (MEP) induced by transcranial magnetic stimulation during expected (via acoustic signal) and unexpected (no signal) perturbations, while standing on a moveable platform in healthy young adults (mean age: 27 ± 2 years). As a result, the MEP for the tibialis anterior muscle was significantly enhanced under expected compared to the unexpected stance perturbation.…”

Presetting of the Corticospinal Excitability in the Tibialis Anterior Muscle in Relation to Prediction of the Magnitude and Direction of Postural Perturbations

“…We calculated the peak-to-peak amplitude of each MEP within 40 ms after stimulus onset and compared the amplitudes among the five conditions. We set a reference value as deviation above 1.5× the interquartile range (IQR) from the 3rd-quartile and below 1.5× the IQR from the 1st-quartile as an outlier (Fujio et al, 2018). After the outliers were discarded, we compared the averaged MEP amplitude among the five conditions.…”

“…We conducted the present study to determine whether the corticospinal excitability in the ankle muscles is specific to the predictions about the magnitude and the direction of perturbations. Our experiments’ results aimed to further the understanding of recent finding that the prediction of future events related to postural stability is a key modulator of corticospinal excitability (Walchli et al, 2017; Fujio et al, 2018).…”

“…Not only when changing position from supine to standing but also when maintaining a posture under unstable environments (such as standing on a foam surface; Papegaaij et al, 2014), the corticospinal excitability is enhanced as the posture must be balanced (Obata et al, 2009; Baudry et al, 2015). The corticospinal excitability can also be enhanced when a postural perturbation is imminent, even though the posture is not actually perturbed (Walchli et al, 2017; Fujio et al, 2018). Notably, this modulation is more pronounced when the timing of the onset of a perturbation is known, which is consistent with the results of investigations of the long-latency response (Ackermann et al, 1991; Fujio et al, 2016).…”