Modulation of corticospinal excitability and muscle synergies during visuomotor locomotor task in individuals with and without cerebral palsy: a TMS and EMG study

Introduction Studies using transcranial magnetic stimulation and electromyography suggest that disrupted functional corticospinal connectivity significantly contributes to difficulty in initiating and controlling voluntary movements such as walking. In individuals with Cerebral Palsy (CP), the corticospinal tract (CST) may therefore be identified as a potential target for improving gait control. Increasing corticospinal excitability may enhance voluntary control of lower-limb muscles and improve selective activation patterns during gait. However, it remains uncertain whether this pathway can be further activated given the damage caused by the brain lesion. Moreover, muscle synergies, a cooperative activation of groups of muscles, play an essential role in efficient and adaptive locomotion. Disrupted CST projections may reduce the specificity and strength of descending commands, which can lead to the fusion or splitting of muscle synergies. This impaired descending modulation could explain the reduced number of synergies and lower variance often reported in people with CP. Understanding and improving the modulation of these synergies could lead to better rehabilitation strategies for individuals with CP. The objective of this study was to assess whether a visuomotor walking task promotes an increase in corticospinal excitability and a modulation of muscle synergies compared to a simple walking task in individuals with CP. Methods Sixteen individuals with CP were initially recruited, muscle synergy analyses were conducted in 14 participants and TMS-based corticospinal excitability assessments in 11 participants, due to contraindications to TMS or technical issues. In addition, 14 control subjects took part in this study. Each participant performed a simple walking task and a visuomotor walking task (i.e., stepping onto virtual targets) at comfortable speed, in counterbalanced order. Transcranial magnetic stimulations were delivered during walking at approximately 40% of the gait cycle (late stance phase), corresponding to minimal tibialis anterior activity. Muscle synergies were extracted from full gait cycles recorded throughout each condition. Motor evoked potentials (MEPs) in the tibialis anterior muscle were induced using transcranial magnetic stimulation. Muscle synergies were extracted from surface electromyography signals acquired from six key lower-limb muscles during both tasks. Values were expressed as (median Q1–Q3). Results In the visuomotor task, MEPs increased by 59.4% in the CP group (simple task MEP = 1.89 1.00–3.09 a.u vs. visuomotor task MEP = 2.70 1.59–4.80 a.u; p ≤ 0.01) and 113.8% in the control group (simple task MEP = 1.95 0.99–2.72 a.u vs. visuomotor task MEP = 2.91 1.97–3.66 a.u; p ≤ 0.01). An increase in the number of synergies was observed during visuomotor task in CP group ( p = 0.018). Conclusion These results suggest that performing a visuomotor walking task allows to enhance the corticospinal excitability in both individuals with CP and control subjects. Moreover, CP individuals showed that either the number or the structure of synergies are modulated by the visuomotor task, in comparison to control subjects. Longitudinal studies are recommended to assess the impact of the integration of complex tasks in gait rehabilitation interventions.