Pre-Movement Cortico-Muscular Dynamics Underlying Improved Parkinson Gait Initiation after Instructed Arm Swing

Abstract

Background: The supplementary motor area (SMA) is implicated in both motor initiation and stereotypic multi-limb movements such as walking with arm swing. Gait in Parkinson’s disease exhibits starting difficulties and reduced arm swing, consistent with reduced SMA activity. Objective: We tested whether enhanced arm swing could improve Parkinson gait initiation and assessed whether increased SMA activity during preparation might facilitate such improvement. Methods: Effects of instructed arm swing on cortical activity, muscle activity and kinematics were assessed by ambulant EEG, EMG, accelerometers and video in 17 Parkinson patients and 19 controls. At baseline, all participants repeatedly started walking after a simple auditory cue. Next, patients started walking at this cue, which now meant starting with enhanced arm swing. EEG changes over the putative SMA and leg motor cortex were assessed by event related spectral perturbation (ERSP) analysis of recordings at Fz and Cz. Results: Over the putative SMA location (Fz), natural PD gait initiation showed enhanced alpha/theta synchronization around the auditory cue, and reduced alpha/beta desynchronization during gait preparation and movement onset, compared to controls. Leg muscle activity in patients was reduced during preparation and movement onset, while the latter was delayed compared to controls. When starting with enhanced arm swing, these group differences virtually disappeared. Conclusion: Instructed arm swing improves Parkinson gait initiation. ERSP normalization around the cue indicates that the attributed information may serve as a semi-internal cue, recruiting an internalized motor program to overcome initiation difficulties.

Intermuscular coherence analysis in older adults reveals that gait‐related arm swing drives lower limb muscles via subcortical and cortical pathways

“…The supplementary motor area is a midline cortical area located anterior of the primary motor cortex, which has strong and widespread connections with the motor field of the contralateral cortex and is therefore also a good candidate for the cortical source involved in this interlimb coupling during gait (Rouiller et al 1994;Ruddy et al 2017). The presently observed directional coupling between shoulder and leg muscles is in line with previous reports of rhythmic upper limb movements affecting reflex responses in lower limb movements (Cerri et al 2003;Frigon et al 2004;Palomino et al 2011;Massaad et al 2014) and provides a neural underpinning for previous observations that the addition of upper limb movements to lower limb movements during rhythmic movement did improve lower limb muscle recruitment in healthy participants (Jakobi & Chilibeck, 2001;Huang & Ferris, 2004Kao & Ferris, 2005;de Kam et al 2013b) and neurologically impaired patients (Zehr et al 2012;de Kam et al 2013a;Weersink et al 2020). On both subcortical (i.e.…”

“…Gait-related arm swing contributes to stabilization (Hof, 2007;Ortega et al 2008) and energetic efficiency (Ortega et al 2008;Umberger, 2008;Yizhar et al 2009) and is also thought to evoke neuronal support for maintaining the cyclic motor pattern (Massaad et al 2014;Weersink et al 2019). This is confirmed by previous studies where adding upper limb movements to lower limb movements during rhythmic tasks improved lower limb muscle recruitment in healthy participants (Huang & Ferris, 2004Kao & Ferris, 2005;de Kam et al 2013b;Ogawa et al 2015) and neurologically impaired patients, such as patients with Parkinson's disease (Weersink et al 2018(Weersink et al , 2020, stroke (Zehr et al 2012) or spinal cord injury (de Kam et al 2013a). Patients with incomplete spinal cord injury and spastic paresis also displayed more efficient lower limb muscle activation when stepping with partial body weight support from a harness, i.e.…”

“…2015) and neurologically impaired patients, such as patients with Parkinson's disease (Weersink et al . 2018, 2020), stroke (Zehr et al . 2012) or spinal cord injury (de Kam et al .…”

Amble Gait EEG Points at Complementary Cortical Networks Underlying Stereotypic Multi-Limb Co-ordination

“…One might infer that the switch from such prominent ERD-ERS alternation into gradual ERD fluctuation reflects a reduction of the optimal balance between movement initiation and inhibition across the two hemispheres, which is considered to be an important SMA contribution to regularly tuned antiphase movements of the opposite hands ( Brinkman, 1981 ; Stephan et al, 1999 ; Potgieser et al, 2014 ). In a similar way, antiphase arm swing is thought to serve efficient gait control ( Collins et al, 2009 ; Kuhtz-Buschbeck and Jing, 2012 ; De Graaf et al, 2019 ; Weersink et al, 2019 , 2020 ). In the less efficient amble gait condition, antiphase movement of upper limbs is maintained, as in normal gait.…”

“…However, it should be considered that in gait, antiphase movements are generated by proximal limb muscles while the referred experimental paradigms concerned distal limb movements. The concept that one of the SMA contributions to gait control concerns the effective recruitment of arm swing is supported by the association between reduced SMA activity and (i) the experimental condition of gait without arm swing and (ii) the circumstance of Parkinson’s disease (PD), a disease characterized by small-step walking with reduced or absent arm swing ( Jenkins et al, 1992 ; Jahanshahi et al, 1995 ; Sabatini et al, 2000 ; Weersink et al, 2019 , 2020 ). The fact that the instruction to start walking with enhanced arm swing results in an improvement of gait initiation in PD patients, associated with virtual normalization of SMA activity, further supports the idea that upper-limb antiphase movement intrinsically serves efficient gait control, mediated by the SMA ( Weersink et al, 2020 ).…”