Neural coupling between upper and lower limb muscles in Parkinsonian gait.

OBJECTIVE: To explore to what extent neuronal coupling between upper and lower limb muscles during gait is preserved or affected in patients with Parkinson's Disease (PD). METHODS: Electromyography recordings were obtained from the bilateral deltoideus anterior and bilateral rectus femoris and biceps femoris muscles during overground gait in 20 healthy participants (median age 69 years) and 20 PD patients (median age 68.5 years). PD patients were able to walk independently (Hoehn and Yahr scale: Stage 2-3), had an equally distributed symptom laterality (6 left side, 7 both sides and 7 right side) and no cognitive problems or tremor dominant PD. Time-dependent directional intermuscular coherence analysis was employed to compare the neural coupling between upper and lower limb muscles between healthy participants and PD patients in three different directions: zero-lag (i.e. common driver), forward (i.e. shoulders driving the legs) and reverse component (i.e. legs driving the shoulders). RESULTS: Compared to healthy participants, PD patients exhibited (i) reduced intermuscular zero-lag coherence in the beta/gamma frequency band during end-of-stance and (ii) enhanced forward as well as reverse directed coherence in the alpha and beta/gamma frequency bands around toe-off. CONCLUSIONS: PD patients had a reduced common cortical drive to upper and lower limb muscles during gait, possibly contributing to disturbed interlimb coordination. Enhanced bidirectional coupling between upper and lower limb muscles on subcortical and transcortical levels in PD patients suggests a mechanism of compensation. SIGNIFICANCE: These findings provide support for the facilitating effect of arm swing instructions in PD gait.

Time-dependent directional intermuscular coherence analysis reveals that forward and backward arm swing equally drive the upper leg muscles during gait initiation.

BACKGROUND: Human bipedal gait benefits from arm swing, as it drives and shapes lower limb muscle activity in healthy participants as well as patients suffering from neurological impairment. Also during gait initiation, arm swing instructions were found to facilitate leg muscle recruitment. RESEARCH QUESTION: The aim of the present study is to exploit the directional decomposition of coherence to examine to what extent forward and backward arm swing contribute to leg muscle recruitment during gait initiation. METHODS: Ambulant electromyography (EMG) from shoulder muscles (deltoideus anterior and posterior) and upper leg muscles (biceps femoris and rectus femoris) was analysed during gait initiation in nineteen healthy participants (median age of 67 ± 12 (IQR) years). To assess to what extent either deltoideus anterior or posterior muscles were able to drive upper leg muscle activity during distinct stages of the gait initiation process, time dependent intermuscular coherence was decomposed into directional components based on their time lag (i.e. forward, reverse and zero-lag). RESULTS: Coherence from the forward directed components, representing shoulder muscle signals leading leg muscle signals, revealed that deltoideus anterior (i.e. forward arm swing) and deltoideus posterior (i.e. backward arm swing) equally drive upper leg muscle activity during the gait initiation process. SIGNIFICANCE: The presently demonstrated time dependent directional intermuscular coherence analysis could be of use for future studies examining directional coupling between muscles or brain areas relative to certain gait (or other time) events. In the present study, this analysis provided neural underpinning that both forward and backward arm swing can provide neuronal support for leg muscle recruitment during gait initiation and can therefore both serve as an effective gait rehabilitation method in patients with gait initiation difficulties.

Enhanced arm swing improves Parkinsonian gait with EEG power modulations resembling healthy gait.

BACKGROUND: The supplementary motor area (SMA) is implicated in stereotypic multi-limb movements such as walking with arm swing. Gait difficulties in Parkinson's Disease (PD) include reduced arm swing, which is associated with reduced SMA activity. OBJECTIVE: To test whether enhanced arm swing improves Parkinsonian gait and explore the role of the SMA in such an improvement. METHODS: Cortical activity and gait characteristics were assessed by ambulant EEG, accelerometers and video recordings in 27 PD patients with self-reported gait difficulties and 35 healthy participants when walking normally. Within these two groups, 19 PD patients additionally walked with enhanced arm swing and 30 healthy participants walked without arm swing. Power changes across the EEG frequency spectrum were assessed by Event Related Spectral Perturbation analysis of recordings from Fz over the putative SMA and gait analysis was performed. RESULTS: Baseline PD gait, characterized by reduced arm swing among other features, exhibited reduced within-step Event Related Desynchronization (ERD)/Synchronization (ERS) alternation (Fz; 20-50Hz), accompanied by a reduced step length and walking speed. All became similar to normal gait when patients walked with enhanced arm swing. When healthy controls walked without arm swing, their alternating ERD-ERS pattern decreased, mimicking baseline PD gait. CONCLUSION: Enhanced arm swing may serve as a driving force to overcome impaired gait control in PD patients by restoring reduced ERD-ERS alternation over the putative SMA. Accompanied by increased step length and walking speed, this provides a neural underpinning of arm swing as an effective rehabilitation concept for improving Parkinsonian gait.

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

BACKGROUND: Walking is characterized by stable antiphase relations between upper and lower limb movements. Such bilateral rhythmic movement patterns are neuronally generated at levels of the spinal cord and brain stem, that are strongly interconnected with cortical circuitries, including the Supplementary Motor Area (SMA). OBJECTIVE: To explore cerebral activity associated with multi-limb phase relations in human gait by manipulating mutual attunement of the upper and lower limb antiphase patterns. METHODS: Cortical activity and gait were assessed by ambulant EEG, accelerometers and videorecordings in 35 healthy participants walking normally and 19 healthy participants walking in amble gait, where upper limbs moved in-phase with the lower limbs. Power changes across the EEG frequency spectrum were assessed by Event Related Spectral Perturbation analysis and gait analysis was performed. RESULTS: Amble gait was associated with enhanced Event Related Desynchronization (ERD) prior to and during especially the left swing phase and reduced Event Related Synchronization (ERS) at final swing phases. ERD enhancement was most pronounced over the putative right premotor, right primary motor and right parietal cortex, indicating involvement of higher-order organization and somatosensory guidance in the production of this more complex gait pattern, with an apparent right hemisphere dominance. The diminished within-step ERD/ERS pattern in amble gait, also over the SMA, suggests that this gait pattern is more stride driven instead of step driven. CONCLUSION: Increased four-limb phase complexity recruits distributed networks upstream of the primary motor cortex, primarily lateralized in the right hemisphere. Similar parietal-premotor involvement has been described to compensate impaired SMA function in Parkinson's disease bimanual antiphase movement, indicating a role as cortical support regions.

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

KEY POINTS: Gait-related arm swing in humans supports efficient lower limb muscle activation, indicating a neural coupling between the upper and lower limbs during gait. Intermuscular coherence analyses of gait-related electromyography from upper and lower limbs in 20 healthy participants identified significant coherence in alpha and beta/gamma bands indicating that upper and lower limbs share common subcortical and cortical drivers that coordinate the rhythmic four-limb gait pattern. Additional directed connectivity analyses revealed that upper limb muscles drive and shape lower limb muscle activity during gait via subcortical and cortical pathways and to a lesser extent vice versa. The results provide a neural underpinning that arm swing may serve as an effective rehabilitation therapy concerning impaired gait in neurological diseases. ABSTRACT: Human gait benefits from arm swing, as it enhances efficient lower limb muscle activation in healthy participants as well as patients suffering from neurological impairment. The underlying neuronal mechanisms of such coupling between upper and lower limbs remain poorly understood. The aim of the present study was to examine this coupling by intermuscular coherence analysis during gait. Additionally, directed connectivity analysis of this coupling enabled assessment of whether gait-related arm swing indeed drives lower limb muscles. To that end, electromyography recordings were obtained from four lower limb muscles and two upper limb muscles bilaterally, during gait, of 20 healthy participants (mean (SD) age 67 (6.8) years). Intermuscular coherence analysis revealed functional coupling between upper and lower limb muscles in the alpha and beta/gamma band during muscle specific periods of the gait cycle. These effects in the alpha and beta/gamma bands indicate involvement of subcortical and cortical sources, respectively, that commonly drive the rhythmic four-limb gait pattern in an efficiently coordinated fashion. Directed connectivity analysis revealed that upper limb muscles drive and shape lower limb muscle activity during gait via subcortical and cortical pathways and to a lesser extent vice versa. This indicates that gait-related arm swing reflects the recruitment of neuronal support for optimizing the cyclic movement pattern of the lower limbs. These findings thus provide a neural underpinning for arm swing to potentially serve as an effective rehabilitation therapy concerning impaired gait in neurological diseases.

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

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.

EEG time-frequency analysis provides arguments for arm swing support in human gait control.

BACKGROUND: Human gait benefits from arm swing, which requires four-limb co-ordination. The Supplementary Motor Area (SMA) is involved in multi-limb coordination. With its location anterior to the leg motor cortex and the pattern of its connections, this suggests a distinct role in gait control. RESEARCH QUESTION: Is the SMA functionally implicated in gait-related arm swing? METHODS: Ambulant electroencephalography (EEG) was employed during walking with and without arm swing in twenty healthy subjects (mean age: 64.9yrs, SD 7.2). Power changes across the EEG frequency spectrum were assessed by Event Related Spectral Perturbation (ERSP) analysis over both the putative SMA at electrode position Fz and additional sensorimotor regions. RESULTS: During walking with arm swing, midline electrodes Fz and Cz showed a step-related pattern of Event Related Desynchronization (ERD) followed by Event Related Synchronization (ERS). Walking without arm swing was associated with significant ERD-ERS power reduction in the high-beta/low-gamma band over Fz and a power increase over Cz. Electrodes C3 and C4 revealed a pattern of ERD during contralateral- and ERS during ipsilateral leg swing. This ERD power decreased in gait without arm swing (low-frequency band). The ERSP pattern during walking with arm swing was similar at CP1 and CP2: ERD was seen during double support and the initial swing phase of the right leg, while a strong ERS emerged during the second half of the left leg's swing. Walking without arm swing showed a significant power reduction of this ERD-ERS pattern over CP2, while over CP1, ERS during left leg's swing turned into ERD. CONCLUSION: The relation between arm swing in walking and a step-related ERD-ERS pattern in the high-beta/low-gamma band over the putative SMA, points at an SMA contribution to integrated cyclic anti-phase movements of upper- and lower limbs. This supports a cortical underpinning of arm swing support in gait control.