Arm swing in healthy and Parkinsonian gait:explorations on brain, muscle and movement level

Human bipedal gait exhibits a coherent four-limb movement pattern comparable to that observed in quadrupedal gait, with upper limbs swinging in anti-phase with both opposite upper and ipsilateral lower limbs. Although the role of these upper limb movements in bipedal gait is not as obvious as in quadrupedal gait, one proposed advantage concerns the modulation of neural control to maintain the cyclic gait pattern. This dissertation broadens the knowledge on this supporting role of arm swing in gait control in healthy participants and patients with Parkinson’s Disease (PD), a neurodegenerative disease that affects both lower-limb gait and gait-related arm swing. We used a multi-level approach including electroencephalography, electromyography and gait analyses to explore how this is organized within and between brain, muscle and movement level, respectively. We demonstrated that arm swing can drive and shape lower limb muscle activity via subcortical and cortical pathways, in which the supplementary motor area plays a central role. As a result of this neural interlimb coupling, we found that disturbed upper and lower limb movements in PD gait are correlated. These findings provide neural support for the observed facilitating effect of arm swing instructions on gait initiation and continued gait in PD patients. Overall, this dissertation supports that arm swing instructions or exercises could potentially be used as an effective non-invasive gait rehabilitation method in PD patients

Correlations of Gait Phase Kinematics and Cortical EEG: Modelling Human Gait with Data from Sensors

Neural coding of gait intent and continuous gait kinematics have advanced brain computer interface (BCI) technology for detection and predicting human upright walking movement. However, the dynamics of cortical involvement in upright walking and upright standing has not been clearly understood especially with the focus of off-laboratory assessments. In this study, wearable low-cost mobile phone accelerometers were used to extract position and velocity at 12 joints during walking and the cortical changes involved during gait phases of walking were explored using non-invasive electroencephalogram (EEG). Extracted gait data included, accelerometer values proximal to brachium of arm, antecubitis, carpus, coxal, femur and tarsus by considering physical parameters including height, weight and stride length. Including EEG data as features, the spectral and temporal features were used to classify and predict the swing and stance instances for healthy subjects. While focusing on stance and swing classification in healthy subjects, this chapter relates to gait features that help discriminate walking movement and its neurophysiological counterparts. With promising initial results, further exploration of gait may help change detection of movement neurological conditions in regions where specialists and clinical facilities may not be at par

Information decomposition of multichannel EMG to map functional interactions in the distributed motor system

The central nervous system needs to coordinate multiple muscles during postural control. Functional coordination is established through the neural circuitry that interconnects different muscles. Here we used multivariate information decomposition of multichannel EMG acquired from 14 healthy participants during postural tasks to investigate the neural interactions between muscles. A set of information measures were estimated from an instantaneous linear regression model and a time-lagged VAR model fitted to the EMG envelopes of 36 muscles. We used network analysis to quantify the structure of functional interactions between muscles and compared them across experimental conditions. Conditional mutual information and transfer entropy revealed sparse networks dominated by local connections between muscles. We observed significant changes in muscle networks across postural tasks localized to the muscles involved in performing those tasks. Information decomposition revealed distinct patterns in task-related changes: unimanual and bimanual pointing were associated with reduced transfer to the pectoralis major muscles, but an increase in total information compared to no pointing, while postural instability resulted in increased information, information transfer and information storage in the abductor longus muscles compared to normal stability. These findings show robust patterns of directed interactions between muscles that are task-dependent and can be assessed from surface EMG recorded during static postural tasks. We discuss directed muscle networks in terms of the neural circuitry involved in generating muscle activity and suggest that task-related effects may reflect gain modulations of spinal reflex pathways

Rhythmic neural activity is comodulated with short-term gait modifications during first-time use of a dummy prosthesis:a pilot study

BACKGROUND: After transfemoral amputation, many hours of practice are needed to re-learn walking with a prosthesis. The long adaptation process that consolidates a novel gait pattern seems to depend on cerebellar function for reinforcement of specific gait modifications, but the precise, step-by-step gait modifications (e.g., foot placement) most likely rely on top-down commands from the brainstem and cerebral cortex. The aim of this study was to identify, in able-bodied individuals, the specific modulations of cortical rhythms that accompany short-term gait modifications during first-time use of a dummy prosthesis. METHODS: Fourteen naïve participants walked on a treadmill without (one block, 4 min) and with a dummy prosthesis (three blocks, 3 × 4 min), while ground reaction forces and 32-channel EEG were recorded. Gait cycle duration, stance phase duration, step width, maximal ground reaction force and, ground reaction force trace over time were measured to identify gait modifications. Independent component analysis of EEG data isolated brain-related activity from distinct anatomical sources. The source-level data were segmented into gait cycles and analyzed in the time-frequency domain to reveal relative enhancement or suppression of intrinsic cortical oscillations. Differences between walking conditions were evaluated with one-way ANOVA and post-hoc testing (α = 0.05). RESULTS: Immediate modifications occurred in the gait parameters when participants were introduced to the dummy prosthesis. Except for gait cycle duration, these modifications remained throughout the duration of the experimental session. Power modulations of the theta, mu, beta, and gamma rhythms, of sources presumably from the fronto-central and the parietal cortices, were found across the experimental session. Significant power modulations of the theta, beta, and gamma rhythms within the gait cycle were predominately found around the heel strike of both feet and the swing phase of the right (prosthetic) leg. CONCLUSIONS: The modulations of cortical activity could be related to whole-body coordination, including the swing phase and placing of the prosthesis, and the bodyweight transfer between legs and arms. Reduced power modulation of the gamma rhythm within the experimental session may indicate initial motor memories being formed. Better understanding of the sensorimotor processes behind gait modifications may inform the development of neurofeedback strategies to assist gait rehabilitation

Corticomuscular interactions during different movement periods in a multi-joint compound movement

While much is known about motor control during simple movements, corticomuscular communication profiles during compound movement control remain largely unexplored. Here, we aimed at examining frequency band related interactions between brain and muscles during different movement periods of a bipedal squat (BpS) task utilizing regression corticomuscular coherence (rCMC), as well as partial directed coherence (PDC) analyses. Participants performed 40 squats, divided into three successive movement periods (Eccentric (ECC), Isometric (ISO) and Concentric (CON)) in a standardized manner. EEG was recorded from 32 channels specifically-tailored to cover bilateral sensorimotor areas while bilateral EMG was recorded from four main muscles of BpS. We found both significant CMC and PDC (in beta and gamma bands) during BpS execution, where CMC was significantly elevated during ECC and CON when compared to ISO. Further, the dominant direction of information flow (DIF) was most prominent in EEG-EMG direction for CON and EMG-EEG direction for ECC. Collectively, we provide novel evidence that motor control during BpS is potentially achieved through central motor commands driven by a combination of directed inputs spanning across multiple frequency bands. These results serve as an important step toward a better understanding of brain-muscle relationships during multi joint compound movements.V.V.N was supported by the HSE Basic Research Program and the Russian Academic Excellence Project '5–100'. This study was supported by the Max-Planck Society

The development of functional and directed corticomuscular connectivity during tonic ankle muscle contraction across childhood and adolescence

In adults, oscillatory activity in the sensorimotor cortex is coherent with contralateral muscle activity at beta frequencies (15-35 Hz) during tonic contraction. This functional coupling reflects the involvement of the sensorimotor cortex, the corticospinal pathway, and likely also ascending sensory feedback in the task at hand. However, little is known about the developmental trajectory of task-related corticomuscular connectivity relating to the voluntary control of the ankle muscles. To address this, we recorded electroencephalography (EEG) from the vertex (Cz) and electromyography (EMG) from ankle muscles (proximal and distal anterior tibial, TA; soleus, SOL; gastrocnemius medialis, GM) in 33 participants aged 7-23 yr during tonic dorsi- and plantar flexion requiring precise maintenance of a submaximal torque level. Coherence was calculated for Cz-TA, Cz-SOL, TA-TA, and SOL-GM signal pairs. We found strong, positive associations between age and beta band coherence for Cz-TA, Cz-SOL, and TA-TA, suggesting that oscillatory corticomuscular connectivity is strengthened during childhood development and adolescence. Directionality analysis indicated that the primary interaction underlying this age-related increase was in the descending direction. In addition, performance during dorsi- and plantar flexion tasks was positively associated with age, indicating more precise control of the ankle joint in older participants. Performance was also positively associated with beta band coherence, suggesting that participants with greater coherence also exhibited greater precision. We propose that these results indicate an age-related increase in oscillatory corticospinal input to the ankle muscle motoneuron pools during childhood development and adolescence, with possible implications for maturation of precision force control. Within the theoretical framework of predictive coding, we suggest that our results may reflect an age-related increase in reliance on feedforward control as the developing nervous system becomes better at predicting the sensory consequences of movement. These findings may contribute to the development of novel intervention strategies targeting improved sensorimotor control in children and adolescents with central motor disorders

Control of human gait stability through foot placement

During human walking, the centre of mass (CoM) is outside the base of support for most of the time, which poses a challenge to stabilizing the gait pattern. Nevertheless, most of us are able to walk without substantial problems. In this review, we aim to provide an integrative overview of how humans cope with an underactuated gait pattern. A central idea that emerges from the literature is that foot placement is crucial in maintaining a stable gait pattern. In this review, we explore this idea; we first describe mechanical models and concepts that have been used to predict how foot placement can be used to control gait stability. These concepts, such as for instance the extrapolated CoM concept, the foot placement estimator concept and the capture point concept, provide explicit predictions on where to place the foot relative to the body at each step, such that gait is stabilized. Next, we describe empirical findings on foot placement during human gait in unperturbed and perturbed conditions. We conclude that humans show behaviour that is largely in accordance with the aforementioned concepts, with foot placement being actively coordinated to body CoM kinematics during the preceding step. In this section, we also address the requirements for such control in terms of the sensory information and the motor strategies that can implement such control, as well as the parts of the central nervous system that may be involved. We show that visual, vestibular and proprioceptive information contribute to estimation of the state of the CoM. Foot placement is adjusted to variations in CoM state mainly by modulation of hip abductor muscle activity during the swing phase of gait, and this process appears to be under spinal and supraspinal, including cortical, control. We conclude with a description of how control of foot placement can be impaired in humans, using ageing as a primary example and with some reference to pathology, and we address alternative strategies available to stabilize gait, which include modulation of ankle moments in the stance leg and changes in body angular momentum, such as rapid trunk tilts. Finally, for future research, we believe that especially the integration of consideration of environmental constraints on foot placement with balance control deserves attention

Unidirectional brain to muscle connectivity reveals motor cortex control of leg muscles during stereotyped walking.

In lower mammals, locomotion seems to be mainly regulated by subcortical and spinal networks. On the contrary, recent evidence suggests that in humans the motor cortex is also significantly engaged during complex locomotion tasks. However, a detailed understanding of cortical contribution to locomotion is still lacking especially during stereotyped activities. Here, we show that cortical motor areas finely control leg muscle activation during treadmill stereotyped walking. Using a novel technique based on a combination of Reliable Independent Component Analysis, source localization and effective connectivity, and by combining electroencephalographic (EEG) and electromyographic (EMG) recordings in able-bodied adults we were able to examine for the first time cortical activation patterns and cortico-muscular connectivity including information flow direction. Results not only provided evidence of cortical activity associated with locomotion, but demonstrated significant causal unidirectional drive from contralateral motor cortex to muscles in the swing leg. These insights overturn the traditional view that human cortex has a limited role in the control of stereotyped locomotion, and suggest useful hypotheses concerning mechanisms underlying gait under other conditions.One sentence summaryMotor cortex proactively drives contralateral swing leg muscles during treadmill walking, counter to the traditional view of stereotyped human locomotion