Frequency‐dependent modulation of neural oscillations across the gait cycle

: Balance and walking are fundamental to support common daily activities. Relatively accurate characterizations of normal and impaired gait features were attained at the kinematic and muscular levels. Conversely, the neural processes underlying gait dynamics still need to be elucidated. To shed light on gait-related modulations of neural activity, we collected high-density electroencephalography (hdEEG) signals and ankle acceleration data in young healthy participants during treadmill walking. We used the ankle acceleration data to segment each gait cycle in four phases: initial double support, right leg swing, final double support, left leg swing. Then, we processed hdEEG signals to extract neural oscillations in alpha, beta, and gamma bands, and examined event-related desynchronization/synchronization (ERD/ERS) across gait phases. Our results showed that ERD/ERS modulations for alpha, beta, and gamma bands were strongest in the primary sensorimotor cortex (M1), but were also found in premotor cortex, thalamus and cerebellum. We observed a modulation of neural oscillations across gait phases in M1 and cerebellum, and an interaction between frequency band and gait phase in premotor cortex and thalamus. Furthermore, an ERD/ERS lateralization effect was present in M1 for the alpha and beta bands, and in the cerebellum for the beta and gamma bands. Overall, our findings demonstrate that an electrophysiological source imaging approach based on hdEEG can be used to investigate dynamic neural processes of gait control. Future work on the development of mobile hdEEG-based brain-body imaging platforms may enable overground walking investigations, with potential applications in the study of gait disorders

Examining Lower Extremity Motor Activity Using Magnetoencephalography

The role of the cortex during locomotion remains unclear, but recent advances in neural imaging technologies have aided in developing ways to measure brain activity during motor tasks. One method is by measuring activations produced by neural oscillations which have been associated with a variety of human behaviors, from sleep and rest to cognitive actions and movement. The physiological and functional methods in which oscillations contribute to cortical control are still largely unknown. In this study, we aim to expand that knowledge by examining human cortical activity in the sensory and motor cortices during pedaling using magnetoencephalography (MEG). We hypothesized that, if the sensory and motor cortices are important for controlling locomotion, then the MEG signal would differ during pedaling as compared to rest and would be modulated with the phase of the pedaling cycle. Moreover, if locomotor-related brain activity is solely caused by sensory feedback, then the MEG signal would be the same during active and passive pedaling. We scanned eight healthy subjects using MEG while they pedaled a custom-made pedaling device. The subjects’ magnetocortical activity was measured in two minute recordings during rest, continuous, self-paced active pedaling, and passive pedaling. The passive condition consisted of the subject relaxing their leg muscles while the experimenter pedaled the device for them at a velocity matching that subject’s active pedaling bout. Task-dependent magnetocortical activity was examined in the primary sensorimotor cortex (M1 and S1), supplemental motor area (SMA), and premotor area (PMA). The power spectrum of the MEG signal during the different tasks was extracted using a Welch periodogram to examine the frequency content throughout each task. The power in the alpha and beta bands of all regions of interest decreased significantly during active and passive pedaling as compared to rest. No significant difference was found between any of the tasks in the gamma band. The temporal pattern of the beta frequency band was also examined across the pedaling cycle by performing a time-frequency decomposition using a Morlet wavelet. Both pedaling conditions demonstrated modulation of the beta band at twice the pedaling frequency. These fluctuations were not found in the rest condition. Our results showed that the brain becomes engaged during pedaling as compared to rest. The magnetocortical activity is different across the movement cycle, suggesting that the brain has input into the regulation of locomotor-like movement. There is also a strong sensory component during movement since the active and passive pedaling conditions are similar

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

Cortical Oscillations During a Lateral Balance Perturbation While Walking

The role of sensory systems in the cortical control of dynamic balance was examined using electroencephalography (EEG) recordings during balance perturbations while walking. Specifically, we examined the impact of sensory deficits on cortical oscillations using vibratory stimuli to suppress sensory feedback and by comparing cortical oscillations during balance perturbations while walking in people with sensory deficits associated with cervical myelopathy and neurologically intact controls. Balance during walking provides a rich framework for investigating cortical control using EEG during a functionally relevant task. While this approach is promising, substantial technical challenges remain in recording and processing EEG in the noisy, artifact laden environment associated with walking. We therefore first investigated the role of sensory attenuation in healthy, adult controls within the framework of a simple, motor task. We then examined the effectiveness of using independent component analysis and additional machine learning techniques such as clustering and linear classifiers for differentiating noise from actual brain activity in EEG signals during walking. Finally, we examined a more complicated experimental framework using a custom cable-servomotor system to deliver a lateral pull to the waist of participants with cervical myelopathy while walking and measured their cortical activity using high density EEG. We observed that the attenuation of sensory input in healthy controls induced a similar change in beta band modulation as found previously in spinal cord injury for simple movements of the ankle. During walking, large increases in theta band power throughout the cortex were observed to modulate with lateral balance perturbations. Theta band modulations in the frontal areas of the cortex were significantly delayed in time and displayed a more spatially lateralized cortical localization for participants with cervical myelopathy compared to age-matched, healthy controls. The timing of these theta power modulations were significantly correlated with the initiation of a widening step width correction in response to the balance perturbation. Our results support a link between the modulation of cortical oscillations and sensorimotor integration in simple and complex motor paradigms

Current state and future prospects of EEG and fNIRS in robot-assisted gait rehabilitation : a brief review

Gait and balance impairments are frequently considered as the most significant concerns among individuals suffering from neurological diseases. Robot-assisted gait training (RAGT) has shown to be a promising neurorehabilitation intervention to improve gait recovery in patients following stroke or brain injury by potentially initiating neuroplastic changes. However, the neurophysiological processes underlying gait recovery through RAGT remain poorly understood. As non-invasive, portable neuroimaging techniques, electroencephalography (EEG) and functional near-infrared spectroscopy (fNIRS) provide new insights regarding the neurophysiological processes occurring during RAGT by measuring different perspectives of brain activity. Due to spatial information about changes in cortical activation patterns and the rapid temporal resolution of bioelectrical changes, more features correlated with brain activation and connectivity can be identified when using fused EEG-fNIRS, thus leading to a detailed understanding of neurophysiological mechanisms underlying motor behavior and impairments due to neurological diseases. Therefore, multi-modal integrations of EEG-fNIRS appear promising for the characterization of neurovascular coupling in brain network dynamics induced by RAGT. In this brief review, we surveyed neuroimaging studies focusing specifically on robotic gait rehabilitation. While previous studies have examined either EEG or fNIRS with respect to RAGT, a multi-modal integration of both approaches is lacking. Based on comparable studies using fused EEG-fNIRS integrations either for guiding non-invasive brain stimulation (NIBS) or as part of brain-machine interface (BMI) paradigms, the potential of this methodologically combined approach in RAGT is discussed. Future research directions and perspectives for targeted, individualized gait recovery that optimize the outcome and efficiency of RAGT in neurorehabilitation were further derived

The neural response is heightened when watching a person approaching compared to walking away: Evidence for dynamic social neuroscience

The action observation network has been proposed to play a key role in predicting the action intentions (or goals) of others, thereby facilitating social interaction. Key information when interacting with others is whether someone (an agent) is moving towards or away from us, indicating whether we are likely to interact with the person. In addition, to determine the nature of a social interaction, we also need to take into consideration the distance of the agent relative to us as the observer. How this kind of information is processed within the brain is unknown, at least in part because prior studies have not involved live whole-body motion. Consequently, here we recorded mobile EEG in 18 healthy participants, assessing the neural response to the modulation of direction (walking towards or away) and distance (near vs. far distance) during the observation of an agent walking. We evaluated whether cortical alpha and beta oscillations were modulated differently by direction and distance during action observation. We found that alpha was only modulated by distance, with a stronger decrease of power when the agent was further away from the observer, regardless of direction. Critically, by contrast, beta was found to be modulated by both distance and direction, with a stronger decrease of power when the agent was near and facing the participant (walking towards) compared to when they were near but viewed from the back (walking away). Analysis revealed differences in both the timing and distribution of alpha and beta oscillations. We argue that these data suggest a full understanding of action observation requires a new dynamic neuroscience, investigating actual interactions between real people, in real world environments

Mobile EEG reveals functionally dissociable dynamic processes supporting real-world ambulatory obstacle avoidance : evidence for early proactive control

This work is supported by a scholarship from the University of Stirling and a reseach grant from SINAPSE (Scottish Imaging Network: A Platform for Scientific excellence). GL is supported by the Wellcome Trust [209209/Z/17/Z].The ability to safely negotiate the world on foot takes humans years to develop, reflecting the huge cognitive demands associated with real‐time planning and control of walking. Despite the importance of walking, methodological limitations mean that surprisingly little is known about the neural and cognitive processes that support ambulatory motor control. Here, we report mobile EEG data recorded from thirty‐two healthy young adults during real‐world ambulatory obstacle avoidance. Participants walked along a path while stepping over expected and unexpected obstacles projected on the floor, allowing us to capture the dynamic oscillatory response to changes in environmental demands. Compared to obstacle‐free walking, time‐frequency analysis of the EEG data revealed clear frontal theta and centro‐parietal beta power neural markers of proactive and reactive forms of movement control (occurring before and after crossing an obstacle). Critically, the temporal profile of changes in frontal theta allowed us to arbitrate between early selection and late adaptation mechanisms of proactive control. Our data show that motor plans are updated as soon as an upcoming obstacle appears, rather than when the obstacle is reached. In addition, regardless of whether motor plans required updating, a clear beta rebound was present after obstacles were crossed, reflecting the resetting of the motor system. Overall, mobile EEG recorded during real‐world walking provides novel insight into the cognitive and neural basis of dynamic motor control in humans, suggesting new routes to the monitoring and rehabilitation of motor disorders such as dyspraxia and Parkinson’s disease.Publisher PDFPeer reviewe

Slow Potentials of the Sensorimotor Cortex during Rhythmic Movements of the Ankle

The objective of this dissertation was to more fully understand the role of the human brain in the production of lower extremity rhythmic movements. Throughout the last century, evidence from animal models has demonstrated that spinal reflexes and networks alone are sufficient to propagate ambulation. However, observations after neural trauma, such as a spinal cord injury, demonstrate that humans require supraspinal drive to facilitate locomotion. To investigate the unique nature of lower extremity rhythmic movements, electroencephalography was used to record neural signals from the sensorimotor cortex during three cyclic ankle movement experiments. First, we characterized the differences in slow movement-related cortical potentials during rhythmic and discrete movements. During the experiment, motion analysis and electromyography were used characterize lower leg kinematics and muscle activation patterns. Second, a custom robotic device was built to assist in passive and active ankle movements. These movement conditions were used to examine the sensory and motor cortical contributions to rhythmic ankle movement. Lastly, we explored the differences in sensory and motor contributions to bilateral, rhythmic ankle movements. Experimental results from all three studies suggest that the brain is continuously involved in rhythmic movements of the lower extremities. We observed temporal characteristics of the cortical slow potentials that were time-locked to the movement. The amplitude of these potentials, localized over the sensorimotor cortex, revealed a reduction in neural activity during rhythmic movements when compared to discrete movements. Moreover, unilateral ankle movements produced unique sensory potentials that tracked the position of the movement and motor potentials that were only present during active dorsiflexion. In addition, the spatiotemporal patterns of slow potentials during bilateral ankle movements suggest similar cortical mechanisms for both unilateral and bilateral movement. Lastly, beta frequency modulations were correlated to the movement-related slow potentials within medial sensorimotor cortex, which may indicate they are of similar cortical origin. From these results, we concluded that the brain is continuously involved in the production of lower extremity rhythmic movements, and that the sensory and motor cortices provide unique contributions to both unilateral and bilateral movemen

What Are Spectral and Spatial Distributions of EEG-EMG Correlations in Overground Walking? An Exploratory Study

You probably believe that a latent relationship between the brain and lower limbs exists and it varies across different walking conditions (e.g., walking with or without an exoskeleton). Have you ever thought what the distributions of measured signals are? To address this question, we simultaneously collected electroencephalogram (EEG) and electromyogram (EMG) signals while healthy participants were conducting four overground walking conditions without any constraints (e.g., specific speed). The EEG results demonstrated that a wide range of frequencies from delta band to gamma band were involved in walking. The EEG power spectral density (PSD) was significantly different in sensorimotor and posterior parietal areas between exoskeleton-assisted walking and non-exoskeleton walking. The EMG PSD difference was predominantly observed in the theta band and the gastrocnemius lateralis muscle. EEG-EMG PSD correlations differed among walking conditions. The alpha and beta bands were primarily involved in consistently increasing EEG-EMG PSD correlations across the walking conditions, while the theta band was primarily involved in consistently decreasing correlations as observed in the EEG involvement. However, there is no dominant frequency band as observed in the EMG involvement. Channels located over the sensorimotor area were primarily involved in consistently decreasing EEG-EMG PSD correlations and the outer-ring channels were involved in the increasing EEG-EMG PSD correlations. Our study revealed the spectral and spatial distributions relevant to overground walking and deepened the understanding of EEG and EMG representations during locomotion, which may inform the development of a more human-compatible exoskeleton and its usage in motor rehabilitation