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

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

Intramuscular coherence enables robust assessment of modulated supra-spinal input in human gait: an inter-dependence study of visual task and walking speed

Intramuscular high-frequency coherence is increased during visually guided treadmill walking as a consequence of increased supra-spinal input. The influence of walking speed on intramuscular coherence and its inter-trial reproducibility need to be established before adoption as a functional gait assessment tool in clinical settings. Here, fifteen healthy controls performed a normal and a target walking task on a treadmill at various speeds (0.3 m/s, 0.5 m/s, 0.9 m/s, and preferred) during two sessions. Intramuscular coherence was calculated between two surface EMG recordings sites of the Tibialis anterior muscle during the swing phase of walking. The results were averaged across low-frequency (5-14 Hz) and high-frequency (15-55 Hz) bands. The effect of speed, task, and time on mean coherence was assessed using three-way repeated measures ANOVA. Reliability and agreement were calculated with the intra-class correlation coefficient and Bland-Altman method, respectively. Intramuscular coherence during target walking was significantly higher than during normal walking across all walking speeds in the high-frequency band as obtained by the three-way repeated measures ANOVA. Interaction effects between task and speed were found for the low- and high-frequency bands, suggesting that task-dependent differences increase at higher walking speeds. Reliability of intramuscular coherence was moderate to excellent for most normal and target walking tasks in all frequency bands. This study confirms previous reports of increased intramuscular coherence during target walking, while providing first evidence for reproducibility and robustness of this measure as a requirement to investigate supra-spinal input.Trial registration Registry number/ClinicalTrials.gov Identifier: NCT03343132, date of registration 2017/11/17

Spectral properties of physiological mirror activity: An investigation of frequency features and common input between homologous muscles

During unilateral contractions, muscular activation can be detected in both active and resting limbs. In healthy populations, the latter is referred to as physiological mirror activity (pMA). The study of pMA holds implications for clinical applications as well as the understanding of bilateral motor control. However, the underlying mechanisms of pMA remain to be fully resolved. A commonality of prevailing explanatory approaches is the concept of shared neural input. With this study, we, therefore, aimed to investigate neural input in the form of multiple analyses of surface electromyography (sEMG) recordings in the frequency domain. For this purpose, 14 healthy, right-handed males aged 18-35 years were recruited. All participants performed a pinch-force task with the dominant hand in a blockwise manner. In total, 9 blocks of 5 contractions each were completed at 80% of maximum force output. Muscle activity was recorded via sEMG of the first dorsal interosseous muscle of the active and resting hand. We analyzed (1) spectral features as well as (2) intermuscular coherence (IMC). Our results demonstrate a blockwise increase in median frequency, mean frequency, and peak frequency in both hands. Frequency ratio analyses revealed a higher low-frequency component in the resting hand. Although we were able to demonstrate IMC on an individual level, results varied greatly and grand-averaged IMC failed to reach significance. Taken together, our findings imply an overlap of spectral properties between active and passive hands during repeated unilateral contractions. Combined with evidence from previous studies, this suggests a common neural origin between active and resting hands during unilateral contractions possibly resulting from a reduction in interhemispheric inhibition due to high force demands. Nevertheless, the exploratory nature of this study necessitates the classification of our results through follow-up studies

Intramuscular coherence enables robust assessment of modulated supra-spinal input in human gait : an inter-dependence study of visual task and walking speed

Intramuscular high-frequency coherence is increased during visually guided treadmill walking as a consequence of increased supra-spinal input. The influence of walking speed on intramuscular coherence and its inter-trial reproducibility need to be established before adoption as a functional gait assessment tool in clinical settings. Here, fifteen healthy controls performed a normal and a target walking task on a treadmill at various speeds (0.3 m/s, 0.5 m/s, 0.9 m/s, and preferred) during two sessions. Intramuscular coherence was calculated between two surface EMG recordings sites of the Tibialis anterior muscle during the swing phase of walking. The results were averaged across low-frequency (5-14 Hz) and high-frequency (15-55 Hz) bands. The effect of speed, task, and time on mean coherence was assessed using three-way repeated measures ANOVA. Reliability and agreement were calculated with the intra-class correlation coefficient and Bland-Altman method, respectively. Intramuscular coherence during target walking was significantly higher than during normal walking across all walking speeds in the high-frequency band as obtained by the three-way repeated measures ANOVA. Interaction effects between task and speed were found for the low- and high-frequency bands, suggesting that task-dependent differences increase at higher walking speeds. Reliability of intramuscular coherence was moderate to excellent for most normal and target walking tasks in all frequency bands. This study confirms previous reports of increased intramuscular coherence during target walking, while providing first evidence for reproducibility and robustness of this measure as a requirement to investigate supra-spinal input.Trial registration Registry number/ClinicalTrials.gov Identifier: NCT03343132, date of registration 2017/11/17

EEG-based investigation of cortical activity during Postural Control

The postural control system regulates the ability to maintain a stable upright stance and to react to changes in the external environment. Although once believed to be dominated by low-level reflexive mechanisms, mounting evidence has highlighted a prominent role of the cortex in this process. Nevertheless, the high-level cortical mechanisms involved in postural control are still largely unexplored. The aim of this thesis is to use electroencephalography, a widely used and non-invasive neuroimaging tool, to shed light on the cortical mechanisms which regulate postural control and allow balance to be preserved in the wake of external disruptions to one’s quiet stance. EEG activity has been initially analysed during a well-established postural task - a sequence of proprioceptive stimulations applied to the calf muscles to induce postural instability – traditionally used to examine the posturographic response. Preliminary results, obtained through a spectral power analysis of the data, highlighted an increased activation in several cortical areas, as well as different activation patterns in the two tested experimental conditions: open and closed eyes. An improved experimental protocol has then been developed, allowing a more advanced data analysis based on source reconstruction and brain network analysis techniques. Using this new approach, it was possible to characterise with greater detail the topological structure of cortical functional connections during the postural task, as well as to draw a connection between quantitative network metrics and measures of postural performance. Finally, with the integration of electromyography in the experimental protocol, we were able to gain new insights into the cortico-muscular interactions which direct the muscular response to a postural challenge. Overall, the findings presented in this thesis provide further evidence of the prominent role played by the cortex in postural control. They also prove how novel EEG-based brain network analysis techniques can be a valid tool in postural research and offer promising perspectives for the integration of quantitative cortical network metrics into clinical evaluation of postural impairment.Kerfi stöðustjórnunar er afturvirkt stýrikerfi sem vinnur stöðugt að því að viðhalda uppréttri stöðu líkamans og bregðast við ójafnvægi. Vaxandi þekking á undanförnum árum hefur lýst því að úrvinnsla þessara upplýsinga á sér stað á öllum stigum miðtaugakerfisins, þá sérstaklega barkarsvæði heilahvela. Engu að síður, er nákvæmu hlutverk heilabarkar við stöðustjórnun enn óljóst að mörgu leyti. Tilgangur þessa verkefnis var að rannsaka nánar hlutverk heilabarkar við truflun og áreiti á kerfi stöðustjórnarinnar, með notkun hágæða heilarafrits (EEG). Við byrjuðum á því að mæla heilarit einstaklinga meðan á þekktri líkamsstöðu-æfingu stóð, til þess að skoða svörun líkamans við röð titringsáreita sem beitt var á kálfavöðvana til að framkalla óstöðugleika. Bráðabirgðaniðurstöður fengnar með PSD-aðferð (power spectral analysis) leiddu í ljós aukna virkni á ákveðnum svæðum í heilaberki og sérstakt viðbragðsmynstur við að framkvæma æfinguna, annars vegar með lokuð augu og hins vegar opin augu. Rannsókn okkar hélt áfram með nýrri og þróaðari tækni sem gerði okkur kleift að framkvæma fullkomnari greiningaraðferðir til að túlka, greina og skilja merki frá heilaritnu. Með fullkomnari greiningaraðferðum var hægt að lýsa með nákvæmari hætti staðfræðilega uppbyggingu starfrænna tenginga í heilaberki meðan á líkamsstöðu æfingunni stóð, sem og að draga tengsl á milli megindlegra netmælinga og mælinga á líkamsstöðu. Að lokum bætist við vöðvarafritsmæling við aðferðafræðina, sem gaf okkur innsýn inn í samskipti heilabarka og vöðvana sem stýra vöðvaviðbrögðum og viðhalda líkamsstöðu við utanaðkomandi áreiti. Á heildina litið gefa niðurstöðurnar sem settar eru fram í þessari ritgerð enn sterkari vísbendingar um það áberandi hlutverk sem heilabörkurinn gegnir við stjórnun líkamsstöðu. Niðurstöðurnar sanna einnig hvernig ný aðferð á greiningu á tengslaneti heilans sem byggir á heilariti getur verið gilt tæki í líkamsstöðu rannsóknum og er nytsamlegt tól fyrir mælingar á heilakerfisneti í klínískt mat á skerðingu líkamsstöðu

EEG-based investigation of cortical activity during Postural Control

The postural control system regulates the ability to maintain a stable upright stance and to react to changes in the external environment. Although once believed to be dominated by low-level reflexive mechanisms, mounting evidence has highlighted a prominent role of the cortex in this process. Nevertheless, the high-level cortical mechanisms involved in postural control are still largely unexplored. The aim of this thesis is to use electroencephalography, a widely used and non-invasive neuroimaging tool, to shed light on the cortical mechanisms which regulate postural control and allow balance to be preserved in the wake of external disruptions to one’s quiet stance. EEG activity has been initially analysed during a well-established postural task - a sequence of proprioceptive stimulations applied to the calf muscles to induce postural instability – traditionally used to examine the posturographic response. Preliminary results, obtained through a spectral power analysis of the data, highlighted an increased activation in several cortical areas, as well as different activation patterns in the two tested experimental conditions: open and closed eyes. An improved experimental protocol has then been developed, allowing a more advanced data analysis based on source reconstruction and brain network analysis techniques. Using this new approach, it was possible to characterise with greater detail the topological structure of cortical functional connections during the postural task, as well as to draw a connection between quantitative network metrics and measures of postural performance. Finally, with the integration of electromyography in the experimental protocol, we were able to gain new insights into the cortico-muscular interactions which direct the muscular response to a postural challenge. Overall, the findings presented in this thesis provide further evidence of the prominent role played by the cortex in postural control. They also prove how novel EEG-based brain network analysis techniques can be a valid tool in postural research and offer promising perspectives for the integration of quantitative cortical network metrics into clinical evaluation of postural impairment

Cortico-muscular coherence in sensorimotor synchronisation

This thesis sets out to investigate the neuro-muscular control mechanisms underlying the ubiquitous phenomenon of sensorimotor synchronisation (SMS). SMS is the coordination of movement to external rhythms, and is commonly observed in everyday life. A large body of research addresses the processes underlying SMS at the levels of behaviour and brain. Comparatively, little is known about the coupling between neural and behavioural processes, i.e. neuro-muscular processes. Here, the neuro-muscular processes underlying SMS were investigated in the form of cortico-muscular coherence measured based on Electroencephalography (EEG) and Electromyography (EMG) recorded in human healthy participants. These neuro-muscular processes were investigated at three levels of engagement: passive listening and observation of rhythms in the environment, imagined SMS, and executed SMS, which resulted in the testing of three hypotheses: (i) Rhythms in the environment, such as music, spontaneously modulate cortico-muscular coupling, (ii) Movement intention modulates cortico-muscular coupling, and (iii) Cortico-muscular coupling is dynamically modulated during SMS time-locked to the stimulus rhythm. These three hypotheses were tested through two studies that used Electroencephalography (EEG) and Electromyography (EMG) recordings to measure Cortico-muscular coherence (CMC). First, CMC was tested during passive music listening, to test whether temporal and spectral properties of music stimuli known to induce groove, i.e., the subjective experience of wanting to move, can spontaneously modulate the overall strength of the communication between the brain and the muscles. Second, imagined and executed movement synchronisation was used to investigate the role of movement intention and dynamics on CMC. The two studies indicate that both top-down, and somatosensory and/or proprioceptive processes modulate CMC during SMS tasks. Although CMC dynamics might be linked to movement dynamics, no direct correlation between movement performance and CMC was found. Furthermore, purely passive auditory or visual rhythmic stimulation did not affect CMC. Together, these findings thus indicate that movement intention and active engagement with rhythms in the environment might be critical in modulating CMC. Further investigations of the mechanisms and function of CMC are necessary, as they could have important implications for clinical and elderly populations, as well as athletes, where optimisation of motor control is necessary to compensate for impaired movement or to achieve elite performance

Measuring Directed Functional Connectivity Using Non-Parametric Directionality Analysis : Validation and Comparison with Non-Parametric Granger Causality

BACKGROUND: 'Non-parametric directionality' (NPD) is a novel method for estimation of directed functional connectivity (dFC) in neural data. The method has previously been verified in its ability to recover causal interactions in simulated spiking networks in Halliday et al. (2015). METHODS: This work presents a validation of NPD in continuous neural recordings (e.g. local field potentials). Specifically, we use autoregressive models to simulate time delayed correlations between neural signals. We then test for the accurate recovery of networks in the face of several confounds typically encountered in empirical data. We examine the effects of NPD under varying: a) signal-to-noise ratios, b) asymmetries in signal strength, c) instantaneous mixing, d) common drive, e) data length, and f) parallel/convergent signal routing. We also apply NPD to data from a patient who underwent simultaneous magnetoencephalography and deep brain recording. RESULTS: We demonstrate that NPD can accurately recover directed functional connectivity from simulations with known patterns of connectivity. The performance of the NPD measure is compared with non-parametric estimators of Granger causality (NPG), a well-established methodology for model-free estimation of dFC. A series of simulations investigating synthetically imposed confounds demonstrate that NPD provides estimates of connectivity that are equivalent to NPG, albeit with an increased sensitivity to data length. However, we provide evidence that: i) NPD is less sensitive than NPG to degradation by noise; ii) NPD is more robust to the generation of false positive identification of connectivity resulting from SNR asymmetries; iii) NPD is more robust to corruption via moderate amounts of instantaneous signal mixing. CONCLUSIONS: The results in this paper highlight that to be practically applied to neural data, connectivity metrics should not only be accurate in their recovery of causal networks but also resistant to the confounding effects often encountered in experimental recordings of multimodal data. Taken together, these findings position NPD at the state-of-the-art with respect to the estimation of directed functional connectivity in neuroimaging

Proceedings of the 3rd International Mobile Brain/Body Imaging Conference : Berlin, July 12th to July 14th 2018

The 3rd International Mobile Brain/Body Imaging (MoBI) conference in Berlin 2018 brought together researchers from various disciplines interested in understanding the human brain in its natural environment and during active behavior. MoBI is a new imaging modality, employing mobile brain imaging methods like the electroencephalogram (EEG) or near infrared spectroscopy (NIRS) synchronized to motion capture and other data streams to investigate brain activity while participants actively move in and interact with their environment. Mobile Brain / Body Imaging allows to investigate brain dynamics accompanying more natural cognitive and affective processes as it allows the human to interact with the environment without restriction regarding physical movement. Overcoming the movement restrictions of established imaging modalities like functional magnetic resonance tomography (MRI), MoBI can provide new insights into the human brain function in mobile participants. This imaging approach will lead to new insights into the brain functions underlying active behavior and the impact of behavior on brain dynamics and vice versa, it can be used for the development of more robust human-machine interfaces as well as state assessment in mobile humans.DFG, GR2627/10-1, 3rd International MoBI Conference 201