Publications

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Bipedal locomotion was a major functional change during hominin evolution, yet, our understanding of this gradual and complex process remains strongly debated. Based on fossil discoveries, it is possible to address functional hypotheses related to bipedal anatomy, however, motor control remains intangible with this approach. Using comparative models which occasionally walk bipedally has proved to be relevant to shed light on the evolutionary transition toward habitual bipedalism. Here, we explored the organization of the neuromuscular control using surface electromyography (sEMG) for six extrinsic muscles in two baboon individuals when they walk quadrupedally and bipedally on the ground. We compared their muscular coordination to five human subjects walking bipedally. We extracted muscle synergies from the sEMG envelopes using the nonnegative matrix factorization algorithm which allows decomposing the sEMG data in the linear combination of two non-negative matrixes (muscle weight vectors and activation coefficients). We calculated different parameters to estimate the complexity of the sEMG signals, the duration of the activation of the synergies, and the generalizability of the muscle synergy model across species and walking conditions. We found that the motor control strategy is less complex in baboons when they walk bipedally, with an increased muscular activity and muscle coactivation. When comparing the baboon bipedal and quadrupedal pattern of walking to human bipedalism, we observed that the baboon bipedal pattern of walking is closer to human bipedalism for both baboons, although substantial differences remain. Overall, our findings show that the muscle activity of a nonadapted biped effectively fulfills the basic mechanical requirements (propulsion and balance) for walking bipedally, but substantial refinements are possible to optimize the efficiency of bipedal locomotion. In the evolutionary context of an expanding reliance on bipedal behaviors, even minor morphological alterations, reducing muscle coactivation, could have faced strong selection pressure, ultimately driving bipedal evolution in hominins.

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The aim of this study was to investigate balance performance and muscle synergies during a Single-Limb Stance (SLS) task in individuals with Chronic Ankle Instability (CAI) and a group of healthy controls. Twenty individuals with CAI and twenty healthy controls were asked to perform a 30-second SLS task in Open-Eyes (OE) and Closed-Eyes (CE) conditions while standing on a force platform with the injured or the dominant limb, respectively. The activation of 13 muscles of the lower limb, hip, and back was recorded by means of surface electromyography. Balance performance was assessed by identifying the number and the duration of SLS epochs, and the Root-Mean-Square (RMS) in Antero-Posterior (AP) and Medio-Lateral (ML) directions of the body-weight normalized ground reaction forces. The optimal number of synergies, weight vectors, and activation coefficients were also analyzed. CAI group showed a higher number and a shorter duration of SLS epochs and augmented ground reaction force RMS in both AP and ML directions compared to controls. Both groups showed an increase in the RMS in AP and ML forces in CE compared to OE. Both groups showed 4 optimal synergies in CE, while controls showed 5 synergies in OE. CAI showed a significantly higher weight of knee flexor muscles in both OE and CE. In conclusion, muscle synergies analysis provided an in–depth knowledge of motor control mechanisms in CAI individuals. They showed worse balance performance, a lower number of muscle synergies in a CE condition and abnormal knee flexor muscle activation compared to healthy controls.

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The aim of this study is to quantitatively assess motor control changes in Parkinson’s disease (PD) patients after bilateral deep brain stimulation of the subthalamic nucleus (STN-DBS), based on a novel muscle synergy evaluation approach. A group of 20 PD patients evaluated at baseline (before surgery, T₀), at 3 months (T₁), and at 12 months (T₂) after STN-DBS surgery, as well as a group of 20 age-matched healthy control subjects, underwent an instrumented gait analysis, including surface electromyography recordings from 12 muscles. A smaller number of muscle synergies was found in PD patients (4 muscle synergies, at each time point) compared to control subjects (5 muscle synergies). The neuromuscular robustness of PD patients—that at T₀ was smaller with respect to controls (PD T₀: 69.3 ± 2.2% vs. Controls: 77.6 ± 1.8%, p = 0.004)—increased at T₁ (75.8 ± 1.8%), becoming not different from that of controls at T₂ (77.5 ± 1.9%). The muscle synergies analysis may offer clinicians new knowledge on the neuromuscular structure underlying PD motor types of behavior and how they can improve after electroceutical STN-DBS therapy.

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Wearable sensors are de facto revolutionizing the assessment of standing balance. The aim of this work is to review the state-of-the-art literature that adopts this new posturographic paradigm, i.e., to analyse human postural sway through inertial sensors directly worn on the subject body. After a systematic search on PubMed and Scopus databases, two raters evaluated the quality of 73 full-text articles, selecting 47 high-quality contributions. A good inter-rater reliability was obtained (Cohen’s kappa = 0.79). This selection of papers was used to summarize the available knowledge on the types of sensors used and their positioning, the data acquisition protocols and the main applications in this field (e.g., “active aging”, biofeedback-based rehabilitation for fall prevention, and the management of Parkinson’s disease and other balance-related pathologies), as well as the most adopted outcome measures. A critical discussion on the validation of wearable systems against gold standards is also presented.

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In motor control studies, the 90% thresholding of variance accounted for (VAF) is the classical way of selecting the number of muscle synergies expressed during a motor task. However, the adoption of an arbitrary cut-off has evident drawbacks. The aim of this work is to describe and validate an algorithm for choosing the optimal number of muscle synergies (ChoOSyn), which can overcome the limitations of VAF-based methods. The proposed algorithm is built considering the following principles: (1) muscle synergies should be highly consistent during the various motor task epochs (i.e., remaining stable in time), (2) muscle synergies should constitute a base with low intra-level similarity (i.e., to obtain information-rich synergies, avoiding redundancy). The algorithm performances were evaluated against traditional approaches (threshold-VAF at 90% and 95%, elbow-VAF and plateau-VAF), using both a simulated dataset and a real dataset of 20 subjects. The performance evaluation was carried out by analyzing muscle synergies extracted from surface electromyographic (sEMG) signals collected during walking tasks lasting 5 min. On the simulated dataset, ChoOSyn showed comparable performances compared to VAF-based methods, while, in the real dataset, it clearly outperformed the other methods, in terms of the fraction of correct classifications, mean error (ME), and root mean square error (RMSE). The proposed approach may be beneficial to standardize the selection of the number of muscle synergies between different research laboratories, independent of arbitrary thresholds

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It is important to find objective biomarkers for evaluating gait in Parkinson’s Disease (PD), especially related to the foot and lower leg segments. Foot-switch signals, analyzed through Statistical Gait Analysis (SGA), allow the foot-floor contact sequence to be characterized during a walking session lasting five-minutes, which includes turnings. Gait parameters were compared between 20 PD patients and 20 age-matched controls. PDs showed similar straight-line speed, cadence, and double-support compared to controls, as well as typical gait-phase durations, except for a small decrease in the flat-foot contact duration (−4% of the gait cycle, p = 0.04). However, they showed a significant increase in atypical gait cycles (+42%, p = 0.006), during both walking straight and turning. A forefoot strike, instead of a “normal” heel strike, characterized the large majority of PD’s atypical cycles, whose total percentage was 25.4% on the most-affected and 15.5% on the least-affected side. Moreover, we found a strong correlation between the atypical cycles and the motor clinical score UPDRS-III (r = 0.91, p = 0.002), in the subset of PD patients showing an abnormal number of atypical cycles, while we found a moderate correlation (r = 0.60, p = 0.005), considering the whole PD population. Atypical cycles have proved to be a valid biomarker to quantify subtle gait dysfunctions in PD patients

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Gait analysis applications in clinics are still uncommon, for three main reasons: (1) the considerable time needed to prepare the subject for the examination; (2) the lack of user-independent tools; (3) the large variability of muscle activation patterns observed in healthy and pathological subjects. Numerical indices quantifying the muscle coordination of a subject could enable clinicians to identify patterns that deviate from those of a reference population and to follow the progress of the subject after surgery or completing a rehabilitation program. In this work, we present two user-independent indices. First, a muscle-specific index (MFI) that quantifies the similarity of the activation pattern of a muscle of a specific subject with that of a reference population. Second, a global index (GFI) that provides a score of the overall activation of a muscle set. These two indices were tested on two groups of healthy and pathological children with encouraging results. Hence, the two indices will allow clinicians to assess the muscle activation, identifying muscles showing an abnormal activation pattern, and associate a functional score to every single muscle as well as to the entire muscle set. These opportunities could contribute to facilitating the diffusion of surface EMG analysis in clinics

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Background

The accurate temporal analysis of muscle activation is of great interest in many research areas, spanning from neurorobotic systems to the assessment of altered locomotion patterns in orthopedic and neurological patients and the monitoring of their motor rehabilitation. The performance of the existing muscle activity detectors is strongly affected by both the SNR of the surface electromyography (sEMG) signals and the set of features used to detect the activation intervals. This work aims at introducing and validating a powerful approach to detect muscle activation intervals from sEMG signals, based on long short-term memory (LSTM) recurrent neural networks.

Methods

First, the applicability of the proposed LSTM-based muscle activity detector (LSTM-MAD) is studied through simulated sEMG signals, comparing the LSTM-MAD performance against other two widely used approaches, i.e., the standard approach based on Teager–Kaiser Energy Operator (TKEO) and the traditional approach, used in clinical gait analysis, based on a double-threshold statistical detector (Stat). Second, the effect of the Signal-to-Noise Ratio (SNR) on the performance of the LSTM-MAD is assessed considering simulated signals with nine different SNR values. Finally, the newly introduced approach is validated on real sEMG signals, acquired during both physiological and pathological gait. Electromyography recordings from a total of 20 subjects (8 healthy individuals, 6 orthopedic patients, and 6 neurological patients) were included in the analysis.

Results

The proposed algorithm overcomes the main limitations of the other tested approaches and it works directly on sEMG signals, without the need for background-noise and SNR estimation (as in Stat). Results demonstrate that LSTM-MAD outperforms the other approaches, revealing higher values of F1-score (F1-score > 0.91) and Jaccard similarity index (Jaccard > 0.85), and lower values of onset/offset bias (average absolute bias < 6 ms), both on simulated and real sEMG signals. Moreover, the advantages of using the LSTM-MAD algorithm are particularly evident for signals featuring a low to medium SNR.

Conclusions

The presented approach LSTM-MAD revealed excellent performances against TKEO and Stat. The validation carried out both on simulated and real signals, considering normal as well as pathological motor function during locomotion, demonstrated that it can be considered a powerful tool in the accurate and effective recognition/distinction of muscle activity from background noise in sEMG signals.

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Purpose

Single-limb stance is a demanding postural task featuring a high number of daily living and sporting activities. Thus, it is widely used for training and rehabilitation, as well as for balance assessment. Muscle activations around single joints have been previously described, however, it is not known which are the muscle synergies used to control posture and how they change between conditions of normal and lack of visual information.

Methods

Twenty-two healthy young participants were asked to perform a 30 s single-limb stance task in open-eyes and closed-eyes condition while standing on a force platform with the dominant limb. Muscle synergies were extracted from the electromyographical recordings of 13 muscles of the lower limb, hip, and back. The optimal number of synergies, together with the average recruitment level and balance control strategies were analyzed and compared between the open- and the closed-eyes condition.

Results

Four major muscle synergies, two ankle-dominant synergies, one knee-dominant synergy, and one hip/back-dominant synergy were found. No differences between open- and closed-eyes conditions were found for the recruitment level, except for the hip/back synergy, which significantly decreased (p = 0.02) in the closed-eyes compared to the open-eyes condition. A significant increase (p = 0.03) of the ankle balance strategy was found in the closed-eyes compared to the open-eyes condition.

Conclusion

In healthy young individuals, single-limb stance is featured by four major synergies, both in open- and closed-eyes condition. Future studies should investigate muscle synergies in participants with other age groups, as well as pathological conditions.

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To help neurologists, physicians, and physical therapists in the management of patients with altered locomotion patterns, it is of the uttermost importance relying on accurate measurements of gait. Gait analysis becomes even more informative if the electrical activity of muscles is recorded, non-invasively, during the dynamic task of walking, through surface electromyography (sEMG) probes. However, sEMG signals must be processed through advanced techniques to obtain reliable results, easily interpretable by healthcare practitioners. Indeed, the study of how muscles are activated during natural walking (in unconstrained environments) is complex for several reasons, including a high stride-to-stride variability, even more pronounced in pathological subjects. On the other hand, it is crucial to provide clinicians with aggregated information relying on validated parameters and easily usable representations that can be effectively included in clinical reports. This chapter is aimed at introducing: (1) Statistical Gait Analysis (SGA) to automatically analyze hundreds of gait cycles collected during a physiological or pathological walk lasting several minutes, (2) the extraction of principal and secondary muscle activations to obtain consistent clinical indexes, (3) the extraction of “muscle synergies” to quantitatively study motor control strategies. Each of these techniques are based on state-of-the-art processing algorithms of the sEMG signal. A brief review of the recent literature published in this field will be presented and discussed.

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The muscle synergy theory has been widely used to assess the modular organization of the central nervous system (CNS) during human locomotion. The pre-processing approach applied to the surface electromyographic (sEMG) signals influences the extraction of muscle synergies. The aim of this contribution is to assess the improvements in muscle synergy extraction obtained by using an innovative pre-processing approach. We evaluate the improvement in terms of the possible variation in the number of muscle synergies, of the intra-subject consistency, of the robustness, and of the interpretability of the results. The pre-processing approach presented in this paper is based on the extraction of the muscle principal activations (muscle activations strictly necessary to accomplish a specific biomechanical task) from the original sEMG signals, to then obtain muscle synergies using principal activations only. The results herein presented show that the application of this novel approach for the extraction of the muscle synergies provides a more robust and easily interpretable description of the modular organization of the CNS with respect to the standard pre-processing approach.

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In the study of muscle synergies during the maintenance of single-leg stance there are several methodological issues that must be taken into account before muscle synergy extraction. In particular, it is important to distinguish between epochs of surface electromyography (sEMG) signals corresponding to “well-balanced” and “unbalanced” single-leg stance, since different motor control strategies could be used to maintain balance. The aim of this work is to present and define a robust procedure to distinguish between “well-balanced” and “unbalanced” single-leg stance to be chosen as input for the algorithm used to extract muscle synergies. Our results demonstrate that the proposed approach for the selection of sEMG epochs relative to “well-balanced” and “unbalanced” single-leg stance is robust with respect to the selection of the segmentation threshold, revealing a high consistency in the number of muscle synergies and high similarity among the weight vectors (correlation values range from 0.75 to 0.97). Moreover, differences in terms of average recruitment levels and balance control strategies were detected, suggesting a slightly different modular organization between “well-balanced” and “unbalanced” single-leg stance. In conclusion, this approach can be successfully used as a pre-processing step before muscle synergy extraction, allowing for a better assessment of motor control strategies during the single-leg stance task.

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The muscle synergy theory was widely used in literature to assess the modular organization of the central nervous system (CNS) during human locomotion. The extraction of muscle synergies may be strongly influenced by the preprocessing techniques applied to surface electromyographic (sEMG) signals. The aim of this contribution is to assess the robustness improvement in muscle synergy extraction obtained using an innovative pre-processing technique with respect to the standard procedure. The new pre-processing technique that we propose is based on the extraction of principal muscle activation intervals (necessary to accomplish a specific biomechanical task during gait) from the original sEMG signals, discarding the secondary muscle activation intervals (activations that occur only in some strides with auxiliary functions). Results suggest that the extraction of the principal activation intervals from sEMG provide a more consistent and stable description of the modular organization of the CNS with respect to the standard pre-processing procedure.

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The modular organization of the central nervous system (CNS) during motor tasks was widely assessed by means of muscle synergies. The aim of this work was to assess the impact of the Signal-to-Noise Ratio (SNR) on muscle synergies extracted from synthetic surface electromyographic (sEMG) signals that simulate the muscle activity of the lower limb during walking. To evaluate the effect of the SNR, the similarity between the weights vectors and the activation coefficients extracted from real sEMG signals and from simulated sEMG signals at different values of SNR was computed. Results reveal that muscle synergy extraction is strongly dependent upon the quality of the sEMG signals simulated.

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The role of central and peripheral vision in the maintenance of upright stance is debated in literature. Stargardt disease causes visual deficits affecting the central field, but leaving unaltered a patient’s peripheral vision. Hence, the study of this rare pathology gives the opportunity to selectively investigate the role of central vision in posture. Postural sway in quiet stance was analyzed in 10 Stargardt patients and 10 control subjects, in three different conditions: (1) eyes closed, (2) eyes open, gazing at a fixed target, and (3) eyes open, tracking a moving target. Stargardt patients outperformed controls in the condition with eyes closed, showing a reduced root mean square (RMS) of the medio-lateral COP displacement, while their performance was not significantly different from controls in the antero-posterior direction. There were no significant differences between patients and controls in open eyes conditions. These results suggest that Stargardt patients adapted to a different visual-somatosensory integration, relying less on vision, especially in the medio-lateral direction. Hence, the central vision seems to affect mostly the medio-lateral direction of postural sway. This finding supports the plausibility of the “functional sensitivity hypothesis”, that assigns complementary roles to central and peripheral vision in the control of posture.

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Background: Texting on a smartphone while walking has become a customary task among young adults. In recent literature many safety concerns on distracted walking have been raised. It is often hypothesized that the allocation of attentional resources toward a secondary task can influence dynamic stability. In the double task of walking and texting it was found that gait speed is reduced, but there is scarce evidence of a modified motor control strategy compromising stability. The aim of this study is twofold: 1) to comprehensively examine the gait modifications occurring when texting while walking, including the study of the lower limb muscle activation patterns, 2) to specifically assess the co-contraction of ankle antagonist muscles. We hypothesized that texting while walking increases co-contractions of ankle antagonist muscles when the body weight is transferred from one lower limb to the other, to improve the distal motor control and joint stabilization.

Methods: From the gait data collected during an instrumented walk lasting 3 min, we calculated the spatio-temporal parameters, the ankle and knee kinematics, the muscle activation patterns of tibialis anterior, gastrocnemius lateralis, peroneus longus, rectus femoris, and lateral hamstrings, and the co-contraction (occurrence and duration) of the ankle antagonist muscles (tibialis anterior and gastrocnemius lateralis), bilaterally.

Results: Young adults showed, overall, small gait modifications that could be mainly ascribable to gait speed reduction and a modified body posture due to phone handling. We found no significant alterations of ankle and knee kinematics and a slightly delayed activation onset of the left gastrocnemius lateralis. However, we found an increased co-contraction of tibialis anterior and gastrocnemius lateralis, especially during mid-stance. Conversely, we found a reduced co-contraction during terminal stance.

Conclusions: Our results suggest that, in young adults, there is an adjustment of the motor control strategy aimed at increasing ankle joint stability in a specific and “critical” phase of the gait cycle, when the body weight is transferred from one leg to the other.

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The aim of this work was to analyze the postural sway of volleyball players in bipedal quiet stance. The center of pressure (CoP) was measured in 46 athletes and 42 non-athlete controls. Each subject was tested in 10 different conditions, 5 with their eyes open and 5 with their eyes closed. Volleyball players showed greater CoP ellipses, suggesting a different model of sensory integration in their postural stability. A multivariate approach to data analysis demonstrated that the postural sway of the two groups was different when the subjects kept their eyes open, but it was not with visual deprivation. This could partially be explained by the better ‘dynamic’ visual acuity of athletes, since possible (‘static’) refractive errors were corrected for both groups. Furthermore, we expected that national players, engaged in more intensive training programs, were more different from controls than regional ones, and that defensive players, whose role requires the quickest reaction times, were more different from controls than hitters. Our results confirmed these hypothesis. The protocol presented might be useful to assess the efficacy of intensive sport training programs and/or to select elite players with an aptitude for a specific playing position.

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Postural instability is a common and devastating consequence of traumatic brain injury (TBI). The majority of TBI patients also suffer from neuro-ophthalmic deficits that can be an important contributing element to their sensation of vertigo and dizziness. Static posturography aims at the objective evaluation of patient balance impairment, but is usually affected by large inter- and intra-subject variability. Here we propose a protocol based on 10 randomized trials stimulating in different ways the visual and vestibular systems. Due to its completeness, our protocol highlights the specific residual difficulties of each patient in the various conditions. In this way, it was possible to evidence significant balance abnormalities in TBI patients with respect to controls. Moreover, by means of a multivariate analysis we were able to discriminate different levels of residual neuro-ophthalmic impairment.

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