Evaluating Muscle Synergies with EMG Data

and Physics Simulation in the Neurorobotics

Platform
Benedikt Feldotto 1,∗ , Cristian Soare 1 , Alois Knoll 1 , Piyanee Sriya 2 , Sarah
Astill 2 , Marc de Kamps 3,4,5 and Samit Chakrabarty 2
1 Robotics,Artificial Intelligence and Real-Time Systems, Technical University of
Munich, Munich, Germany 2 School of Biomedical Sciences, Faculty of Biological
Sciences, University of Leeds, Leeds, United Kingdom 3 School of Computing,
University of Leeds, Leeds, United Kingdom 4 Leeds Institute for Data Analytics,
Leeds, United Kingdom 5 The Alan Turing Institute, London, United Kingdom
Correspondence*:
arXiv:2201.05496v1 [q-bio.NC] 14 Jan 2022

Benedikt Feldotto
[email protected]

ABSTRACT
Although we can measure muscle activity and analyze their activation patterns, we understand
little about how individual muscles affect the joint torque generated. It is known that they are
controlled by circuits in the spinal cord, a system much less well understood than the cortex.
Knowing the contribution of the muscles towards a joint torque would improve our understanding
of human limb control. We present a novel framework to examine the control of biomechanics
using physics simulations informed by electromyography (EMG) data. These signals drive a
virtual musculoskeletal model in the Neurorobotics Platform (NRP), which we then use to evaluate
resulting joint torques. We use our framework to analyze raw EMG data collected during an
isometric knee extension study to identify synergies that drive a musculoskeletal lower limb model.
The resulting knee torques are used as a reference for genetic algorithms (GA) to generate
new simulated activation patterns. On the platform the GA finds solutions that generate torques
matching those observed. Possible solutions include synergies that are similar to those extracted
from the human study. In addition, the GA finds activation patterns that are different from the
the biological ones while still producing the same knee torque. The NRP forms a highly modular
integrated simulation platform allowing these in silico experiments. We argue that our framework
allows for research of the neurobiomechanical control of muscles during tasks, which would
otherwise not be possible.

1 INTRODUCTION
We take our freedom to move around at will for granted. Only when this freedom is impaired do we start to
realize how much so, and only when we try to alleviate the impairment with the aid of technology do we
start to fully appreciate how complex the pathway from intended motion to execution actually is.
Much of our normal walking is unconscious, driven by rhythmic neural activation generated in the spinal
cord by the central pattern generators. It has long been obvious that the spinal cord has considerable
autonomy in calculating appropriate responses to proprioceptive input and that cortical intervention would
be too slow. Examples are the changing load of a coffee cup being filled, the precise drawing of a figure
automatically adapting to the coarseness and resistance of the canvas, or the fastening of a tiny screw in a

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delicate machine. In these cases, cortex generated intent passes down by the descending pathways but the
generation of precise motor output depends substantially on processing in the spinal cord, integrating and
balancing cortical input and proprioceptive feedback.

How this integration is done is still unclear. The neural circuitry of the spinal cord has not been mapped
functionally at the same level of detail as that of the cortex. This is because much of the knowledge gained
through invasive techniques, e.g. multi-electrode arrays, cannot be performed in humans, except in unusual
circumstances. The generalization of ideas that were developed in models of four-legged creatures to
human performance is clearly problematic.

A non-invasive technique is electromyography (EMG), where relatively small wearable sensors are used
to record muscle activity. As we will see, together with neural modelling, such measurements can provide
insight in local processing in the spinal cord. We have experimental evidence that demonstrates so-called
synergies, the co-activation of several muscle groups to produce a desired motor output. Recently, we have
demonstrated that proprioceptive feedback plays a role in the generation of such synergies ((York et al.,
2021)), contrary to what has been reported in the literature. Using non-negative matrix factorization in the
data analysis, we can identify these synergies. The model produces the same synergy trends as observed in
the data, driven by changes in the afferent input. Neural modelling helps interpret these data. To match the
activation patterns from each knee angle and position of the study, the model predicts the need for three
distinct inputs: two to control a non-linear bias towards the extensors against the flexors, and a further
input to control additional inhibition of the rectus femoris. Simulations suggests that proprioception may
be involved in modulating muscle synergies encoded in cortical or spinal neural circuits.

What this work does not show and cannot show is how these synergies are involved in the generation of
force vectors. Our data shows, strikingly, that individuals can use different synergies to produce the same
force vectors. This is a very important observation as understanding this probably helps in understanding
the considerable amount of redundancy that is available in the musculo-skeletal system: there is more than
one way to produce a given motor output.

Importantly, even in animal studies there is no access to muscle forces. To understand how force is
generated once the activation pattern has been established, simulation is the only available option. The
Neurorobotics Platform (NRP) ((Knoll and Gewaltig, 2016)) ((Albanese et al., 2018)) ((Hinkel et al., 2017))
developed within the Human Brain Project ((Amunts et al., 2016)) ((Markram et al., 2011)) is a natural
simulation environment for gaining an understanding of force vector output by neural signals, as we can
model the entire system: neural activation, resulting muscle tensions and resulting force output, in this
experiment the resultant force on a knee torque.

In this paper, we extend the feature rich framework of the NRP for EMG data evaluation and demonstrate
that it is ideally suited to investigate force generation in a musculo-skeletal model. Moreover, since it is an
entirely simulated environment, this allows in silico experimentation. We applied machine learning and
signal processing to reanalyze the data trials, determine features and recover the synergies in the signal. We
feed the muscle activation into the physics simulation and quantify resulting knee torques. Finally, we use
a Genetic Algorithm (GA) to generate alternative control signals that produce the same torque output as
in the study. We find that there are various synergies possible. Some of the synergies found in simulation
match those identified in the experimental data. This suggests that a simulated environment can be used to
infer potential implementations for control strategies.

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2 NEUROROBOTICS PLATFORM
The Neurorobotics Platform (NRP) is developed within the European Human Brain Project and is integrated
into the EBRAINS research infrastructure for brain simulation on supercomputing infrastructure. The NRP
uses the robot simulator Gazebo ((Koenig and Howard, 2004)) for rigid body computations and has been
extended with the muscle simulation framework from OpenSim ((Seth et al., 2018)) ((Delp et al., 2007)) to
simulate musculoskeletal models interacting with virtual environments. This unique integration enables
simulation of classical motor-driven robots and biologically derived musculoskeletal mammalian bodies in
the same experiment, in our case a musculoskeletal lower limb model in a virtual test environment. As part
of the NRP the Closed Loop Engine is implemented to synchronize spiking neural network simulations
in NEST ((Gewaltig and Diesmann, 2007)) with the physics simulation in predefined simulation steps.
Transfer Functions specify the bidirectional exchange of sensory data and motor control commands. To
optimize the workflow for experiment design the NRP provides user tools for fully customized setups
such as a Robot Designer, Environment Designer, a Virtual Coach for scripted experiments and State
Machine for automated control. Communication is based on the widely used Robot Operating System
(ROS) ((Quigley et al., 2009)) that enables modular interchange of information within the NRP, as well as
with external processing nodes in soft- and hardware. In this work we add an additional processing node
within this modular framework for EMG data processing and control with a Genetic Algorithm. The NRP
is deployed on the EBRAINS computing cluster infrastructure and hereby accessible via web browser. We
here employ a local installation of the NRP on a local computer as it is offered open source to a wide user
community. Use cases include the evaluation of neural networks based on neurophysiological experiments
in embodied closed-loop simulations with musculoskeletal and robotic models.
The NRP has been used for reconstruction of physical experiments before, in particular a stroke
rehabilitation study with mice has been implemented in ((Mascaro et al., 2020)). Here, we focus on
the human musculoskeletal system and EMG data of muscle activation that help us better understand
biological muscular motion control patterns.

3 EXPERIMENTAL SETUP
In this section we describe the experimental study that has been realized in this work. We first introduce
the participant study of human knee extension and then we describe the simulation architecture that has
been implemented to reproduce and evaluate the study data virtually.

3.1 Human knee extension study

We conducted a modified knee extension study with human participants as lower limb muscles are
expected to provide the strongest muscle activation feedback in the human body ((York et al., 2021)). Here,
we focus on the knee angle alone as the one degree of freedom (DOF) at the rotary joint as all others will
be avoided by providing support. One degree of freedom also provided better measurable one dimensional
feedback, reducing the effect of extraneous variables.
A cross-sectional, single-blinded control study was designed to compare the muscle activity at four
distinct knee angles during isometric contractions. Healthy participants (n = 17, female = 8) within the
ages of 18-30 (24.4± 2.57 years) without previous knee joint injury participated in the study. Participants
were randomly allocated to different groups, and all measurements were conducted in the motor control
laboratories of the center for sports sciences, in the School of Biomedical Sciences, University of Leeds,
UK..

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Figure 1. Human knee extension experiment: Participant Study with EMG recordings (Left) and
experiment replication in the Neurorobotics Platform (Right).

A physio-clear plastic Goniometer angle ruler was used to measure the knee extension angles. Participants
lay supine on the bed with the head, back and leg muscles being fully supported. The setup is adapted from
the Fugel-Meyer’s knee control test used in stroke rehabilitation ((Fugl-Meyer et al., 1975)). The knee was
held in position using a locking knee brace (DonjoyTM).

3.1.1 Study Procedure

Subjects were asked to perform an isometric knee extension experiment with maximal voluntary effort.
Initially, participants lay suspine on the bed with both legs stretched out in front, the hip, knee and ankle
are located at a 0° to each other. For every recording the participant contracted their muscles at the back
of the thigh of the right leg, while the knee is placed at a given steady angle. Participants were asked to
activate the Rectus Femoris (RF) voluntarily, to ensure RF was the most active muscle, in line with current
literature. We examined four different knee angles: at 0° (foot extended, so straight at the knee), 20° (knee
is slightly bent with foot pointing away), 60° (middle of the range of knee flexion), and 90° (foot is at a
perpendicular to the hip regarding the knee).
The order in which the knee angles were presented for testing was randomized across participants.
Overall, participants contracted their muscles at each angle 6 times, with each contraction lasting 5 seconds,
with a 3-minute break between each contraction.

3.1.2 EMG data recording

For all the four fixed knee angles with maximal muscle effort EMG data was recorded. For this purpose
sensor pads were attached to record from the knee muscles Rectus femoris (RF), Vastus Lateralis (VL),
Vastus Medialis (VM), Semitendinosus (Se) and Biceps Femoris (BF). For recording wireless sEMG
sensors (Delsys TrignoTM system; at 1.9 kHz, the bandwidth of 20 to 450 Hz) were used. Electrode
placement and recording sites were selected based on the SENIAM protocol ((Rainoldi et al., 2004)).
We used anatomical landmarks to identify the muscles following the SENIAM guidelines ((Rainoldi
et al., 2004)). Prior to placement of sEMG electrodes, relevant skin areas were shaved and cleaned with
isopropyl alcohol, abraded with preparation gel (Nuprep, NRSign Inc., Canada), ((Merletti et al., 1998)).
The electrode placement was verified in each subject by palpating the muscles and asking participants
to perform a muscle contraction. The root-mean-square (RMS) of the evoked muscle activity was then
calculated. Activity across muscles was normalized to that in RF, which was voluntarily activated by the
participants at each angle in both tasks.

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Figure 2. Muscles of the simulated lower limbs considered in our experiment: Rectus Femoris, Vastus
Lateralis, Vastus Medialis, Semitendinosus, Biceps Femoris, Medial Gastrocnemius, Tibialis Anterior

3.2 Simulation Architecture

EMG data analysis reveals insights into correlation between muscle activation and knee angle, but solely
looking at the recorded EMG data a conclusion about resulting joint torques cannot be derived. We therefore
reconstruct the physical human knee extension study in a simulated environment: We model a virtual room
that contains an experiment bed and a musculoskeletal body model as a physics simulation in the NRP.
Figure 1 shows both an exemplary test setup of the original participant study (left) and its replication with
the musculoskeletal simulation as the basis for the experiments described in this paper.
An available OpenSim model of the lower limb ((Au and Dunne, 2013)) ((Anderson and Pandy, 1999))
((Delp et al., 1990)) is adapted for this study and its implementation in the NRP. Joints are reduced to basic
revolute motions and only muscles recorded in the physical study are used. These are visualized in Figure 2:
Rectus Femoris (RF), Vastus Lateralis (VL), Vastus Medialis (VM), Semitendinosus (Se), Biceps Femoris
(BF) as well Medial Gastrocnemius (MG) and Tibialis Anterior (TA). All muscles are simulated according
to ”Thelen2003” ((Thelen, 2003)) hill type models that emulate characteristics of elasticity and damping.
The torso is fixated to the virtual bed, the right leg can move in a planar space in line with the physical
setup. We implement a ROS control node in Python that controls simulated muscles with an activation
value in range [0,1] (0 represents a fully relaxed muscle and 1 expresses maximal activation). Muscle
synergies as well as resulting biomechanic behaviors measured in terms of joint angles and torques are
recorded for analysis.
In this paper we demonstrate a pipeline that consists of two different control and evaluation steps to
actuate the musculoskeletal model. First, we calculate normalized muscle activation values from EMG data
collected during the participant study. Second, we implement GA to compute an optimal muscle control
pattern by active trial on the simulated model. Figure 3 visualizes the architecture, that is centered around
the virtual experiment replicate, conceptually. In both control steps we interface derived muscle activation
data with the physics simulation by means of ROS topics. As a result we inspect and record knee joint
angles and torques on the simulated model.

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Figure 3. Experiment setup in the Neurorobotics Platform with two distinct control approaches: EMG
data from the participant study is processed and applied to the simulated model to record resulting knee
forces. In a second step optimal synergies are calculated by Genetic Algorithms using the simulation model
as test and evaluation bed.

4 DATA PROCESSSING
Data passes through several steps before the final virtual experiment can be performed. First, the raw EMG
data is preprocessed and muscle activations are extracted from the trial recordings. The normalized inputs
are then fed into the NRP simulated muscles and the resulting torques are measured. Finally, these torques
are taken as reference and a GA is used to generate muscle activation configurations which replicate the
measured values.

4.1 EMG Data Analysis

4.1.1 Trial Localisation
To perform the experiment, the trials have to be isolated and extracted from the original recordings
and the EMG signals have to be preprocessed and readied for the simulation. As previously stated in
subsubsection 3.1.1, the experiments consists of 6 trials, each lasting 5 seconds, with a 3 minute break in
between. Signals are first transferred into frequency domain, rendering 7 spectrograms per experiment,
corresponding to the 7 muscles of interest. The spectrograms are then summed into a single muscle activity
spectrogram Figure 4 (top) which, in turn, is collapsed into a 2D plot Figure 4 (middle) by further summing
the amplitudes over all frequencies at any given time point. Each time the activity plot is greater than a
threshold determined by the SNR, an activity event is marked in time domain. Since it is known that each
experiment has 6 trials, the K-means algorithm is used to find the trial origin of each activity event by
clustering them in 6 clusters. Finally, the median time point of a trial’s activity events determine its central
time-wise occurrence (Figure 4 bottom).
4.1.2 Signal Preprocessing
The data contains noise components which have to be filtered out. Moreover, only a specific bandwidth
may offer relevant information for further analysis. By observing the signals in frequency domain, it
becomes evident that most high amplitude activity occurs in the lower end of the spectrum, as seen in
Figure 5. Therefore, to increase the signal analysis reliability, we need to find a heuristic that automates
calculating a cut-off point that is tailored to our data set. The FFT analysis showed that lower frequencies
are of higher amplitude and are in fact a minority when compared the rest of the spectrum, a property which

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Figure 4. EMG data knee extension trial localization: (top) Activity spectrogram of muscle all recordings:
Frequency spectograms for all recorded muscles are added up to identify overall muscle activation during a
participant trial session. (middle) Summed activity spectrogram: Frequencies are added up at any given time
point to spot knee extension trial durations. (bottom) Identified knee extension trials in original recorded
EMG data (colors represent individual muscles): A participant executes several trials of knee extension in a
row, we apply signal processing to identify trial duration (vertical lines) and centers (crosses).

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has proven useful in analyzing the signal from a statistical angle. The proposed heuristic is as follows:
After averaging the FFT values across all study experiments and creating an amplitude-wise histogram
of the frequencies, we fit a binomial distribution envelope to said histogram. We then find that the first
outlier outside the standard deviation acts as a good amplitude threshold. The highest frequency reaching
this threshold will therefore be considered the cut-off point.

Figure 5. Frequency domain plot: The FFT-generated data is averaged over all trials, which shows that
the most prominent frequencies lie within the lower end of the spectrum. All frequencies higher than the
computed cut-off point will be ignored in further analysis

4.1.3 Feature Extraction

To be consistent with the study experiment, muscle activation data has to be inferred from the EMG
signals. It is known that a muscle unit (MU) exerts a muscle unit activation potential (MUAP) when
activated. An increased firing rate of a neuron translates into a higher stimulation of the muscle fibers,
resulting in a sustained force (tetanic contraction) in the MU. Furthermore, due to the size principle in MU
recruitment (((Mendell, 2005))), larger neurons, associated with a higher firing threshold are activated with
the increase of force, which can be observed as an increase of voltage in the EMG recordings. Taking these
into account, our muscle force approximation heuristic equates to

X
high
F = f × v(f )
f =low

A weighted sum where each constituent frequency component is multiplied by its amplitude.

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4.2 From Muscle Activation to Simulation Control

Once the EMG recordings have been converted to muscle activation scalars, these values are normalized
and applied on the NRP leg model muscles. Consequentially, the virtual muscles are contracted and the leg
is extended with a resulting knee torque. The NRP does not provide a way to directly measure a muscle
generated torque in a given joint. However, it does allow dynamic interaction with the model via its Python
API. Therefore, by applying an increasingly stronger virtual torque opposing the muscle generated one
(shown in Figure 6), once the leg reaches its original bent position it can be inferred that the artificial
force equals the muscle driven one. The approach of applying torques that are increasing is supported by
((Beltman et al., 2004)).

Figure 6. Knee torque evaluation on the simulated musculoskeletal model in the Neurorobotics Platform:
Muscles are activated (muscle color coding: blue - no activation, red - maximal activation)) by either
processed EMG signals or a Genetic Algorithm Muscle generated torque (red arrow). A counter acting
knee torque (yellow arrow) is iteratively increased until the goal knee angle is reached.

4.3 Genetic Algorithms to Compute Optimal Muscle Activation

Having extracted the knee torques from the original EMG recordings, using the NRP simulation, we can
test whether the same rotational force can be achieved through different synergies. To do this, a GA is
used in conjunction with the simulation to evolve an activation pattern that matches the target torque. The
GA makes constant use of the simulation to measure the fitness of its population. In this problem context,
each individual has 7 genes representing the activations for the controlled muscles. Its fitness is defined
by cos(|acurrent − atarget |), where acurrent is the knee angle observed in the simulation using the current
individual’s activations and atarget is the target angle of the algorithm.

While this evolutionary approach can find muscle configurations that match the target study experiment
torques, it is not guaranteed that any given solution has at least a fully tensed muscle. Each gene within an
individual is created randomly with a value between 0 and 1. This means that the configuration does not
represent maximal voluntary effort. To mitigate this, the genes of an individual are scaled to the maximal
value which becomes 1, while the others increase proportionally.

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Figure 7. Muscle to knee angle Pearson correlations for multiple patients: RF, VL and VM show a strong
negative muscle activation correlation with given angle, ST and TA a positive correlation.

5 RESULTS

5.1 EMG Data Analysis

The muscle activation approximation heuristic described in subsubsection 4.1.3 demonstrates results
in accordance with physical expectations. As seen in Figure 7, the quadriceps muscles (Rectus Femoris,
Vastus Lateralis, Vastus Medialis) are inversely correlated with the knee angle, while the posterior muscles
(Semitendinosus, Biceps Femoris) show weak correlations as they don’t take an active part in the leg
extension effort.

5.2 Simulated Knee Extension

The NRP has proven crucial in analysing the resulting knee torque by applying the EMG derived muscle
activations. As seen in Figure 8, the simulation is showing under which trials the subject might not have
performed the maximum voluntary effort study experiment correctly (i.e. the second 20 and 60 degree
trials show below average muscular activation when compared to the rest of the trials).

5.3 Comparison of EMG derived and GA generated Muscle Activation

Our experiments have shown that the GA reaches a conclusion fairly rapidly after around 20 generations.
However, since the fitness function waits a couple of seconds for the simulation to reach a stable position
with the evaluation of new individual, the entire process may take up to tens of minutes.

Comparing natural and evolved muscle activations achieving the same extension torque, configurations
are not linearly correlated for any given subject and angle. This is to be expected indeed, as even comparing
two experiments belonging to two different subjects, recorded at the same angle does not present any
relevant similarity.

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Figure 8. Knee torque for subject aad: Generated torques show a common pattern across trials and non
optimal trial executions can be identified.

Figure 9 shows a detailed comparison between the natural and the evolved synergies for two exemplary
subjects at at a given angle. The GA found a suitable extension force pattern which closely resembles the
original recorded values.

Figure 9. Positive comparison of natural vs evolved synergies: The Genetic Algorithm computes synergies
that recreate the muscle activation of processed EMG data of the participant study.

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However, Figure 10 shows that while the algorithm does reach a valid extension effort end state, its
results can also end up quite distinct from the original, natural configuration.

Figure 10. Negative comparison of natural vs evolved synergies: The Genetic Algorithm recreates the
knee torque of study participants but identifies different synergies to reach the same torque.

The only consistent characteristic in all subjects for both approaches is the overall dominance of the
quadriceps extensor over the posterior contracting muscles. Therefore, the conclusion is that the same
results, both in pose and in extension torque, can be achieved by different activation patterns.

6 CONCLUSION
In this paper we introduced a simulation framework that uses a virtual musculoskeletal model in the NRP
for calculating effective joint torques of recorded surface EMG data. The model skeleton is simulated with
rigid body dynamics in Gazebo and extended with hill type muscles of OpenSim. Within our framework
we implemented two different control components to actuate the virtual model. First, we analyzed surface
EMG data and computed normalized muscle activation to control the simulated model. We could replicate
the experimental study virtually and inspected the physical impact of muscle forces and joint torques by
applying increasing counteracting torques. Both force values are highly relevant research objectives ((Zhu
et al., 2017)) ((Zhou et al., 2011)) but could only be accessed invasively so far ((Roberts and Gabaldón,
2008)) ((Disselhorst-Klug et al., 2009)). Furthermore, our implementation makes use of a physics simulated
model in a virtual environment and hereby is more generic than other approaches with e.g. LabView in
((Zuchruf et al., 2021)). Using this model in a second step we implemented a Genetic Algorithm that
computes optimal muscle control configurations that can reproduce observed joint torques. Overall, the
framework is implemented using ROS interfaces and design tools provided with the NRP and hereby is
highly modular and can easily be applied to a variety of musculoskeletal models and experiment scenarios.
In this work, we demonstrated the capabilities of our framework and its advantages for EMG evaluation
with specific data from a human knee extension study. For this purpose we integrated a human
musculoskeletal model of the lower limbs into the NRP and hereby replicated the physical study setup
in-silico. In line with the physical constraints applied in the human participant study the simulated leg in

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the NRP is restricted to motions in a vertical space. However, the simulated model can easily be extended
(e.g. in terms of number of muscles, Degrees of Freedom and limb) and hereby opens up the introduced
framework for a variety of further studies in the future. Previous work with musculoskeletal models in the
NRP focused on rodent motion control paradigms to study stroke rehabilitation in the cortex ((Mascaro
et al., 2020)). We investigated neural activation signals to muscles, the lowest level of neural activation in
the motion control hierarchy contributing to a better understanding of the descending pathways of motor
control. The data analysis showed that quadriceps muscles are inversely correlated with the knee angle,
while the posterior muscles show weak correlations. With the simulated model we demonstrated that even
with the same goal knee angles participants applied different muscle configurations to achieve these.
With our GA approach, we can reproduce this variability of synergies and showcase additional control
strategies leading to the same knee torque. The GA suggests solutions that match the experimental outcomes,
but also some unlike what the subjects produced - e.g. in individuals there is maximal activity in primary
muscles while the GA also finds solutions with increased activity across multiple muscles. This is maybe
because GA is unbiased and not working within the human biomechanical constraints.
Overall, the NRP allowed us for the first time to know and reproduce the effective joint torques and
muscle synergies that are generated during a task. The observed variability supports the idea that the
muscle interactions are not all hardwired or predefined but fairly flexible even if the endpoint or the torque
generated is almost the same across all individuals. The observed muscle recruiting requires a neural
control system that is less rigid and responsive to the specific needs, as predicted by ((York et al., 2021))
recently, where they show that the proprioceptive inputs are capable of affecting the muscle recruitment
pattern depending on the need. Our study shows that the synergies generated are mapped to the specific
need too, so the controller is probably modulated by the sensory perception to produce both the knee
torque to be generated. This can also explain how to account for the state of the muscle and the level of
recruitment of the fibres or state of fatigue that it may be in when conducting a task.

CONFLICT OF INTEREST STATEMENT

The authors declare that the research was conducted in the absence of any commercial or financial
relationships that could be construed as a potential conflict of interest.

ACKNOWLEDGMENTS
This project/research has received funding from the European Union’s Horizon 2020 Framework
Programme for Research and Innovation under the Specific Grant Agreement No. 785907 (Human
Brain Project SGA2) and No. 945539 (Human Brain Project SGA3). PS was funded by the Royal Thai
Government Scholarships.

STUDY DETAILS
This study of knee flexion was conducted with healthy participants (n = 17, female =8) within the age of
18-30 (24.4± 2.57 years). All participants were healthy and free on any injuries, fully informed about the
tests, and all gave their written, informed consent before participation. The study was conducted according
to the declaration of Helsinki and was approved by the Local Ethics Committee of the University of
Leeds (reference number BIOSCI 16-004). Participants were excluded if they d 1) recently done exercise
within 48 hours prior to testing 2) Knee stiffness, self-reported pain 3) Muscle or knee joint injury 4)

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Used recreational or performance-enhancing drugs 5) Ingested alcohol in the previous 24 hours 6) Unable
to provide informed consent. The data were recorded directly onto a PC running Spike 2.8. version 10
(Cambridge Electronic Designed limited, (CED)) software using the Delsys talker (CED) for later offline
processing and analysis.

AUTHOR CONTRIBUTION
BF conceptualized the experiment design of EMG data evaluation in a virtual simulation environment
exploiting the NRP simulation in discussion with MdK. PS conducted the participant study and collected
the EMG data under supervision of SC and SA. Human experiments were designed by PS and SC. AK
supervised the NRP development and provided input for the given use case. CS and BF analyzed the
data and implemented the experiment in discussion with SC and MdK. BF wrote the paper with text
input from MdK and SC for the introduction and EMG data collection, as well as CS for the analysis and
implementation.

REFERENCES
U. Albanese, K. Sharma, B. Feldotto, M. Akl, S. Weber, H. Mahmud, M. Angelidis, A. von Arnim,
K. Cantero, G. Hinkel, F. Aichele, M. Welter, S. Murphy, L. Guyot, C. Sousa, Y. Schmid, M.-O.
Gewaltig, and A. Knoll. HBP NeuroRobotics Platform, 2018.
K. Amunts, C. Ebell, J. Muller, M. Telefont, A. Knoll, and T. Lippert. The Human Brain Project: Creating
a european research infrastructure to decode the human brain. Neuron, 92(3):574–581, 2016. doi:
10.1016/j.neuron.2016.10.046.
F. C. Anderson and M. G. Pandy. A dynamic optimization solution for vertical jumping in three dimensions.
Computer Methods in Biomechanics and Biomedical Engineering, 2(3):201–231, 1999. doi: 10.1080/
10255849908907988.
C. Au and J. Dunne. Gait 2392 and 2354 models, 2013. URL https://simtk-confluence.
stanford.edu:8443/display/OpenSim/Gait+2392+and+2354+Models. Accessed
06/2018.
J. Beltman, A. Sargeant, W. Van Mechelen, and A. De Haan. Voluntary activation level and muscle fiber
recruitment of human quadriceps during lengthening contractions. Journal of Applied Physiology, 97(2):
619–626, 2004.
S. L. Delp, J. P. Loan, M. G. Hoy, F. E. Zajac, E. L. Topp, and J. M. Rosen. An interactive graphics-based
model of the lower extremity to study orthopaedic surgical procedures. IEEE Transactions on Biomedical
Engineering, 37(8):757–767, Aug 1990. ISSN 1558-2531. doi: 10.1109/10.102791.
S. L. Delp, F. C. Anderson, A. S. Arnold, P. Loan, A. Habib, C. T. John, E. Guendelman, and D. G.
Thelen. Opensim: open-source software to create and analyze dynamic simulations of movement.
IEEE transactions on bio-medical engineering, 54(11):1940–1950, 2007. ISSN 0018-9294. doi:
10.1109/TBME.2007.901024.
C. Disselhorst-Klug, T. Schmitz-Rode, and G. Rau. Surface electromyography and muscle force: Limits in
semg–force relationship and new approaches for applications. Clinical Biomechanics, 24(3):225–235,
2009.
A. R. Fugl-Meyer, L. Jääskö, I. Leyman, S. Olsson, and S. Steglind. The post-stroke hemiplegic patient. 1.
a method for evaluation of physical performance. Scandinavian journal of Rehabilitation Medicine, 7
(1):13–31, 1975.
M.-O. Gewaltig and M. Diesmann. Nest (neural simulation tool). Scholarpedia, 2(4):1430, 2007.

14
Feldotto et al., 2022 Evaluating Muscle Synergies

G. Hinkel, H. Groenda, S. Krach, L. Vannucci, O. Denninger, N. Cauli, S. Ulbrich, A. Roennau, E. Falotico,

M.-O. Gewaltig, et al. A framework for coupled simulations of robots and spiking neuronal networks.
Journal of Intelligent & Robotic Systems, 85(1):71–91, 2017.
A. Knoll and M.-O. Gewaltig. Neurorobotics: A strategic pillar of the human brain project. Science
Robotics, pages 2–3, 2016.
N. Koenig and A. Howard. Design and use paradigms for gazebo, an open-source multi-robot simulator. In
2004 IEEE, pages 2149–2154. IEEE, 2004. ISBN 0-7803-8463-6. doi: 10.1109/IROS.2004.1389727.
H. Markram, K. Meier, T. Lippert, S. Grillner, R. Frackowiak, S. Dehaene, A. Knoll, H. Sompolinsky,
K. Verstreken, J. DeFelipe, S. Grant, J.-P. Changeux, and A. Saria. Introducing the human brain project.
Procedia Computer Science, 7:39–42, 2011. ISSN 18770509. doi: 10.1016/j.procs.2011.12.015.
A. L. A. Mascaro, E. Falotico, S. Petkoski, M. Pasquini, L. Vannucci, N. Tort-Colet, E. Conti, F. Resta,
C. Spalletti, S. T. Ramalingasetty, et al. Experimental and computational study on motor control
and recovery after stroke: Toward a constructive loop between experimental and virtual embodied
neuroscience. Frontiers in Systems Neuroscience, 14, 2020.
L. M. Mendell. The size principle: a rule describing the recruitment of motoneurons. Journal of
Neurophysiology, 93(6):3024–3026, 2005.
R. Merletti, A. Fiorito, L. Lo Conte, and C. Cisari. Repeatability of electrically evoked emg signals in
the human vastus medialis muscle. Muscle & Nerve: Official Journal of the American Association of
Electrodiagnostic Medicine, 21(2):184–193, 1998.
M. Quigley, K. Conley, B. Gerkey, J. Faust, T. Foote, J. Leibs, R. Wheeler, and A. Y. Ng. Ros: an
open-source robot operating system. In ICRA workshop on open source software, volume 3, page 5.
Kobe, Japan, 2009.
A. Rainoldi, G. Melchiorri, and I. Caruso. A method for positioning electrodes during surface emg
recordings in lower limb muscles. Journal of Neuroscience Methods, 134(1):37–43, 2004.
T. J. Roberts and A. M. Gabaldón. Interpreting muscle function from emg: lessons learned from direct
measurements of muscle force. Integrative and Comparative Biology, 48(2):312–320, 2008.
A. Seth, J. L. Hicks, T. K. Uchida, A. Habib, C. L. Dembia, J. J. Dunne, C. F. Ong, M. S. DeMers,
A. Rajagopal, M. Millard, S. R. Hamner, E. M. Arnold, J. R. Yong, S. K. Lakshmikanth, M. A. Sherman,
J. P. Ku, and S. L. Delp. Opensim: Simulating musculoskeletal dynamics and neuromuscular control
to study human and animal movement. PLoS computational biology, 14(7):e1006223, 2018. doi:
10.1371/journal.pcbi.1006223.
D. G. Thelen. Adjustment of muscle mechanics model parameters to simulate dynamic contractions
in older adults. Journal of Biomechanical Engineering, 125(1):70–77, 2003. ISSN 01480731. doi:
10.1115/1.1531112.
G. J. R. York, H. Osborne, P. Sriya, S. Astill, M. de Kamps, and S. Chakrabarty. The effect of limb position
on a static knee extension task can be explained with a simple spinal cord circuit model. Journal of
Neurophysiology, 2021.
P. Zhou, N. L. Suresh, and W. Z. Rymer. Surface electromyogram analysis of the direction of isometric
torque generation by the first dorsal interosseous muscle. Journal of Neural Engineering, 8(3):036028,
2011.
X. Zhu, X. Zhang, X. Tang, X. Gao, and X. Chen. Re-evaluating electromyogram–force relation in healthy
biceps brachii muscles using complexity measures. Entropy, 19(11):624, 2017.
Y. Zuchruf, T. Asmaria, R. Rulaningtyas, A. Rahmatillah, I. Kartika, and N. Rochman. Simulation of knee
joint angle estimation from emg signal for post acl reconstruction surgical rehabilitation. In Journal of
Physics: Conference Series, volume 1805, page 012019. IOP Publishing, 2021.

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