Publications by authors named "Dagmar Sternad"

94 Publications

Preparing to move: Setting initial conditions to simplify interactions with complex objects.

PLoS Comput Biol 2021 12 17;17(12):e1009597. Epub 2021 Dec 17.

Department of Electrical and Computer Engineering, Northeastern University, Boston, Massachusetts, United States of America.

Humans dexterously interact with a variety of objects, including those with complex internal dynamics. Even in the simple action of carrying a cup of coffee, the hand not only applies a force to the cup, but also indirectly to the liquid, which elicits complex reaction forces back on the hand. Due to underactuation and nonlinearity, the object's dynamic response to an action sensitively depends on its initial state and can display unpredictable, even chaotic behavior. With the overarching hypothesis that subjects strive for predictable object-hand interactions, this study examined how subjects explored and prepared the dynamics of an object for subsequent execution of the target task. We specifically hypothesized that subjects find initial conditions that shorten the transients prior to reaching a stable and predictable steady state. Reaching a predictable steady state is desirable as it may reduce the need for online error corrections and facilitate feed forward control. Alternative hypotheses were that subjects seek to reduce effort, increase smoothness, and reduce risk of failure. Motivated by the task of 'carrying a cup of coffee', a simplified cup-and-ball model was implemented in a virtual environment. Human subjects interacted with this virtual object via a robotic manipulandum that provided force feedback. Subjects were encouraged to first explore and prepare the cup-and-ball before initiating a rhythmic movement at a specified frequency between two targets without losing the ball. Consistent with the hypotheses, subjects increased the predictability of interaction forces between hand and object and converged to a set of initial conditions followed by significantly decreased transients. The three alternative hypotheses were not supported. Surprisingly, the subjects' strategy was more effortful and less smooth, unlike the observed behavior in simple reaching movements. Inverse dynamics of the cup-and-ball system and forward simulations with an impedance controller successfully described subjects' behavior. The initial conditions chosen by the subjects in the experiment matched those that produced the most predictable interactions in simulation. These results present first support for the hypothesis that humans prepare the object to minimize transients and increase stability and, overall, the predictability of hand-object interactions.
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http://dx.doi.org/10.1371/journal.pcbi.1009597DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8683040PMC
December 2021

Ambulatory Voice Biofeedback: Acquisition and Retention of Modified Daily Voice Use in Patients With Phonotraumatic Vocal Hyperfunction.

Am J Speech Lang Pathol 2022 01 29;31(1):409-418. Epub 2021 Nov 29.

Massachusetts General Hospital, Boston.

Purpose: Voice ambulatory biofeedback (VAB) has potential to improve carryover of therapeutic voice use into daily life. Previous work in vocally healthy participants demonstrated that motor learning inspired variations to VAB produced expected differences in acquisition and retention of modified daily voice use. This proof-of-concept study was designed to evaluate whether these VAB variations have the same desired effects on acquisition and retention in patients with phonotraumatic vocal hyperfunction (PVH).

Method: Seventeen female patients with PVH wore an ambulatory voice monitor for 6 days: three baseline days, one biofeedback day, one short-term retention day, and one long-term retention day. Short- and long-term retention were 1- and 7-days postbiofeedback, respectively. Patients were block-randomized to receive one of three types of VAB: 100%, 25%, and Summary. Performance was measured in terms of adherence time below a subject-specific vocal intensity threshold.

Results: All three types of VAB produced a biofeedback effect with 13 out of 17 patients displaying an increase in adherence time compared to baseline days. Additionally, multiple patients from each VAB group increased their adherence time during short- and/or long-term retention monitoring compared to baseline.

Conclusions: These findings show that VAB can be associated with acquisition and retention of desired voice use in patients with PVH. Specifically, all three feedback types improved multiple patients' performance and retention for up to 1 week after biofeedback removal. Future work can investigate the impact of incorporating VAB into voice therapy.
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http://dx.doi.org/10.1044/2021_AJSLP-21-00141DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC9135013PMC
January 2022

Central nervous system physiology.

Clin Neurophysiol 2021 12 14;132(12):3043-3083. Epub 2021 Oct 14.

Department of Neurology and Stroke, and Hertie Institute for Clinical Brain Research, Eberhard Karls University, Tübingen, Germany.

This is the second chapter of the series on the use of clinical neurophysiology for the study of movement disorders. It focusses on methods that can be used to probe neural circuits in brain and spinal cord. These include use of spinal and supraspinal reflexes to probe the integrity of transmission in specific pathways; transcranial methods of brain stimulation such as transcranial magnetic stimulation and transcranial direct current stimulation, which activate or modulate (respectively) the activity of populations of central neurones; EEG methods, both in conjunction with brain stimulation or with behavioural measures that record the activity of populations of central neurones; and pure behavioural measures that allow us to build conceptual models of motor control. The methods are discussed mainly in relation to work on healthy individuals. Later chapters will focus specifically on changes caused by pathology.
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http://dx.doi.org/10.1016/j.clinph.2021.09.013DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8863401PMC
December 2021

Frequency-dependent force direction elucidates neural control of balance.

J Neuroeng Rehabil 2021 09 25;18(1):145. Epub 2021 Sep 25.

Department of Mechanical Engineering, Massachusetts Institute of Technology, Cambridge, MA, 02139, USA.

Background: Maintaining upright posture is an unstable task that requires sophisticated neuro-muscular control. Humans use foot-ground interaction forces, characterized by point of application, magnitude, and direction to manage body accelerations. When analyzing the directions of the ground reaction forces of standing humans in the frequency domain, previous work found a consistent pattern in different frequency bands. To test whether this frequency-dependent behavior provided a distinctive signature of neural control or was a necessary consequence of biomechanics, this study simulated quiet standing and compared the results with human subject data.

Methods: Aiming to develop the simplest competent and neuromechanically justifiable dynamic model that could account for the pattern observed across multiple subjects, we first explored the minimum number of degrees of freedom required for the model. Then, we applied a well-established optimal control method that was parameterized to maximize physiologically-relevant insight to stabilize the balancing model.

Results: If a standing human was modeled as a single inverted pendulum, no controller could reproduce the experimentally observed pattern. The simplest competent model that approximated a standing human was a double inverted pendulum with torque-actuated ankle and hip joints. A range of controller parameters could stabilize this model and reproduce the general trend observed in experimental data; this result seems to indicate a biomechanical constraint and not a consequence of control. However, details of the frequency-dependent pattern varied substantially across tested control parameter values. The set of parameters that best reproduced the human experimental results suggests that the control strategy employed by human subjects to maintain quiet standing was best described by minimal control effort with an emphasis on ankle torque.

Conclusions: The findings suggest that the frequency-dependent pattern of ground reaction forces observed in quiet standing conveys quantitative information about human control strategies. This study's method might be extended to investigate human neural control strategies in different contexts of balance, such as with an assistive device or in neurologically impaired subjects.
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http://dx.doi.org/10.1186/s12984-021-00907-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8466643PMC
September 2021

The effects of continuous oromotor activity on speech motor learning: speech biomechanics and neurophysiologic correlates.

Exp Brain Res 2021 Dec 15;239(12):3487-3505. Epub 2021 Sep 15.

Department of Rehabilitation Sciences, MGH Institute of Health Professions, Building 79/96, 2nd Floor 13th Street, Boston, MA, 02129, USA.

Sustained limb motor activity has been used as a therapeutic tool for improving rehabilitation outcomes and is thought to be mediated by neuroplastic changes associated with activity-induced cortical excitability. Although prior research has reported enhancing effects of continuous chewing and swallowing activity on learning, the potential beneficial effects of sustained oromotor activity on speech improvements is not well-documented. This exploratory study was designed to examine the effects of continuous oromotor activity on subsequent speech learning. Twenty neurologically healthy young adults engaged in periods of continuous chewing and speech after which they completed a novel speech motor learning task. The motor learning task was designed to elicit improvements in accuracy and efficiency of speech performance across repetitions of eight-syllable nonwords. In addition, transcranial magnetic stimulation was used to measure the cortical silent period (cSP) of the lip motor cortex before and after the periods of continuous oromotor behaviors. All repetitions of the nonword task were recorded acoustically and kinematically using a three-dimensional motion capture system. Productions were analyzed for accuracy and duration, as well as lip movement distance and speed. A control condition estimated baseline improvement rates in speech performance. Results revealed improved speech performance following 10 min of chewing. In contrast, speech performance following 10 min of continuous speech was degraded. There was no change in the cSP as a result of either oromotor activity. The clinical implications of these findings are discussed in the context of speech rehabilitation and neuromodulation.
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http://dx.doi.org/10.1007/s00221-021-06206-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8599312PMC
December 2021

Predicting apneic events in preterm infants using cardio-respiratory and movement features.

Comput Methods Programs Biomed 2021 Sep 30;209:106321. Epub 2021 Jul 30.

Department of Neurology, Dell Medical School, Austin, TX 78712, United States; Oden Institute for Computational Sciences and Engineering, The University of Texas at Austin, Austin, TX 78712, United States. Electronic address:

Background And Objective: Preterm neonates are prone to episodes of apnea, bradycardia and hypoxia (ABH) that can lead to neurological morbidities or even death. There is broad interest in developing methods for real-time prediction of ABH events to inform interventions that prevent or reduce their incidence and severity. Using advances in machine learning methods, this study develops an algorithm to predict ABH events.

Methods: Following previous studies showing that respiratory instabilities are closely associated with bouts of movement, we present a modeling framework that can predict ABH events using both movement and cardio-respiratory features derived from routine clinical recordings. In 10 preterm infants, movement onsets and durations were estimated with a wavelet-based algorithm that quantified artifactual distortions of the photoplethysmogram signal. For prediction, cardio-respiratory features were created from time-delayed correlations of inter-beat and inter-breath intervals with past values; movement features were derived from time-delayed correlations with inter-breath intervals. Gaussian Mixture Models and Logistic Regression were used to develop predictive models of apneic events. Performance of the models was evaluated with ROC curves.

Results: Performance of the prediction framework (mean AUC) was 0.77 ± 0.04 for 66 ABH events on training data from 7 infants. When grouped by the severity of the associated bradycardia during the ABH event, the framework was able to predict 83% and 75% of the most severe episodes in the 7-infant training set and 3-infant test set, respectively. Notably, inclusion of movement features significantly improved the predictions compared with modeling with only cardio-respiratory signals.

Conclusions: Our findings suggest that recordings of movement provide important information for predicting ABH events in preterm infants, and can inform preemptive interventions designed to reduce the incidence and severity of ABH events.
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http://dx.doi.org/10.1016/j.cmpb.2021.106321DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8898595PMC
September 2021

Hand pose selection in a bimanual fine-manipulation task.

J Neurophysiol 2021 07 9;126(1):195-212. Epub 2021 Jun 9.

Learning Algorithms and Systems Laboratory, School of Engineering, École Polytechnique Fédérale de Lausanne, Lausanne, Switzerland.

Many daily tasks involve the collaboration of both hands. Humans dexterously adjust hand poses and modulate the forces exerted by fingers in response to task demands. Hand pose selection has been intensively studied in unimanual tasks, but little work has investigated bimanual tasks. This work examines hand poses selection in a bimanual high-precision-screwing task taken from watchmaking. Twenty right-handed subjects dismounted a screw on the watch face with a screwdriver in two conditions. Results showed that although subjects used similar hand poses across steps within the same experimental conditions, the hand poses differed significantly in the two conditions. In the free-base condition, subjects needed to stabilize the watch face on the table. The role distribution across hands was strongly influenced by hand dominance: the dominant hand manipulated the tool, whereas the nondominant hand controlled the additional degrees of freedom that might impair performance. In contrast, in the fixed-base condition, the watch face was stationary. Subjects used both hands even though single hand would have been sufficient. Importantly, hand poses decoupled the control of task-demanded force and torque across hands through virtual fingers that grouped multiple fingers into functional units. This preference for bimanual over unimanual control strategy could be an effort to reduce variability caused by mechanical couplings and to alleviate intrinsic sensorimotor processing burdens. To afford analysis of this variety of observations, a novel graphical matrix-based representation of the distribution of hand pose combinations was developed. Atypical hand poses that are not documented in extant hand taxonomies are also included. We study hand poses selection in bimanual fine motor skills. To understand how roles and control variables are distributed across the hands and fingers, we compared two conditions when unscrewing a screw from a watch face. When the watch face needed positioning, role distribution was strongly influenced by hand dominance; when the watch face was stationary, a variety of hand pose combinations emerged. Control of independent task demands is distributed either across hands or across distinct groups of fingers.
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http://dx.doi.org/10.1152/jn.00635.2020DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8325606PMC
July 2021

Effect of spontaneous movement on respiration in preterm infants.

Exp Physiol 2021 05 18;106(5):1285-1302. Epub 2021 Mar 18.

Departments of Biology, Electrical and Computer Engineering & Physics, Northeastern University, Boston, MA, USA.

New Findings: What is the central question of this study? The respiratory centres in the brainstem that control respiration receive inputs from various sources, including proprioceptors in muscles and joints and suprapontine centres, which all affect limb movements. What is the effect of spontaneous movement on respiration in preterm infants? What is the main finding and its importance? Apnoeic events tend to be preceded by movements. These activity bursts can cause respiratory instability that leads to an apnoeic event. These findings show promise that infant movements might serve as potential predictors of life-threatening apnoeic episodes, but more research is required.

Abstract: A common condition in preterm infants (<37 weeks' gestational age) is apnoea resulting from immaturity and instability of the respiratory system. As apnoeas are implicated in several acute and long-term complications, prediction of apnoeas may preempt their onset and subsequent complications. This study tests the hypothesis that infant movements are a predictive marker for apnoeic episodes and examines the relation between movement and respiration. Movement was detected using a wavelet algorithm applied to the photoplethysmographic signal. Respiratory activity was measured in nine infants using respiratory inductance plethysmography; in an additional eight infants, respiration and partial pressure of airway carbon dioxide ( ) were measured by a nasal cannula with side-stream capnometry. In the first cohort, the distribution of movements before and after the onset of 370 apnoeic events was compared. Results showed that apnoeic events were associated with longer movement duration occurring before apnoea onsets compared to after. In the second cohort, respiration was analysed in relation to movement, comparing standard deviation of inter-breath intervals (IBI) before and after apnoeas. Poincaré maps of the respiratory activity quantified variability of airway in phase space. Movement significantly increased the variability of IBI and . Moreover, destabilization of respiration was dependent on the duration of movement. These findings support that bodily movements of the infants precede respiratory instability. Further research is warranted to explore the predictive value of movement for life-threatening events, useful for clinical management and risk stratification.
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http://dx.doi.org/10.1113/EP089143DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8087648PMC
May 2021

Neural Encoding and Representation of Time for Sensorimotor Control and Learning.

J Neurosci 2021 02 30;41(5):866-872. Epub 2020 Dec 30.

Brown University, Providence, RI 02912

The ability to perceive and produce movements in the real world with precise timing is critical for survival in animals, including humans. However, research on sensorimotor timing has rarely considered the tight interrelation between perception, action, and cognition. In this review, we present new evidence from behavioral, computational, and neural studies in humans and nonhuman primates, suggesting a pivotal link between sensorimotor control and temporal processing, as well as describing new theoretical frameworks regarding timing in perception and action. We first discuss the link between movement coordination and interval-based timing by addressing how motor training develops accurate spatiotemporal patterns in behavior and influences the perception of temporal intervals. We then discuss how motor expertise results from establishing task-relevant neural manifolds in sensorimotor cortical areas and how the geometry and dynamics of these manifolds help reduce timing variability. We also highlight how neural dynamics in sensorimotor areas are involved in beat-based timing. These lines of research aim to extend our understanding of how timing arises from and contributes to perceptual-motor behaviors in complex environments to seamlessly interact with other cognitive processes.
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http://dx.doi.org/10.1523/JNEUROSCI.1652-20.2020DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7880297PMC
February 2021

Quantitative Assessment of Learning and Retention in Virtual Vocal Function Exercises.

J Speech Lang Hear Res 2021 01 7;64(1):1-15. Epub 2020 Dec 7.

Northeastern University, Boston, MA.

Purpose Successful voice therapy requires the patient to learn new vocal behaviors, but little is currently known regarding how vocal motor skills are improved and retained. To quantitatively characterize the motor learning process in a clinically meaningful context, a virtual task was developed based on the Vocal Function Exercises. In the virtual task, subjects control a computational model of a ball floating on a column of airflow via modifications to mean airflow (L/s) and intensity (dB-C) to keep the ball within a target range representing a normative ratio (dB × s/L). Method One vocally healthy female and one female with nonphonotraumatic vocal hyperfunction practiced the task for 11 days and completed retention testing 1 and 6 months later. The mapping between the two execution variables (airflow and intensity) and one error measure (proximity to the normative ratio) was evaluated by quantifying distributional variability (tolerance cost and noise cost) and temporal variability (scaling index of detrended fluctuation analysis). Results Both subjects reduced their error over practice and retained their performance 6 months later. Tolerance cost and noise cost were positively correlated with decreases in error during early practice and late practice, respectively. After extended practice, temporal variability was modulated to align with the task's solution manifold. Conclusions These case studies illustrated, in a healthy control and a patient with nonphonotraumatic vocal hyperfunction, that the virtual floating ball task produces quantitative measures characterizing the learning process. Future work will further investigate the task's potential to enhance clinical assessment and treatments involving voice control. Supplemental Material https://doi.org/10.23641/asha.13322891.
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http://dx.doi.org/10.1044/2020_JSLHR-20-00357DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8608156PMC
January 2021

Back to reality: differences in learning strategy in a simplified virtual and a real throwing task.

J Neurophysiol 2021 01 4;125(1):43-62. Epub 2020 Nov 4.

Department of Biology, Electrical and Computer Engineering, and Physics, Northeastern University, Boston, Massachusetts.

Virtual environments have been widely used in motor neuroscience and rehabilitation, as they afford tight control of sensorimotor conditions and readily afford visual and haptic manipulations. However, typically, studies have only examined performance in the virtual testbeds, without asking how the simplified and controlled movement in the virtual environment compares to behavior in the real world. To test whether performance in the virtual environment was a valid representation of corresponding behavior in the real world, this study compared throwing in a virtual set-up with realistic throwing, where the task parameters were precisely matched. Even though the virtual task only required a horizontal single-joint arm movement, similar to many simplified movement assays in motor neuroscience, throwing accuracy and precision were significantly worse than in the real task that involved all degrees of freedom of the arm; only after 3 practice days did success rate and error reach similar levels. To gain more insight into the structure of the learning process, movement variability was decomposed into deterministic and stochastic contributions. Using the tolerance-noise-covariation decomposition method, distinct stages of learning were revealed: While tolerance was optimized first in both environments, it was higher in the virtual environment, suggesting that more familiarization and exploration was needed in the virtual task. Covariation and noise showed more contributions in the real task, indicating that subjects reached the stage of fine-tuning of variability only in the real task. These results showed that while the tasks were precisely matched, the simplified movements in the virtual environment required more time to become successful. These findings resonate with the reported problems in transfer of therapeutic benefits from virtual to real environments and alert that the use of virtual environments in research and rehabilitation needs more caution. This study compared human performance of the same throwing task in a real and a matched virtual environment. With 3 days' practice, subjects improved significantly faster in the real task, even though the arm and hand movements were more complex. Decomposing variability revealed that performance in the virtual environment, despite its simplified hand movements, required more exploration. Additionally, due to fewer constraints in the real task, subjects could modify the geometry of the solution manifold, by shifting the release position, and thereby simplify the task.
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http://dx.doi.org/10.1152/jn.00197.2020DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8087380PMC
January 2021

Human control of complex objects: Towards more dexterous robots.

Adv Robot 2020 16;34(17):1137-1155. Epub 2020 Jun 16.

Department of Biology, Northeastern University, Boston, Massachusetts 02115, USA.

Manipulation of objects with underactuated dynamics remains a challenge for robots. In contrast, humans excel at 'tool use' and more insight into human control strategies may inform robotic control architectures. We examined human control of objects that exhibit complex - underactuated, nonlinear, and potentially chaotic dynamics, such as transporting a cup of coffee. Simple control strategies appropriate for unconstrained movements, such as maximizing smoothness, fail as interaction forces have to be compensated or preempted. However, predictive control based on internal models appears daunting when the objects have nonlinear and unpredictable dynamics. We hypothesized that humans learn strategies that make these interactions predictable. Using a virtual environment subjects interacted with a virtual cup and rolling ball using a robotic visual and haptic interface. Two different metrics quantified predictability: stability or contraction, and mutual information between controller and object. In point-to-point displacements subjects exploited the contracting regions of the object dynamics to safely navigate perturbations. Control contraction metrics showed that subjects used a controller that exponentially stabilized trajectories. During continuous cup-and-ball displacements subjects developed predictable solutions sacrificing smoothness and energy efficiency. These results may stimulate control strategies for dexterous robotic manipulators and human-robot interaction.
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http://dx.doi.org/10.1080/01691864.2020.1777198DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7577404PMC
June 2020

Automated movement detection reveals features of maturation in preterm infants.

Annu Int Conf IEEE Eng Med Biol Soc 2020 07;2020:600-603

Nearly 10% of all births in the United States are preterm. Preterm birth is a major risk for developmental neuromotor disorders. Early characterization of a future developmental outcome is necessary to design early interventions. However, such evaluations are currently subjective and typically happen only several months after birth. The aim of this study was to quantify movement bouts after birth and to determine if features of maturation might be characterized. Four preterm infants were continuously monitored for several months, from a few days after birth until discharge, in the Neonatal Intensive Care Unit. Movement was quantified from the photoplethysmogram using a wavelet-based algorithm. In all 4 infants, maturation was associated with a decrease (p < 0.001) in the occurrence of movement bouts ≤ 30s and an increase (p < 0.001) in longer movement bouts (> 30s). The distribution of movement durations followed a power law function with its exponent defining the characteristic of the distribution. The exponent significantly increased with post-menstrual age. Future research will test whether these maturational changes can predict developmental outcomes.Clinical Relevance- Early identification of changes in features of preterm infant movement may be useful in predicting neuromotor development and potential disorders.
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http://dx.doi.org/10.1109/EMBC44109.2020.9176091DOI Listing
July 2020

Rigid soles improve balance in beam walking, but improvements do not persist with bare feet.

Sci Rep 2020 05 6;10(1):7629. Epub 2020 May 6.

Departments of Biology, Electrical and Computer Engineering, and Physics, Northeastern University, Boston, Massachusetts, USA.

Maintaining balance while walking on a narrow beam is a challenging motor task. One important factor is that the foot's ability to exert torque on the support surface is limited by the beam width. Still, the feet serve as a critical interface between the body and the external environment, and it is unclear how the mechanical properties of the feet affect balance. This study examined how constraining the motion of the foot joints with rigid soles influenced balance performance when walking on a beam. We recorded whole-body kinematics of subjects with varying skill levels as they walked on a narrow beam with and without wearing flat, rigid soles on their feet. We computed changes in whole-body motion and angular momentum across the two conditions. Results showed that walking with rigid soles improved balance performance in both expert and novice subjects, but that improvements in balance performance with rigid soles did not affect or transfer to subsequent task performance with bare feet. The absence of any aftereffects suggested that the improved balance performance resulting from constraining the foot joints by a rigid sole was the result of a mechanical effect rather than a change in neural control. Although wearing rigid soles can be used to assist balance, there appears to be limited benefit for training or rehabilitation of balance ability.
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http://dx.doi.org/10.1038/s41598-020-64035-yDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7203137PMC
May 2020

Robustness in Human Manipulation of Dynamically Complex Objects through Control Contraction Metrics.

IEEE Robot Autom Lett 2020 Apr 10;5(2):2578-2585. Epub 2020 Feb 10.

Salah Bazzi and Dagmar Sternad are in the Department of Electrical and Computer Engineering and the Department of Biology, Northeastern University, Boston, Massachusetts 02115.

Control and manipulation of objects with underactuated dynamics remains a challenge for robots. Due to their typically nonlinear dynamics, it is computationally taxing to implement model-based planning and control techniques. Yet humans can skillfully manipulate such objects, seemingly with ease. More insight into human control strategies may inform how to enhance control strategies in robots. This study examined human control of objects that exhibit complex - underactuated and nonlinear - dynamics. We hypothesized that humans seek to make their trajectories exponentially stable to achieve robustness in the face of external perturbations. A stable trajectory is also robust to the high levels of noise in the human neuromotor system. Motivated by the task of carrying a cup of coffee, a virtual implementation of transporting a cart-pendulum system was developed. Subjects interacted with the virtual system via a robotic manipulandum that provided a haptic and visual interface. Human subjects were instructed to transport this simplified system to a target position as fast as possible without 'spilling coffee', while accommodating different visible perturbations that could be anticipated. To test the hypothesis of exponential convergence, tools from the framework of control contraction metrics were leveraged to analyze human trajectories. Results showed that with practice the trajectories indeed became exponentially stable, selectively around the perturbation. While these findings are agnostic about the involvement of feedback and feedforward control, they do support the hypothesis that humans learn to make trajectories stable, consistent with achieving predictability.
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http://dx.doi.org/10.1109/lra.2020.2972863DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7098464PMC
April 2020

Portable Motion-Analysis Device for Upper-Limb Research, Assessment, and Rehabilitation in Non-Laboratory Settings.

IEEE J Transl Eng Health Med 2019 13;7:2800314. Epub 2019 Nov 13.

1Electrical & Computer Engineering and Physics DepartmentNortheastern UniversityBostonMA02115USA.

This study presents the design and feasibility testing of an interactive portable motion-analysis device for the assessment of upper-limb motor functions in clinical and home settings. The device engages subjects to perform tasks that imitate activities of daily living, e.g. drinking from a cup and moving other complex objects. Sitting at a magnetic table subjects hold a 3D printed cup with an adjustable magnet and move this cup on the table to targets that can be drawn on the table surface. A ball rolling inside the cup can enhance the task challenge by introducing additional dynamics. A single video camera with a portable computer tracks real-time kinematics of the cup and the rolling ball using a custom-developed, color-based computer-vision algorithm. Preliminary verification with marker-based 3D-motion capture demonstrated that the device produces accurate kinematic measurements. Based on the real-time 2D cup coordinates, audio-visual feedback about performance can be delivered to increase motivation. The feasibility of using this device in clinical diagnostics is demonstrated on 2 neurotypical children and also 3 children with upper-extremity impairments in the hospital, where conventional motion-analysis systems are difficult to use. The device meets key needs for clinical practice: 1) a portable solution for quantitative motor assessment for upper-limb movement disorders at non-laboratory clinical settings, 2) a low-cost rehabilitation device that can increase the volume of in-home physical therapy, and 3) the device affords testing and training a variety of motor tasks inspired by daily challenges to enhance self-confidence to participate in day-to-day activities.
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http://dx.doi.org/10.1109/JTEHM.2019.2953257DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6889943PMC
November 2019

Separating neural influences from peripheral mechanics: the speed-curvature relation in mechanically constrained actions.

J Neurophysiol 2020 05 11;123(5):1870-1885. Epub 2020 Mar 11.

Department of Mechanical Engineering, Massachusetts Institute of Technology, Cambridge, Massachusetts.

While the study of unconstrained movements has revealed important features of neural control, generalizing those insights to more sophisticated object manipulation is challenging. Humans excel at physical interaction with objects, even when those objects introduce complex dynamics and kinematic constraints. This study examined humans turning a horizontal planar crank (radius 10.29 cm) at their preferred and three instructed speeds (with visual feedback), both in clockwise and counterclockwise directions. To explore the role of neuromechanical dynamics, the instructed speeds covered a wide range: fast (near the limits of performance), medium (near preferred speed), and very slow (rendering dynamic effects negligible). Because kinematically constrained movements involve significant physical interaction, disentangling neural control from the influences of biomechanics presents a challenge. To address it, we modeled the interactive dynamics to "subtract off" peripheral biomechanics from observed force and kinematic data, thereby estimating aspects of underlying neural action that may be expressed in terms of motion. We demonstrate the value of this method: remarkably, an approximately elliptical path emerged, and speed minima coincided with curvature maxima, similar to what is seen in unconstrained movements, even though the hand moved at nearly constant speed along a constant-curvature path. These findings suggest that the neural controller takes advantage of peripheral biomechanics to simplify physical interaction. As a result, patterns seen in unconstrained movements persist even when physical interaction prevents their expression in hand kinematics. The reemergence of a speed-curvature relation indicates that it is due, at least in part, to neural processes that emphasize smoothness and predictability. Physically interacting with kinematic constraints is commonplace in everyday actions. We report a study of humans turning a crank, a circular constraint that imposes constant hand path curvature and hence should suppress variations of hand speed due to the power-law speed-curvature relation widely reported for unconstrained motions. Remarkably, we found that, when peripheral biomechanical factors are removed, a speed-curvature relation reemerges, indicating that it is, at least in part, of neural origin.
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http://dx.doi.org/10.1152/jn.00536.2019DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7444923PMC
May 2020

Learning and transfer of complex motor skills in virtual reality: a perspective review.

J Neuroeng Rehabil 2019 10 18;16(1):121. Epub 2019 Oct 18.

Biology, Electrical and Computer Engineering, and Physics, Northeastern University, 503 Richards Hall, 360 Huntington Avenue, Boston, MA, 02118, USA.

The development of more effective rehabilitative interventions requires a better understanding of how humans learn and transfer motor skills in real-world contexts. Presently, clinicians design interventions to promote skill learning by relying on evidence from experimental paradigms involving simple tasks, such as reaching for a target. While these tasks facilitate stringent hypothesis testing in laboratory settings, the results may not shed light on performance of more complex real-world skills. In this perspective, we argue that virtual environments (VEs) are flexible, novel platforms to evaluate learning and transfer of complex skills without sacrificing experimental control. Specifically, VEs use models of real-life tasks that afford controlled experimental manipulations to measure and guide behavior with a precision that exceeds the capabilities of physical environments. This paper reviews recent insights from VE paradigms on motor learning into two pressing challenges in rehabilitation research: 1) Which training strategies in VEs promote complex skill learning? and 2) How can transfer of learning from virtual to real environments be enhanced? Defining complex skills by having nested redundancies, we outline findings on the role of movement variability in complex skill acquisition and discuss how VEs can provide novel forms of guidance to enhance learning. We review the evidence for skill transfer from virtual to real environments in typically developing and neurologically-impaired populations with a view to understanding how differences in sensory-motor information may influence learning strategies. We provide actionable suggestions for practicing clinicians and outline broad areas where more research is required. Finally, we conclude that VEs present distinctive experimental platforms to understand complex skill learning that should enable transfer from therapeutic practice to the real world.
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http://dx.doi.org/10.1186/s12984-019-0587-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6798491PMC
October 2019

Gender Differences in Throwing Revisited: Sensorimotor Coordination in a Virtual Ball Aiming Task.

Front Hum Neurosci 2019 18;13:231. Epub 2019 Jul 18.

Department of Physics, Northeastern University, Boston, MA, United States.

Numerous studies have demonstrated that boys throw balls faster, farther and more accurately than girls. This may be largely due to well-known anatomical and muscle-physiological differences that play a central role in overarm throwing. With the objective to understand the potential contribution of the equally essential coordinative aspects in throwing for this gender difference, this large cross-sectional study examined a simplified forearm throw that eliminated the requirements that give males an advantage.While the overall performance error indeed became similar in the age groups younger than 20 years and older than 50 years, it was attenuated for middle-aged individuals. The gender differences remained in individuals who reported no throwing experience, but females with throwing experience reached similar performance as males. Two fine-grained spatiotemporal metrics displayed similar age-dependent gender disparities: while overall, males showed better spatiotemporal coordination of the ball release, age group comparisons specified that it was particularly middle-aged females that made more timing errors and did not develop a noise-tolerant strategy as males did. As throwing experience did not explain this age-dependency, the results are discussed in the context of spatial abilities and video game experience, both more pronounced in males. In contrast, a measure of rhythmicity developed over successive throws only revealed weak gender differences, speaking to the fundamental tendency in humans to fall into rhythmic patterns. Only the youngest individuals between 5 and 9 years of age showed significantly less rhythmicity in their performance. This computational study was performed in a large cohort in the context of an outreach activity, demonstrating that robust quantitative measures can also be obtained in less controlled environments. The findings also alert that motor neuroscience may need to pay more attention to gender differences.
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http://dx.doi.org/10.3389/fnhum.2019.00231DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6657012PMC
July 2019

Control of goal-directed movements within (or beyond) reach?: Comment on "Muscleless motor synergies and actions without movements: From motor neuroscience to cognitive robotics" by Vishwanathan Mohan et al.

Phys Life Rev 2019 10 27;30:126-129. Epub 2019 Mar 27.

Departments of Mechanical Engineering and Brain and Cognitive Sciences, Massachusetts Institute of Technology, United States of America. Electronic address:

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http://dx.doi.org/10.1016/j.plrev.2019.03.016DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7362311PMC
October 2019

The primacy of rhythm: how discrete actions merge into a stable rhythmic pattern.

J Neurophysiol 2019 02 19;121(2):574-587. Epub 2018 Dec 19.

Department of Biology, Electrical and Computer Engineering, and Physics, Northeastern University , Boston, Massachusetts.

This study examined how humans spontaneously merge a sequence of discrete actions into a rhythmic pattern, even when periodicity is not required. Two experiments used a virtual throwing task, in which subjects performed a long sequence of discrete throwing movements, aiming to hit a virtual target. In experiment 1, subjects performed the task for 11 sessions. Although there was no instruction to perform rhythmically, the variability of the interthrow intervals decreased to a level comparable to that of synchronizing with a metronome; furthermore, dwell times shortened or even disappeared with practice. Floquet multipliers and decreasing variability of the arm trajectories estimated in state space indicated an increasing degree of dynamic stability. Subjects who achieved a higher level of periodicity and stability also displayed higher accuracy in the throwing task. To directly test whether rhythmicity affected performance, experiment 2 disrupted the evolving continuity and periodicity by enforcing a pause between successive throws. This discrete group performed significantly worse and with higher variability in their arm trajectories than the self-paced group. These findings are discussed in the context of previous neuroimaging results showing that rhythmic movements involve significantly fewer cortical and subcortical activations than discrete movements and therefore may pose a computationally more parsimonious solution. Such emerging stable rhythms in neuromotor subsystems may serve as building blocks or dynamic primitives for complex actions. The tendency for humans to spontaneously fall into a rhythm in voluntary movements is consistent with the ubiquity of rhythms at all levels of the physiological system. NEW & NOTEWORTHY When performing a series of throws to hit a target, humans spontaneously merged successive actions into a continuous approximately periodic pattern. The degree of rhythmicity and stability correlated with hitting accuracy. Enforcing irregular pauses between throws to disrupt the rhythm deteriorated performance. Stable rhythmic patterns may simplify control of movement and serve as dynamic primitives for more complex actions. This observation reveals that biological systems tend to exhibit rhythmic behavior consistent with a plethora of physiological processes.
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http://dx.doi.org/10.1152/jn.00587.2018DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6397394PMC
February 2019

Stability and predictability in human control of complex objects.

Chaos 2018 Oct;28(10):103103

Department of Biology, Northeastern University, Boston, Massachusetts 02115, USA.

Previous research on movement control suggested that humans exploit stability to reduce vulnerability to internal noise and external perturbations. For interactions with complex objects, predictive control based on an internal model of body and environment is needed to preempt perturbations and instabilities due to delays. We hypothesize that stability can serve as means to render the complex dynamics of the body and the task more predictable and thereby simplify control. However, the assessment of stability in complex interactions with nonlinear and underactuated objects is challenging, as for existent stability analyses the system needs to be close to a (known) attractor. After reviewing existing methods for stability analysis of human movement, we argue that contraction theory provides a suitable approach to quantify stability or convergence in complex transient behaviors. To test its usefulness, we examined the task of carrying a cup of coffee, an object with internal degrees of freedom. A simplified model of the task, a cart with a suspended pendulum, was implemented in a virtual environment to study human control strategies. The experimental task was to transport this cart-and-pendulum on a horizontal line from rest to a target position as fast as possible. Each block of trials presented a visible perturbation, which either could be in the direction of motion or opposite to it. To test the hypothesis that humans exploit stability to overcome perturbations, the dynamic model of the free, unforced system was analyzed using contraction theory. A contraction metric was obtained by numerically solving a partial differential equation, and the contraction regions with respect to that metric were computed. Experimental results showed that subjects indeed moved through the contraction regions of the free, unforced system. This strategy attenuated the perturbations, obviated error corrections, and made the dynamics more predictable. The advantages and shortcomings of contraction analysis are discussed in the context of other stability analyses.
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http://dx.doi.org/10.1063/1.5042090DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6170195PMC
October 2018

Quantifying Movement in Preterm Infants Using Photoplethysmography.

Ann Biomed Eng 2019 Feb 25;47(2):646-658. Epub 2018 Sep 25.

Department of Neurology, Dell Medical School, and Institute for Computational Engineering and Sciences, The University of Texas, 1701 Trinity St. Stop Z0700, Health Discovery Bldg, 5.708A, Austin, TX, 78712, USA.

Long-term recordings of movement in preterm infants might reveal important clinical information. However, measurement of movement is limited because of time-consuming and subjective analysis of video or reluctance to attach additional sensors to the infant. We evaluated whether photoplethysmogram (PPG), routinely used for oximetry in preterm infants in the neonatal intensive care unit (NICU), can provide reliable long-term measurements of movement. In 18 infants [mean post-conceptional age (PCA) 31.10 weeks, range 29-34.29 weeks], we designed and tested a wavelet-based algorithm that detects movement signals from the PPG. The algorithm's performance was optimized relative to subjective assessments of movement using video and accelerometers attached to two limbs and force sensors embedded within the mattress (five infants, three raters). We then applied the optimized algorithm to infants receiving routine care in the NICU without additional sensors. The algorithm revealed a decline in brief movements (< 5 s) with increasing PCA (13 infants, r = - 0.87, p < 0.001, PCA range 27.3-33.9 weeks). Our findings suggest that quantitative relationships between motor activity and clinical outcomes in preterm infants can be studied using routine photoplethysmography.
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http://dx.doi.org/10.1007/s10439-018-02135-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6344309PMC
February 2019

It's Not (Only) the Mean that Matters: Variability, Noise and Exploration in Skill Learning.

Authors:
Dagmar Sternad

Curr Opin Behav Sci 2018 Apr 1;20:183-195. Epub 2018 Mar 1.

Department of Biology, Electrical and Computer Engineering and Physics, Center for the Interdisciplinary Study of Complex Systems, Northeastern University, Boston, MA.

Mastering a motor skill is typified by a decrease in variability. However, variability is much more than the undesired signature of discoordination: structure in both its distributional properties and temporal sequence can reveal control priorities. Extending from the notion that signal-dependent noise corrupts information transmission in the neuromotor system, this review tracks more recent recognitions that the complex dynamic motor system in its interaction with task constraints creates high-dimensional spaces with multiple equivalent solutions. Further analysis differentiates these solutions to have different degrees of noise-sensitivity, goal-relevance or additional costs. Practice proceeds from exploration of these solution spaces to then exploitation with further channeling of noise. Extended practice leads to fine-tuning of skill brought about by reducing noise. These distinct changes in variability are suggested as a way to characterize stages of learning. Capitalizing on the sensitivity of the CNS to noise, interventions can add extrinsic or amplify intrinsic noise to guide (re-)learning desired behaviors. The persistence and generalization of acquired skill is still largely understudied, although an essential element of skill. Consistent with advances in the physical sciences, there is increasing realization that noise can have beneficial effects. Analysis of the non-random structure of variability may reveal more than analysis of only its mean.
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http://dx.doi.org/10.1016/j.cobeha.2018.01.004DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6051545PMC
April 2018

Velocity-curvature patterns limit human-robot physical interaction.

IEEE Robot Autom Lett 2018 Jan 9;3(1):249-256. Epub 2017 Aug 9.

Action Lab, the Departments of Biology, Electrical and Computer Engineering, and Physics, Northeastern University, Boston, MA 02115, USA.

Physical human-robot collaboration is becoming more common, both in industrial and service robotics. Cooperative execution of a task requires intuitive and efficient interaction between both actors. For humans, this means being able to predict and adapt to robot movements. Given that natural human movement exhibits several robust features, we examined whether human-robot physical interaction is facilitated when these features are considered in robot control. The present study investigated how humans adapt to biological and non-biological velocity patterns in robot movements. Participants held the end-effector of a robot that traced an elliptic path with either biological (two-thirds power law) or non-biological velocity profiles. Participants were instructed to minimize the force applied on the robot end-effector. Results showed that the applied force was significantly lower when the robot moved with a biological velocity pattern. With extensive practice and enhanced feedback, participants were able to decrease their force when following a non-biological velocity pattern, but never reached forces below those obtained with the 2/3 power law profile. These results suggest that some robust features observed in natural human movements are also a strong preference in guided movements. Therefore, such features should be considered in human-robot physical collaboration.
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http://dx.doi.org/10.1109/LRA.2017.2737048DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5937985PMC
January 2018

Stability and Predictability in Dynamically Complex Physical Interactions.

IEEE Int Conf Robot Autom 2018 May 13;2018:5540-5545. Epub 2018 Sep 13.

Department of Biology, Department of Electrical and Computer Engineering, Northeastern University, Boston, Massachusetts 02115.

This study examines human control of physical interaction with objects that exhibit complex (nonlinear, chaotic, underactuated) dynamics. We hypothesized that humans exploited stability properties of the human-object interaction. Using a simplified 2D model for carrying a "cup of coffee", we developed a virtual implementation to identify human control strategies. Transporting a cup of coffee was modeled as a cart with a suspended pendulum, where humans moved the cart on a horizontal line via a robotic manipulandum. The specific task was to transport the cart-pendulum system to a target, as fast as possible, while accommodating assistive and resistive perturbations. To assess trajectory stability, we applied contraction analysis. We showed that when the perturbation was assistive, humans absorbed the perturbation by controlling cart trajectories into a contraction region prior to the perturbation. When the perturbation was resistive, subjects passed through a contraction region following the perturbation. Entering a contraction region stabilizes performance and makes the dynamics more predictable. This human control strategy could inspire more robust control strategies for physical interaction in robots.
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http://dx.doi.org/10.1109/icra.2018.8460774DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7187481PMC
May 2018

Author Correction: Low-dimensional organization of angular momentum during walking on a narrow beam.

Sci Rep 2018 Apr 18;8(1):6362. Epub 2018 Apr 18.

Section for Computational Sensomotorics, Department of Cognitive Neurology, Hertie Institute for Clinical Brain Research, Centre for Integrative Neuroscience, University Clinic Tübingen, Tübingen, Germany.

A correction to this article has been published and is linked from the HTML and PDF versions of this paper. The error has been fixed in the paper.
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http://dx.doi.org/10.1038/s41598-018-24802-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5906439PMC
April 2018

Predictability, force, and (anti)resonance in complex object control.

J Neurophysiol 2018 08 18;120(2):765-780. Epub 2018 Apr 18.

Department of Biology, Northeastern University , Boston, Massachusetts.

Manipulation of complex objects as in tool use is ubiquitous and has given humans an evolutionary advantage. This study examined the strategies humans choose when manipulating an object with underactuated internal dynamics, such as a cup of coffee. The dynamics of the object renders the temporal evolution complex, possibly even chaotic, and difficult to predict. A cart-and-pendulum model, loosely mimicking coffee sloshing in a cup, was implemented in a virtual environment with a haptic interface. Participants rhythmically manipulated the virtual cup containing a rolling ball; they could choose the oscillation frequency, whereas the amplitude was prescribed. Three hypotheses were tested: 1) humans decrease interaction forces between hand and object; 2) humans increase the predictability of the object dynamics; and 3) humans exploit the resonances of the coupled object-hand system. Analysis revealed that humans chose either a high-frequency strategy with antiphase cup-and-ball movements or a low-frequency strategy with in-phase cup-and-ball movements. Counter to hypothesis 1, they did not decrease interaction force; instead, they increased the predictability of the interaction dynamics, quantified by mutual information, supporting hypothesis 2. To address hypothesis 3, frequency analysis of the coupled hand-object system revealed two resonance frequencies separated by an antiresonance frequency. The low-frequency strategy exploited one resonance, whereas the high-frequency strategy afforded more choice, consistent with the frequency response of the coupled system; both strategies avoided the antiresonance. Hence, humans did not prioritize small interaction forces but rather strategies that rendered interactions predictable. These findings highlight that physical interactions with complex objects pose control challenges not present in unconstrained movements. NEW & NOTEWORTHY Daily actions involve manipulation of complex nonrigid objects, which present a challenge since humans have no direct control of the whole object. We used a virtual-reality experiment and simulations of a cart-and-pendulum system coupled to hand movements with impedance to analyze the manipulation of this underactuated object. We showed that participants developed strategies that increased the predictability of the object behavior by exploiting the resonance structure of the object but did not minimize the hand-object interaction force.
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http://dx.doi.org/10.1152/jn.00918.2017DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6139444PMC
August 2018

Exploiting the geometry of the solution space to reduce sensitivity to neuromotor noise.

PLoS Comput Biol 2018 02 20;14(2):e1006013. Epub 2018 Feb 20.

Department of Physics, Northeastern University, Boston, Massachusetts, United States of America.

Throwing is a uniquely human skill that requires a high degree of coordination to successfully hit a target. Timing of ball release appears crucial as previous studies report required timing accuracies as short as 1-2ms, which however appear physiologically challenging. This study mathematically and experimentally demonstrates that humans can overcome these seemingly stringent timing requirements by shaping their hand trajectories to create extended timing windows, where ball releases achieve target hits despite temporal imprecision. Subjects practiced four task variations in a virtual environment, each with a distinct geometry of the solution space and different demands for timing. Model-based analyses of arm trajectories revealed that subjects first decreased timing error, followed by lengthening timing windows in their hand trajectories. This pattern was invariant across solution spaces, except for a control case. Hence, the exquisite skill that humans evolved for throwing is achieved by developing strategies that are less sensitive to temporal variability arising from neuromotor noise. This analysis also provides an explanation why coaches emphasize the "follow-through" in many ball sports.
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http://dx.doi.org/10.1371/journal.pcbi.1006013DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5834204PMC
February 2018

Low-dimensional organization of angular momentum during walking on a narrow beam.

Sci Rep 2018 01 8;8(1):95. Epub 2018 Jan 8.

Section for Computational Sensomotorics, Department of Cognitive Neurology, Hertie Institute for Clinical Brain Research, Centre for Integrative Neuroscience, University Clinic Tübingen, Tübingen, Germany.

Walking on a beam is a challenging motor skill that requires the regulation of upright balance and stability. The difficulty in beam walking results from the reduced base of support compared to that afforded by flat ground. One strategy to maintain stability and hence avoid falling off the beam is to rotate the limb segments to control the body's angular momentum. The aim of this study was to examine the coordination of the angular momentum variations during beam walking. We recorded movement kinematics of participants walking on a narrow beam and computed the angular momentum contributions of the body segments with respect to three different axes. Results showed that, despite considerable variability in the movement kinematics, the angular momentum was characterized by a low-dimensional organization based on a small number of segmental coordination patterns. When the angular momentum was computed with respect to the beam axis, the largest fraction of its variation was accounted for by the trunk segment. This simple organization was robust and invariant across all participants. These findings support the hypothesis that control strategies for complex balancing tasks might be easier to understand by investigating angular momentum instead of the segmental kinematics.
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http://dx.doi.org/10.1038/s41598-017-18142-yDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5758518PMC
January 2018
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