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      Separating Timing, Movement Conditions and Individual Differences in the Analysis of Human Movement

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          Abstract

          A central task in the analysis of human movement behavior is to determine systematic patterns and differences across experimental conditions, participants and repetitions. This is possible because human movement is highly regular, being constrained by invariance principles. Movement timing and movement path, in particular, are linked through scaling laws. Separating variations of movement timing from the spatial variations of movements is a well-known challenge that is addressed in current approaches only through forms of preprocessing that bias analysis. Here we propose a novel nonlinear mixed-effects model for analyzing temporally continuous signals that contain systematic effects in both timing and path. Identifiability issues of path relative to timing are overcome by using maximum likelihood estimation in which the most likely separation of space and time is chosen given the variation found in data. The model is applied to analyze experimental data of human arm movements in which participants move a hand-held object to a target location while avoiding an obstacle. The model is used to classify movement data according to participant. Comparison to alternative approaches establishes nonlinear mixed-effects models as viable alternatives to conventional analysis frameworks. The model is then combined with a novel factor-analysis model that estimates the low-dimensional subspace within which movements vary when the task demands vary. Our framework enables us to visualize different dimensions of movement variation and to test hypotheses about the effect of obstacle placement and height on the movement path. We demonstrate that the approach can be used to uncover new properties of human movement.

          Author Summary

          When you move a cup to a new location on a table, the movement of lifting, transporting, and setting down the cup appears to be completely automatic. Although the hand could take continuously many different paths and move on any temporal trajectory, real movements are highly regular and reproducible. From repetition to repetition movements vary, and the pattern of variance reflects movement conditions and movement timing. If another person performs the same task, the movement will be similar. When we look more closely, however, there are systematic individual differences. Some people will overcompensate when avoiding an obstacle and some people will systematically move slower than others. When we want to understand human movement, all these aspects are important. We want to know which parts of a movement are common across people and we want to quantify the different types of variability. Thus, the models we use to analyze movement data should contain all the mentioned effects. In this work, we developed a framework for statistical analysis of movement data that respects these structures of movements. We showed how this framework modeled the individual characteristics of participants better than other state-of-the-art modeling approaches. We combined the timing-and-path-separating model with a novel factor analysis model for analyzing the effect of obstacles on spatial movement paths. This combination allowed for an unprecedented ability to quantify and display different sources of variation in the data. We analyzed data from a designed experiment of arm movements under various obstacle avoidance conditions. Using the proposed statistical models, we documented three findings: a linearly amplified deviation in mean path related to increase in obstacle height; a consistent asymmetric pattern of variation along the movement path related to obstacle placement; and the existence of obstacle-distance invariant focal points where mean trajectories intersect in the frontal and vertical planes.

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          Nonlinear mixed effects models for repeated measures data.

          We propose a general, nonlinear mixed effects model for repeated measures data and define estimators for its parameters. The proposed estimators are a natural combination of least squares estimators for nonlinear fixed effects models and maximum likelihood (or restricted maximum likelihood) estimators for linear mixed effects models. We implement Newton-Raphson estimation using previously developed computational methods for nonlinear fixed effects models and for linear mixed effects models. Two examples are presented and the connections between this work and recent work on generalized linear mixed effects models are discussed.
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            The uncontrolled manifold concept: identifying control variables for a functional task.

            The degrees of freedom problem is often posed by asking which of the many possible degrees of freedom does the nervous system control? By implication, other degrees of freedom are not controlled. We give an operational meaning to "controlled" and "uncontrolled" and describe a method of analysis through which hypotheses about controlled and uncontrolled degrees of freedom can be tested. In this conception, control refers to stabilization, so that lack of control implies reduced stability. The method was used to analyze an experiment on the sit-to-stand transition. By testing different hypotheses about the controlled variables, we systematically approximated the structure of control in joint space. We found that, for the task of sit-to-stand, the position of the center of mass in the sagittal plane was controlled. The horizontal head position and the position of the hand were controlled less stably, while vertical head position appears to be no more controlled than joint motions.
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              Dynamic field theory of movement preparation.

              A theoretical framework for understanding movement preparation is proposed. Movement parameters are represented by activation fields, distributions of activation defined over metric spaces. The fields evolve under the influence of various sources of localized input, representing information about upcoming movements. Localized patterns of activation self-stabilize through cooperative and competitive interactions within the fields. The task environment is represented by a 2nd class of fields, which preshape the movement parameter representation. The model accounts for a sizable body of empirical findings on movement initiation (continuous and graded nature of movement preparation, dependence on the metrics of the task, stimulus uncertainty effect, stimulus-response compatibility effects, Simon effect, precuing paradigm, and others) and suggests new ways of exploring the structure of motor representations.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Comput Biol
                PLoS Comput. Biol
                plos
                ploscomp
                PLoS Computational Biology
                Public Library of Science (San Francisco, CA USA )
                1553-734X
                1553-7358
                September 2016
                22 September 2016
                : 12
                : 9
                : e1005092
                Affiliations
                [1 ]Department of Mathematical Sciences, University of Copenhagen, Copenhagen, Denmark
                [2 ]Institut für Neuroinformatik, Ruhr-Universität Bochum, Bochum, Germany
                [3 ]Department of Computer Science, University of Copenhagen, Copenhagen, Denmark
                Western University, CANADA
                Author notes

                The authors have declared that no competing interests exist.

                • Conceived and designed the experiments: BG GS.

                • Performed the experiments: BG.

                • Analyzed the data: LLR BG CI BM.

                • Wrote the paper: LLR BG GS CI BM.

                Author information
                http://orcid.org/0000-0001-7099-2314
                http://orcid.org/0000-0001-7793-9620
                Article
                PCOMPBIOL-D-16-00048
                10.1371/journal.pcbi.1005092
                5033575
                27657545
                3fc7fdb1-252a-43f6-ac40-aafc8ad5c5ea
                © 2016 Raket et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 13 January 2016
                : 29 July 2016
                Page count
                Figures: 14, Tables: 2, Pages: 27
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft;
                Award ID: FKZ 01GQ0951
                Award Recipient :
                The authors acknowledge support from the German Federal Ministry of Education and Research within the National Network Computational Neuroscience - Bernstein Fokus: "Learning behavioral models: From human experiment to technical assistance", grant FKZ 01GQ0951. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Earth Sciences
                Geography
                Human Geography
                Human Mobility
                Social Sciences
                Human Geography
                Human Mobility
                Biology and Life Sciences
                Anatomy
                Musculoskeletal System
                Medicine and Health Sciences
                Anatomy
                Musculoskeletal System
                Physical Sciences
                Mathematics
                Probability Theory
                Random Variables
                Covariance
                Research and Analysis Methods
                Mathematical and Statistical Techniques
                Statistical Methods
                Maximum Likelihood Estimation
                Physical Sciences
                Mathematics
                Statistics (Mathematics)
                Statistical Methods
                Maximum Likelihood Estimation
                Research and Analysis Methods
                Mathematical and Statistical Techniques
                Statistical Methods
                Factor Analysis
                Physical Sciences
                Mathematics
                Statistics (Mathematics)
                Statistical Methods
                Factor Analysis
                Physical Sciences
                Mathematics
                Statistics (Mathematics)
                Statistical Models
                Physical Sciences
                Physics
                Classical Mechanics
                Acceleration
                Physical Sciences
                Mathematics
                Applied Mathematics
                Algorithms
                Research and Analysis Methods
                Simulation and Modeling
                Algorithms
                Custom metadata
                Data files are available from the following repository: https://github.com/larslau/Bochum_movement_data.

                Quantitative & Systems biology
                Quantitative & Systems biology

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