journal article·2025-04-25Open access

Neurobiomechanical Characterization of Feedforward Phase of Gait Initiation in Chronic Stroke: A Linear and Non-Linear Approach

Marta Freitas, Pedro Fonseca, Leonel Alves, Liliana Pinho, Sandra Silva, Vânia Figueira, José Félix, Francisco Pinho, João Paulo Vilas-Boas, Augusta Silva

Applied Sciences· Volume 15· Issue 9

Abstract

Postural control arises from the complex interplay of stability, adaptability, and dynamic adjustments, which are disrupted post-stroke, emphasizing the importance of examining these mechanisms during functional tasks. This study aimed to analyze the complexity and variability of postural control in post-stroke individuals during the feedforward phase of gait initiation. A cross-sectional study analyzed 17 post-stroke individuals and 16 matched controls. Participants had a unilateral ischemic stroke in the chronic phase and could walk independently. Exclusions included cognitive impairments, recent surgery, and neurological/orthopedic conditions. Kinematic and kinetic data were collected during 10 self-initiated gait trials to analyze centre of pressure (CoP) dynamics and joint angles (−600 ms to +50 ms). A 12-camera motion capture system (Qualisys, Gothenburg, Sweden) recorded full-body kinematics using 72 reflective markers placed on anatomical landmarks of the lower limbs, pelvis, trunk, and upper limbs. Ground reaction forces were measured via force plates (Bertec, Columbus, OH, USA) to compute CoP variables. Linear (displacement, amplitude, and velocity) and non-linear (Lyapunov exponent—LyE and multiscale entropy—MSE) measures were applied to assess postural control complexity and variability. Mann–Whitney U tests were applied (p < 0.05). The stroke group showed greater CoP displacement (p < 0.05) and reduced velocity (p = 0.021). Non-linear analysis indicated lower LyE values and reduced complexity and adaptability in CoP position and amplitude across scales (p < 0.05). In the sagittal plane, the stroke group had higher displacement and amplitude in the head, trunk, pelvis, and limbs, with reduced LyE and MSE values (p < 0.05). Frontal plane findings showed increased displacement and amplitude in the head, trunk, and ankle, with reduced LyE and MSE (p < 0.05). In the transverse plane, exaggerated rotational patterns were observed with increased displacement and amplitude in the head, trunk, pelvis, and hip, alongside reduced LyE convergence and MSE complexity (p < 0.05). Stroke survivors exhibit increased linear variability, indicating instability, and reduced non-linear complexity, reflecting limited adaptability. These results highlight the need for rehabilitation strategies that address both stability and adaptability across time scales.
Source: crossref · Quality: baseline

Research context

OpenAlex topics: Stroke Rehabilitation and Recovery · Balance, Gait, and Falls Prevention · Motor Control and Adaptation

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

Affiliations

School of Health Sciences of Vale do Ave, Polytechnic and University Higher Education Cooperative, Rua José António Vidal, 81, 4760-409 Vila Nova de Famalicão, Portugal

H2M—Health and Human Movement Unit, Polytechnic University of Health, Cooperativa de Ensino Superior Politécnico e Universitário, CRL, 4760-409 Vila Nova de Famalicão, Portugal

Centre of Research Rehabilitation (CIR), Escola Superior de Saúde, Rua Dr. António Bernardino de Almeida 400, 4200-072 Porto, Portugal

Porto Biomechanics Laboratory (LABIOMEP), Faculty of Sports, University of Porto, 4200-450 Porto, Portugal

Centre for Research, Training, Innovation, and Intervention in Sport (CIFI2D), Faculty of Sport, University of Porto, 4200-450 Porto, Portugal

Department of Medical Sciences, University of Aveiro, 3810-193 Aveiro, Portugal

School of Health Sciences, University of Aveiro, 3810-193 Aveiro, Portugal

Funding

national funds through FCT under the project

References (100+)

Show source-provided references
1. Movement System Diagnoses for Balance Dysfunction: Recommendations From the Academy of Neurologic Physical Therapy’s Movement System Task Force10.1093/ptj/pzab153 ↗
2. Postural orientation and equilibrium: What do we need to know about neural control of balance to prevent falls?10.1093/ageing/afl077 ↗
3. Using the Systems Framework for Postural Control to Analyze the Components of Balance Evaluated in Standardized Balance Measures: A Scoping Review10.1016/j.apmr.2014.06.021 ↗
4. Shumway-Cook, A., and Woollacott, M.H. (2017). Motor Control: Translating Research Into Clinical Practice, Wolters Kluwer.
5. Defining a Bobath clinical framework—A modified e-Delphi study10.1080/09593985.2016.1228722 ↗
6. Human movement variability, nonlinear dynamics, and pathology: Is there a connection?10.1016/j.humov.2011.06.002 ↗
7. Learning New Feedforward Motor Commands Based on Feedback Responses10.1016/j.cub.2020.03.005 ↗
8. Farinelli, V., Bolzoni, F., Marchese, S.M., Esposti, R., and Cavallari, P. (2021). A Novel Viewpoint on the Anticipatory Postural Adjustments During Gait Initiation. Front. Hum. Neurosci., 15.10.3389/fnhum.2021.709780 ↗
9. Early postural adjustments in preparation to whole-body voluntary sway10.1016/j.jelekin.2011.11.005 ↗
10. Latash, M.L., and Zatsiorsky, V. (2015). Biomechanics and Motor Control: Defining Central Concepts, Human Kinetics.
11. Improvement of anticipatory postural adjustments for balance control: Effect of a single training session10.1016/j.jelekin.2014.11.002 ↗
12. Complexity of postural control in infants: Linear and nonlinear features revealed by principal component analysis
13. Movement variability and the use of nonlinear tools: Principles to guide physical therapist practice10.2522/ptj.20080130 ↗
14. Postural Dysfunction in Stroke Rehabilitation
15. Reliability of Two Methods for Identifying the Postural Phase of Gait Initiation in Healthy and Poststroke Subjects10.1123/jab.2014-0222 ↗
16. Sousa, A.S.P., Moreira, J., Silva, C., Mesquita, I., Silva, A., Macedo, R., and Santos, R. (2022). Postural control during turn on the light task assisted by functional electrical stimulation in post stroke subjects. Sci. Rep., 12.10.1038/s41598-022-10893-7 ↗
17. Postural instability years after stroke10.1016/j.jstrokecerebrovasdis.2020.105038 ↗
18. Hugues, A., Di Marco, J., Ribault, S., Ardaillon, H., Janiaud, P., Xue, Y., Zhu, J., Pires, J., Khademi, H., and Rubio, L. (2019). Limited evidence of physical therapy on balance after stroke: A systematic review and meta-analysis. PLoS ONE, 14.10.1371/journal.pone.0221700 ↗
19. Effects of Cognitive Task Training on Dynamic Balance and Gait of Patients with Stroke: A Preliminary Randomized Controlled Study10.12659/MSMBR.925264 ↗
20. Motor strategies of postural control after hemispheric stroke10.1016/j.neucli.2015.09.003 ↗
21. Cabanas-Valdés, R., Boix-Sala, L., Grau-Pellicer, M., Guzmán-Bernal, J.A., Caballero-Gómez, F.M., and Urrútia, G. (2021). The Effectiveness of Additional Core Stability Exercises in Improving Dynamic Sitting Balance, Gait and Functional Rehabilitation for Subacute Stroke Patients (CORE-Trial): Study Protocol for a Randomized Controlled Trial. Int. J. Environ. Res. Public Health, 18.10.21203/rs.3.rs-162002/v1 ↗
22. Effect of a visual dual task on postural stability-A comparative study using linear and nonlinear methods10.1002/hsr2.1437 ↗
23. Risk Factors Related to Falling in Patients after Stroke
24. Spontaneous Improvement in PosturalControl after Stroke: A LongitudinalProspective Study
25. Functional Balance and Postural Control Improvements in Patients with Stroke after Non-Invasive Brain Stimulation: A Meta-Analysis10.1016/j.apmr.2019.09.003 ↗
26. Association of trunk control with mobility performance and accelerometry-based gait characteristics in hemiparetic patients with subacute stroke10.1016/j.gaitpost.2015.11.011 ↗
27. Postural control of individuals with chronic stroke compared to healthy participants: Timed-Up-and-Go, Functional Reach Test and center of pressure movement10.23736/S1973-9087.17.04522-1 ↗
28. Vonesch, A., Duhot, C., Lelard, T., Léonard, G., Błażkiewicz, M., and Mouras, H. (2023). Non-Linear Measures of Postural Control in Response to Painful and Non-Painful Visual Stimuli. Entropy, 25.10.3390/e25111561 ↗
29. Hua, A., Wang, G., Bai, J., Hao, Z., Liu, J., Meng, J., and Wang, J. (2024). Nonlinear dynamics of postural control system under visual-vestibular habituation balance practice: Evidence from EEG, EMG and center of pressure signals. Front. Hum. Neurosci., 18.10.3389/fnhum.2024.1371648 ↗
30. Postural control strategies are revealed by the complexity of fractional components of COP10.1152/jn.00426.2021 ↗
31. Reliability of novel centre of pressure measures of quiet standing balance in people with chronic stroke10.1016/j.gaitpost.2023.03.021 ↗
32. Posture control, aging, and attention resources: Models and posture-analysis methods10.1016/j.neucli.2008.09.005 ↗
33. Comparing dynamical systems concepts and techniques for biomechanical analysis10.1016/j.jshs.2016.01.013 ↗
34. Non-linear tools and methodological concerns measuring human movement variability: An overview
35. Kędziorek, J., and Błażkiewicz, M. (2020). Nonlinear Measures to Evaluate Upright Postural Stability: A Systematic Review. Entropy, 22.10.3390/e22121357 ↗
36. Freitas, M., Pinho, F., Pinho, L., Silva, S., Figueira, V., Vilas-Boas, J.P., and Silva, A. (2024). Biomechanical Assessment Methods Used in Chronic Stroke: A Scoping Review of Non-Linear Approaches. Sensors, 24.10.3390/s24072338 ↗
37. Investigating the effects of visual biofeedback therapy on recovery of postural balance in stroke patients using a complexity measure10.1080/10749357.2015.1122311 ↗
38. Effects of cognitive load on the amount and temporal structure of postural sway variability in stroke survivors10.1007/s00221-017-5126-x ↗
39. Characteristic muscle activity patterns during gait initiation in the healthy younger and older adults10.1016/j.gaitpost.2015.09.014 ↗
40. Lelard, T., Doutrellot, P.-L., Temfemo, A., and Ahmaidi, S. (2017). Electromyographic Pattern during Gait Initiation Differentiates Yoga Practitioners among Physically Active Older Subjects. Front. Hum. Neurosci., 11.10.3389/fnhum.2017.00300 ↗
41. Balance control during gait initiation: State-of-the-art and research perspectives10.5312/wjo.v8.i11.815 ↗
42. Fettrow, T., Reimann, H., Grenet, D., Thompson, E., Crenshaw, J., Higginson, J., and Jeka, J. (2019). Interdependence of balance mechanisms during bipedal locomotion. PLoS ONE, 14.10.1101/658120 ↗
43. Kilby, M.C., Molenaar, P.C.M., and Newell, K.M. (2015). Models of Postural Control: Shared Variance in Joint and COM Motions. PLoS ONE, 10.10.1371/journal.pone.0126379 ↗
44. Integrating Motor Variability Evaluation Into Movement System Assessment10.1093/ptj/pzad075 ↗
45. Center-of-Pressure Parameters Used in the Assessment of Postural Control10.1123/jsr.11.1.51 ↗
46. Linear and non-linear analysis of lower limb joints angle variability during running at different speeds
47. Typical and atypical development of reaching and postural control in infancy10.1111/dmcn.12298 ↗
48. Adaptação à população portuguesa da tradução do Mini Mental State Examination
49. Novos valores Normativos do mini-mental state examination
50. Ankle antagonist coactivation in the double-support phase of walking: Stroke vs. healthy subjects10.3109/08990220.2015.1012492 ↗
51. Age and sex differences in normative gait patterns10.1016/j.gaitpost.2021.05.014 ↗
52. Guidelines for data processing and analysis of the International Physical Activity Questionnaire (IPAQ)
53. Outcomes in severe middle cerebral artery ischemic stroke10.1007/s12028-013-9838-x ↗
54. Interlimb coordination during the stance phase of gait in subjects with stroke10.1016/j.apmr.2013.06.032 ↗
55. Standardized measurement of sensorimotor recovery in stroke trials: Consensus-based core recommendations from the Stroke Recovery and Rehabilitation Roundtable10.1177/1747493017711813 ↗
56. Campaniço, H. (2016). Validade Simultânea do Questionário Internacional de Atividade Física Através da Medição Objetiva da Atividade Física por Actigrafia Proporcional. [Master's Thesis, Faculdade de Motricidade Humana, Universidade de Lisboa].
57. International Physical Activity Questionnaire: 12-Country Reliability and Validity10.1249/01.MSS.0000078924.61453.FB ↗
58. Costa, S.V. (2003). Adaptação e Validação Cultural e Linguística do Fugl-Meyer Assessment of Sensorimotor Recovery after Stroke. [Bachelor’s Thesis, Escola Superior de Tecnologia da Saúde de Coimbra].
59. Reliability of the Fugl-Meyer assessment of sensorimotor recovery following cerebrovascular accident10.1093/ptj/63.10.1606 ↗
60. Cutoff Score of the Lower-Extremity Motor Subscale of Fugl-Meyer Assessment in Chronic Stroke Survivors: A Cross-Sectional Study10.1016/j.apmr.2019.01.027 ↗
61. Freitas, M., Pinho, F., Cruz-Martins, N., Pinho, L., Silva, S., Figueira, V., Vilas-Boas, J.P., and Silva, A. (2024). European Portuguese version of the Mini-BESTest: A cross-cultural adaptation and psychometric measurements in individuals with sensorimotor impairments. Disabil. Rehabil., ahead of print, 1–11.10.1080/09638288.2024.2402085 ↗
62. Using psychometric techniques to improve the Balance Evaluation Systems Test: The mini-BESTest10.2340/16501977-0537 ↗
63. Position and orientation in space of bones during movement: Anatomical frame definition and determination10.1016/0268-0033(95)91394-T ↗
64. A new anatomically based protocol for gait analysis in children10.1016/j.gaitpost.2006.12.018 ↗
65. Koltermann, J.J., Floessel, P., Hammerschmidt, F., and Disch, A.C. (2023). The Influence of Anthropometric Variables and Filtering Frequency on Center of Pressure Data. Sensors, 23.10.3390/s23115105 ↗
66. Schroeder, S., Jaeger, S., Schwer, J., Seitz, A., Hamann, I., Werner, M., Thorwaechter, C., Santos, I., Wendler, T., and Nebel, D. (2022). Accuracy measurement of different marker based motion analysis systems for biomechanical applications: A round robin study. PLoS ONE, 17.10.1371/journal.pone.0271349 ↗
67. Interlimb Coordination during Double Support Phase of Gait in People with and without Stroke10.1080/00222895.2023.2282088 ↗
68. Gait initiation and partial body weight unloading for functional improvement in post-stroke individuals10.1016/j.gaitpost.2018.12.008 ↗
69. The Influence of a Cognitive Task on the Postural Phase of Gait Initiation in Parkinson’s Disease: An Electromyographic-Based Analysis10.1123/mc.2015-0032 ↗
70. Caderby, T., Yiou, E., Peyrot, N., de Viviés, X., Bonazzi, B., and Dalleau, G. (2017). Effects of Changing Body Weight Distribution on Mediolateral Stability Control during Gait Initiation. Front. Hum. Neurosci., 11.10.3389/fnhum.2017.00127 ↗
71. Atypical anticipatory postural adjustments during gait initiation among individuals with sub-acute stroke10.1016/j.gaitpost.2016.12.020 ↗
72. Osada, Y., Motojima, N., Kobayashi, Y., and Yamamoto, S. (2022). Differences in mediolateral dynamic stability during gait initiation according to whether the non-paretic or paretic leg is used as the leading limb. PLoS ONE, 17.10.1371/journal.pone.0267577 ↗
73. ISB recommendations on the reporting of intersegmental forces and moments during human motion analysis10.1016/j.jbiomech.2019.109533 ↗
74. Accuracy and Reliability of Onset Detection Algorithms in Gait Initiation for Healthy Controls and Participants With Parkinson’s Disease10.1123/jab.2018-0431 ↗
75. Multiscale entropy analysis of complex physiologic time series10.1103/PhysRevLett.89.068102 ↗
76. Multiscale entropy analysis of biological signals10.1103/PhysRevE.71.021906 ↗
77. Multiscale entropy: A tool for understanding the complexity of postural control10.1016/j.jshs.2016.01.018 ↗
78. PhysioBank, PhysioToolkit, and PhysioNet: Components of a new research resource for complex physiologic signals10.1161/01.CIR.101.23.e215 ↗
79. Physiological time-series analysis using approximate entropy and sample entropy10.1152/ajpheart.2000.278.6.H2039 ↗
80. Determining Lyapunov exponents from a time series10.1016/0167-2789(85)90011-9 ↗
81. Mademli, L., Mavridi, D., Bohm, S., Patikas, D.A., Santuz, A., and Arampatzis, A. (2021). Standing on unstable surface challenges postural control of tracking tasks and modulates neuromuscular adjustments specific to task complexity. Sci. Rep., 11.10.1038/s41598-021-84899-y ↗
82. Marouvo, J., Sousa, F., Fernandes, O., Castro, M.A., and Paszkiel, S. (2021). Gait Kinematics Analysis of Flatfoot Adults. Appl. Sci., 11.10.3390/app11157077 ↗
83. Extracting qualitative dynamics from experimental data10.1016/0167-2789(86)90031-X ↗
84. Matilla-García, M., Morales, I., Rodríguez, J.M., and Ruiz Marín, M. (2021). Selection of Embedding Dimension and Delay Time in Phase Space Reconstruction via Symbolic Dynamics. Entropy, 23.10.3390/e23020221 ↗
85. Vlachos, I., and Kugiumtzis, D. (2008). State Space Reconstruction for Multivariate Time Series Prediction. arXiv.10.1142/9789814271349_0043 ↗
86. Generalized Multiscale Entropy Analysis: Application to Quantifying the Complex Volatility of Human Heartbeat Time Series10.3390/e17031197 ↗
87. Marôco, J. (2018). Análise Estatística com o SPSS Statistics: 7ª Edição, ReportNumber, Lda.
88. Altered Anticipatory Postural Adjustments During Whole-Body Reaching in Subjects With Stroke10.1177/15459683241231528 ↗
89. Lundy-Ekman, L., and Weyer, A. (2022). Neuroscience: Fundamentals for Rehabilitation, Elsevier.
90. Functional Neuroanatomy for Posture and Gait Control10.14802/jmd.16062 ↗
91. Delafontaine, A., Vialleron, T., Hussein, T., Yiou, E., Honeine, J.-L., and Colnaghi, S. (2019). Anticipatory Postural Adjustments During Gait Initiation in Stroke Patients. Front. Neurol., 10.10.3389/fneur.2019.00352 ↗
92. Measurements of the centre of pressure of individual legs reveal new characteristics of reduced anticipatory postural adjustments during gait initiation in patients with post-stroke hemiplegia10.2340/16501977-2856 ↗
93. Gandolfi, M., Valè, N., Dimitrova, E., Zanolin, M.E., Mattiuz, N., Battistuzzi, E., Beccari, M., Geroin, C., Picelli, A., and Waldner, A. (2019). Robot-Assisted Stair Climbing Training on Postural Control and Sensory Integration Processes in Chronic Post-stroke Patients: A Randomized Controlled Clinical Trial. Front. Neurosci., 13.10.3389/fnins.2019.01143 ↗
94. Postural control during quiet standing and voluntary stepping response tasks in individuals post-stroke: A case-control study10.1080/10749357.2021.1943803 ↗
95. Static and dynamic visual cues in feed-forward postural control10.1007/s00221-012-3286-2 ↗
96. Increasing mediolateral standing sway is associated with increasing corticospinal excitability, and decreasing M1 inhibition and facilitation10.1016/j.gaitpost.2017.11.021 ↗
97. Dynamical structure of center-of-pressure trajectories in patients recovering from stroke10.1007/s00221-006-0441-7 ↗
98. Speed and Rhythm Affect Temporal Structure of Variability in Reaching Poststroke: A Pilot Study10.1080/00222895.2016.1219304 ↗
99. Stergiou, N. (2016). Nonlinear Analysis for Human Movement Variability, CRC Press.10.1201/b19571 ↗
100. Andreasen, S.C., Wright, T.R., Crenshaw, J.R., Reisman, D.S., and Knarr, B.A. (2020). Relationships of Linear and Non-linear Measurements of Post-stroke Walking Activity and Their Relationship to Weather. Front. Sports Act. Living, 2.10.3389/fspor.2020.551542 ↗