A low-dimensional representation of arm movements and hand grip forces in post-stroke individuals

Christoph M Kanzler, Giuseppe Averta, Anne Schwarz, Jeremia P O Held, Roger Gassert, Antonio Bicchi, Marco Santello, Olivier Lambercy, Matteo Bianchi, Christoph M Kanzler, Giuseppe Averta, Anne Schwarz, Jeremia P O Held, Roger Gassert, Antonio Bicchi, Marco Santello, Olivier Lambercy, Matteo Bianchi

Abstract

Characterizing post-stroke impairments in the sensorimotor control of arm and hand is essential to better understand altered mechanisms of movement generation. Herein, we used a decomposition algorithm to characterize impairments in end-effector velocity and hand grip force data collected from an instrumented functional task in 83 healthy control and 27 chronic post-stroke individuals with mild-to-moderate impairments. According to kinematic and kinetic raw data, post-stroke individuals showed reduced functional performance during all task phases. After applying the decomposition algorithm, we observed that the behavioural data from healthy controls relies on a low-dimensional representation and demonstrated that this representation is mostly preserved post-stroke. Further, it emerged that reduced functional performance post-stroke correlates to an abnormal variance distribution of the behavioural representation, except when reducing hand grip forces. This suggests that the behavioural repertoire in these post-stroke individuals is mostly preserved, thereby pointing towards therapeutic strategies that optimize movement quality and the reduction of grip forces to improve performance of daily life activities post-stroke.

Conflict of interest statement

The authors declare no competing interests.

© 2022. The Author(s).

Figures

Figure 1
Figure 1
Overview of the approach to capture the control of arm movements and grip forces. Kinematic and kinetic time-series were collected in a control and post-stroke population using a technology-based assessment with a goal-directed functional task, the Virtual Peg Insertion Test (representative raw data in left panel). After a pre-processing and temporal segmentation (middle panel), functional Principal Component Analysis (fPCA) was applied. fPCA allows reconstructing the time-series with a set of low dimensional basis functions, named fPCs. These fPCs can have a subject-specific shape and explain certain variance of the input signal, which was compared between a representative control and post-stroke individual, indicating a similar shape of the fPCs and a different distribution of variance explained between the subjects (right panel). The control was male and 40 years old. The post-stroke individual presented a mild upper limb sensorimotor impairment according to the Fugl-Meyer assessment for the upper extremity (score 55, age 52 years, male).
Figure 2
Figure 2
Movement and hand grip force coordination during the transport phase of the functional task. The preprocessed end-effector velocity (A) and grip force rate (C) signals were visualized for the paretic side of post-stroke subjects (red) and a healthy age-matched control population (gray). In addition, the shapes of the fPCs for the velocity (B) and the force rate (D) signals were visualized. The time-series of the stroke and control population were compared using statistical parametric mapping and the p- and t-values of significant periods annotated.
Figure 3
Figure 3
Grip force coordination during the force buildup and the force release phases of the functional task. The preprocessed end-effector grip force rate signals during buildup (A) and release (C) phases were visualized for the paretic side of post-stroke subjects (red) and a healthy age-matched control population (gray). In addition, the shapes of the fPCs for the buildup (B) and the release (D) signals were visualized. The time-series of the stroke and control population were compared using statistical parametric mapping and the P- and t-values of significant periods annotated.
Figure 4
Figure 4
Number of fPCs required to explain 90% of the variance in the input signal. This information was provided for each task phase and modality (end-effector velocity and grip force rate), visualized for the paretic side of post-stroke subjects (dark red), the non-paretic side of post-stroke subjects (light red), the dominant arm of the healthy age-matched control population (light gray) and the non-dominant arm of the healthy age-matched control population (dark gray). Horizontal black line indicates median, boxes represent the IQR, and the whiskers the min and max value within 1.5IQR. Horizontal solid line on top indicates results from an omnibus test and dashed lines from post-hoc tests. *Indicates P < 0.05, **P < 0.001.
Figure 5
Figure 5
Population-level comparison of variance explained per fPC, task phase, and modality. Horizontal solid line indicates results from an omnibus test and dashed lines from post-hoc tests. *Indicates P < 0.05, **P < 0.001.

References

    1. Lawrence ES, et al. Estimates of the prevalence of acute stroke impairments and disability in a multiethnic population. Stroke. 2001;32:1279–1284. doi: 10.1161/01.STR.32.6.1279.
    1. Burridge J, et al. A systematic review of international clinical guidelines for rehabilitation of people with neurological conditions: What recommendations are made for upper limb assessment? Front. Neurol. 2019;10:1–14. doi: 10.3389/fneur.2019.00567.
    1. Gladstone DJ, Danells CJ, Black SE. The fugl-meyer assessment of motor recovery after stroke: A critical review of its measurement properties. Neurorehabil. Neural Repair. 2002;16:232–240. doi: 10.1177/154596802401105171.
    1. Lang CE, Wagner JM, Dromerick AW, Edwards DF. Measurement of upper-extremity function early after stroke: Properties of the action research arm test. Arch. Phys. Med. Rehabil. 2006;87:1605–1610. doi: 10.1016/j.apmr.2006.09.003.
    1. Kwakkel G, et al. Standardized measurement of sensorimotor recovery in stroke trials: Consensus-based core recommendations from the stroke recovery and rehabilitation roundtable. Neurorehabil. Neural Repair. 2017;31:784–792. doi: 10.1177/1545968317732662.
    1. Schwarz A, Kanzler CM, Lambercy O, Luft AR, Veerbeek JM. Systematic review on kinematic assessments of upper limb movements after stroke. Stroke. 2019;50:718–727. doi: 10.1161/STROKEAHA.118.023531.
    1. Scott SH, Dukelow SP. Potential of robots as next-generation technology for clinical assessment of neurological disorders and upper-limb therapy. J. Rehabil. Res. Dev. 2011;48:335. doi: 10.1682/JRRD.2010.04.0057.
    1. Gassert R, Dietz V. Rehabilitation robots for the treatment of sensorimotor deficits: A neurophysiological perspective. J. Neuroeng. Rehabil. 2018;15:1–15. doi: 10.1186/s12984-018-0383-x.
    1. Panarese A, et al. Model-based variables for the kinematic assessment of upper-extremity impairments in post-stroke patients. J. Neuroeng. Rehabil. 2016;13:81. doi: 10.1186/s12984-016-0187-9.
    1. Ellis MD, Lan Y, Yao J, Dewald JPAA. Robotic quantification of upper extremity loss of independent joint control or flexion synergy in individuals with hemiparetic stroke: A review of paradigms addressing the effects of shoulder abduction loading. J. Neuroeng. Rehabil. 2016;13:95. doi: 10.1186/s12984-016-0203-0.
    1. Balasubramanian S, Melendez-Calderon A, Roby-Brami A, Burdet E. On the analysis of movement smoothness. J. Neuroeng. Rehabil. 2015;12:112. doi: 10.1186/s12984-015-0090-9.
    1. Kanzler CM, et al. A data-driven framework for selecting and validating digital health metrics: Use-case in neurological sensorimotor impairments. NPJ Digit. Med. 2020;3:80. doi: 10.1038/s41746-020-0286-7.
    1. Tresch MC, Cheung VCK, d’Avella A. Matrix factorization algorithms for the identification of muscle synergies: Evaluation on simulated and experimental data sets. J. Neurophysiol. 2006;2:1789.
    1. Vinjamuri R, Patel V, Powell M, Mao ZH, Crone N. Candidates for synergies: Linear Discriminants versus principal components. Comput. Intell. Neurosci. 2014;2014:14489. doi: 10.1155/2014/373957.
    1. Averta G, et al. Unvealing the principal modes of human upper limb movements through functional analysis. Front. Robot. AI. 2017;4:1–12. doi: 10.3389/frobt.2017.00037.
    1. Schwarz, A. et al. A functional analysis-based approach to quantify upper limb impairment level in chronic stroke patients: A pilot study. In Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC) 1–7 (2019).
    1. Cheung VCK, et al. Stability of muscle synergies for voluntary actions after cortical stroke in humans. Proc. Natl. Acad. Sci. U. S. A. 2009;106:19563–19568. doi: 10.1073/pnas.0910114106.
    1. Cheung VCK, et al. Muscle synergy patterns as physiological markers of motor cortical damage. Proc. Natl. Acad. Sci. 2012;109:14652–14656. doi: 10.1073/pnas.1212056109.
    1. Santello M, Lang CE. Are movement disorders and sensorimotor injuries pathologic synergies? When normal multi-joint movement synergies become pathologic. Front. Hum. Neurosci. 2015;8:1–13. doi: 10.3389/fnhum.2014.01050.
    1. Irastorza-Landa N, García-Cossio E, Sarasola-Sanz A, Broetz D, Ramos-Murguialday A. Functional synergy recruitment index as a reliable biomarker of motor function and recovery in chronic stroke patients. J. Neural Eng. 2021 doi: 10.1088/1741-2552/abe244.
    1. Lindberg PG, et al. Affected and unaffected quantitative aspects of grip force control in hemiparetic patients after stroke. Brain Res. 2012;1452:96–107. doi: 10.1016/j.brainres.2012.03.007.
    1. Hermsdörfer J, Hagl E, Nowak DA, Marquardt C. Grip force control during object manipulation in cerebral stroke. Clin. Neurophysiol. 2003;114:915–929. doi: 10.1016/S1388-2457(03)00042-7.
    1. Allgöwer K, Hermsdörfer J. Fine motor skills predict performance in the Jebsen Taylor Hand Function Test after stroke. Clin. Neurophysiol. 2017;128:1858–1871. doi: 10.1016/j.clinph.2017.07.408.
    1. Toledo SF, Yamanaka J, Friedman J, Feldman AG, Levin MF. Referent control of anticipatory grip force during reaching in stroke : An experimental and modeling study. Exp. Brain Res. 2019;237:1655–1672. doi: 10.1007/s00221-019-05498-y.
    1. Mason CR, Gomez JE, Ebner TJ. Hand synergies during reach-to-grasp. J. Neurophysiol. 2001;86:2896–2910. doi: 10.1152/jn.2001.86.6.2896.
    1. Santello M, Flanders M, Soechting JF. Patterns of hand motion during grasping and the influence of sensory guidance. J. Neurosci. 2002;22:1426–1435. doi: 10.1523/JNEUROSCI.22-04-01426.2002.
    1. Fluet, M., Lambercy, O. & Gassert, R. Upper limb assessment using a Virtual Peg Insertion Test. in 2011 IEEE International Conference on Rehabilitation Robotics 1–6 (IEEE, 2011). 10.1109/ICORR.2011.5975348.
    1. Kanzler CM, et al. Technology-aided assessment of functionally relevant sensorimotor impairments in arm and hand of post-stroke individuals. J. Neuroeng. Rehabil. 2020;17:128. doi: 10.1186/s12984-020-00748-5.
    1. Scott SH. Optimal feedback control and the neural basis of volitional motor control. Nat. Rev. Neurosci. 2004;5:532–546. doi: 10.1038/nrn1427.
    1. Rohrer B, et al. Submovements grow larger, fewer, and more blended during stroke recovery. Mot. Control. 2004;8:472–483. doi: 10.1123/mcj.8.4.472.
    1. Rohrer B, et al. Movement smoothness changes during stroke recovery. J. Neurosci. Off. J. Soc. Neurosci. 2002;22:8297–8304. doi: 10.1523/JNEUROSCI.22-18-08297.2002.
    1. Hussain N, Sunnerhagen K, Alt MM. Recovery of arm function during acute to chronic stage of sactroke quantified by kinematics. J. Rehabil. Med. 2021 doi: 10.2340/16501977-2813.
    1. Saes M, et al. Smoothness metric during reach-to-grasp after stroke: Part 2. Longitudinal association with motor impairment. J. Neuroeng. Rehabil. 2021;18:1–10. doi: 10.1186/s12984-021-00937-w.
    1. Sathian K, et al. Neurological principles and rehabilitation of action disorders: Common clinical deficits. Neurorehabil. Neural Repair. 2011;25:21S–32S. doi: 10.1177/1545968311410941.
    1. Flanagan JR, Wing A. Modulation of grip force with load force during point-to-point arm movements. Exp. Brain Res. 1993;95:301–324. doi: 10.1007/BF00229662.
    1. Forssberg H, et al. Development of human precision grip I: Basic coordination of force. Exp. Brain Res. 1992;90:393–398. doi: 10.1007/BF00227253.
    1. Flanagan JR, Tresilian JR. Grip-load force coupling: A general control strategy for transporting objects. J. Exp. Psychol. Hum. Percept. Perform. 1994;20:944–957. doi: 10.1037/0096-1523.20.5.944.
    1. Semrau JA, Herter TM, Scott SH, Dukelow SP. Examining differences in patterns of sensory and motor recovery after stroke with robotics. Stroke. 2015;46:3459–3469. doi: 10.1161/STROKEAHA.115.010750.
    1. Seo NJ, Rymer WZ, Kamper DG. Delays in grip initiation and termination in persons with stroke: Effects of arm support and active muscle stretch exercise. J. Neurophysiol. 2009;101:3108–3115. doi: 10.1152/jn.91108.2008.
    1. Kamper DG, Rymer WZ. Impairment of voluntary control of finger motion following stroke: Role of inappropriate muscle coactivation. Muscle Nerve. 2001;24:673–681. doi: 10.1002/mus.1054.
    1. Kamper DG, Harvey RL, Suresh S, Rymer WZ. Relative contributions of neural mechanisms versus muscle mechanics in promoting finger extension deficits following stroke. Muscle Nerve. 2003;28:309–318. doi: 10.1002/mus.10443.
    1. Dewald JPA, Beer RF. Abnormal joint torque patterns in the paretic upper limb of subjects with hemiparesis. Muscle Nerve. 2001;24:273–283. doi: 10.1002/1097-4598(200102)24:2<273::AID-MUS130>;2-Z.
    1. de Rugy A, Loeb GE, Carroll TJ. Are muscle synergies useful for neural control? Front. Comput. Neurosci. 2013;7:1–13.
    1. Krakauer JW, Carmichael ST. Broken Movement: The Neurobiology of Motor Recovery after Stroke. MIT Press; 2017.
    1. Wolf SL, et al. Effect of constraint-induced movement therapy on upper extremity function 3 to 9 months after stroke. JAMA. 2006;296:2095. doi: 10.1001/jama.296.17.2095.
    1. Ward NS, Brander F, Kelly K. Intensive upper limb neurorehabilitation in chronic stroke: Outcomes from the Queen Square programme. J. Neurol. Neurosurg. Psychiatry. 2019;90:498–506. doi: 10.1136/jnnp-2018-319954.
    1. Franklin DW, Wolpert DM. Review computational mechanisms of sensorimotor control. Neuron. 2011;72:425–442. doi: 10.1016/j.neuron.2011.10.006.
    1. Langhammer B, Stanghelle JK. Can physiotherapy after stroke based on the bobath concept result in improved quality of movement compared to the motor relearning programme. Physiother. Res. Int. 2011;16:69–80. doi: 10.1002/pri.474.
    1. Kwakkel G, et al. Standardized measurement of quality of upper limb movement after stroke: Consensus-based core recommendations from the second stroke recovery and rehabilitation roundtable. Int. J. Stroke. 2019;14:783–791. doi: 10.1177/1747493019873519.
    1. Mccabe J, Monkiewicz M, Holcomb J, Pundik S, Daly JJ. Comparison of robotics, functional electrical stimulation, and motor learning methods for treatment of persistent upper extremity dysfunction after stroke: A randomized controlled trial. Arch. Phys. Med. Rehabil. 2015;96:981–990. doi: 10.1016/j.apmr.2014.10.022.
    1. Levin MF, Liebermann DG, Parmet Y, Berman S. Compensatory versus noncompensatory shoulder movements used for reaching in stroke. Neurorehabil. Neural Repair. 2016;30:635–646. doi: 10.1177/1545968315613863.
    1. Gagnon C, et al. The virtual peg insertion test as an assessment of upper limb coordination in ARSACS patients: A pilot study. J. Neurol. Sci. 2014;347:341–344. doi: 10.1016/j.jns.2014.09.032.
    1. Lambercy, O. et al. Assessment of upper limb motor function in patients with multiple sclerosis using the Virtual Peg Insertion Test: A pilot study. In 2013 IEEE 13th International Conference on Rehabilitation Robotics (ICORR) 1–6 (IEEE, 2013). 10.1109/ICORR.2013.6650494.
    1. Ramsay J, Silverman BW. Functional Data Analysis. Springer; 2005.
    1. Averta G, et al. U-Limb: A multi-modal, multi-center database on arm motion control in healthy and post-stroke conditions. Gigascience. 2021;10:1–17. doi: 10.1093/gigascience/giab043.
    1. Pataky TC, Robinson MA, Vanrenterghem J. Vector field statistical analysis of kinematic and force trajectories. J. Biomech. 2013;46:2394–2401. doi: 10.1016/j.jbiomech.2013.07.031.

Source: PubMed

3
Subscribe