Abstract
We compared gait using the planar law of intersegmental coordination between 14 hemorrhagic stroke subjects walking at a self-selected normal speed (56 ± 21 cm/s) and 15 age-matched healthy controls walking at a very slow speed (56 ± 19 cm/s). Sagittal plane elevation angles of the thigh, shank, and foot segments were submitted to principal component analysis. Additional outcome measures included the range of elevation angle and timing of peak elevation angle of the thigh, shank, and foot segments. The range of elevation angles at the shank and foot was significantly smaller in the paretic leg than non-paretic and control legs. Also, the peak elevation angle at the thigh occurred significantly later in the gait cycle in the paretic than control leg. Gait of both stroke and control subjects followed the planar law with the first two principal components explaining approximately 99 % of the variance. However, the three-dimensional trajectory of elevation angles (gait loop) in stroke subjects deviated from the typical teardrop shape bilaterally, which was more exaggerated in the paretic leg. Compared to the non-paretic and control legs, the paretic leg showed significantly increased absolute loading of the thigh elevation angle and decreased absolute loadings of the shank and foot elevation angles on the first principal component, whereas the opposite was observed for the second principal component. Despite following the planar law, the gait of chronic stroke subjects is characterized by atypical timing of the thigh motion and disrupted intersegmental coordination of both legs.
Similar content being viewed by others
References
Allen JL, Kautz SA, Neptune RR (2011) Step length asymmetry is representative of compensatory mechanisms used in post-stroke hemiparetic walking. Gait Posture 33:538–543
Bianchi L, Angelini D, Lacquaniti F (1998) Individual characteristics of human walking mechanics. Pflugers Arch 436:343–356
Bleyenheuft C, Cockx S, Caty G, Stoquart G, Lejeune T, Detrembleur C (2009) The effect of botulinum toxin injections on gait control in spastic stroke patients presenting with a stiff-knee gait. Gait Posture 30:168–172
Bleyenheuft C, Deltombe T, Detrembleur C (2013) Influence of ankle-foot orthoses on kinematic segmental covariation among stroke patients. Ann Phys Rehabil Med 56:3–13
Borghese NA, Bianchi L, Lacquaniti F (1996) Kinematic determinants of human locomotion. J Physiol 494(Pt 3):863–879
Chau T (2001) A review of analytical techniques for gait data. Part 1: fuzzy, statistical and fractal methods. Gait Posture 13:49–66
Cheron G, Bouillot E, Dan B, Bengoetxea A, Draye JP, Lacquaniti F (2001) Development of a kinematic coordination pattern in toddler locomotion: planar covariation. Exp Brain Res 137:455–466
Chow JW, Yablon SA, Horn TS, Stokic DS (2010) Temporospatial characteristics of gait in patients with lower limb muscle hypertonia after traumatic brain injury. Brain Inj 24:1575–1584
Courtine G, Schieppati M (2003a) Human walking along a curved path. I. Body trajectory, segment orientation and the effect of vision. Eur J Neurosci 18:177–190
Courtine G, Schieppati M (2003b) Human walking along a curved path. II. Gait features and EMG patterns. Eur J Neurosci 18:191–205
Courtine G, Schieppati M (2004) Tuning of a basic coordination pattern constructs straight-ahead and curved walking in humans. J Neurophysiol 91:1524–1535
Dan B, Bouillot E, Bengoetxea A, Cheron G (2000) Effect of intrathecal baclofen on gait control in human hereditary spastic paraparesis. Neurosci Lett 280:175–178
De Wit L, Molas M, Dejaeger E, De Weerdt W, Feys H, Jenni W, Lincoln N, Putman K, Schupp W, Lesaffre E (2009) The use of a biplot in studying outcomes after stroke. Neurorehabil Neural Repair 23:825–830
Dominici N, Ivanenko YP, Cappellini G, Zampagni ML, Lacquaniti F (2010) Kinematic strategies in newly walking toddlers stepping over different support surfaces. J Neurophysiol 103:1673–1684
Grasso R, Bianchi L, Lacquaniti F (1998) Motor patterns for human gait: backward versus forward locomotion. J Neurophysiol 80:1868–1885
Grasso R, Peppe A, Stratta F, Angelini D, Zago M, Stanzione P, Lacquaniti F (1999) Basal ganglia and gait control: apomorphine administration and internal pallidum stimulation in Parkinson’s disease. Exp Brain Res 126:139–148
Grasso R, Zago M, Lacquaniti F (2000) Interactions between posture and locomotion: motor patterns in humans walking with bent posture versus erect posture. J Neurophysiol 83:288–300
Hicheur H, Terekhov AV, Berthoz A (2006) Intersegmental coordination during human locomotion: does planar covariation of elevation angles reflect central constraints? J Neurophysiol 96:1406–1419
Hyngstrom A, Onushko T, Chua M, Schmit BD (2010) Abnormal volitional hip torque phasing and hip impairments in gait post stroke. J Neurophysiol 103:1557–1568
Hyngstrom AS, Kuhnen HR, Kirking KM, Hunter SK (2014) Functional implications of impaired control of submaximal hip flexion following stroke. Muscle Nerve 49:225–232
Ivanenko YP, Grasso R, Macellari V, Lacquaniti F (2002) Control of foot trajectory in human locomotion: role of ground contact forces in simulated reduced gravity. J Neurophysiol 87:3070–3089
Ivanenko YP, d’Avella A, Poppele RE, Lacquaniti F (2008) On the origin of planar covariation of elevation angles during human locomotion. J Neurophysiol 99:1890–1898
Jonkers I, Delp S, Patten C (2009) Capacity to increase walking speed is limited by impaired hip and ankle power generation in lower functioning persons post-stroke. Gait Posture 29:129–137
Jonsdottir J, Recalcati M, Rabuffetti M, Casiraghi A, Boccardi S, Ferrarin M (2009) Functional resources to increase gait speed in people with stroke: strategies adopted compared to healthy controls. Gait Posture 29:355–359
Kadaba MP, Ramakrishnan HK, Wootten ME (1990) Measurement of lower extremity kinematics during level walking. J Orthop Res 8:383–392
Lacquaniti F, Grasso R, Zago M (1999) Motor Patterns in Walking. News Physiol Sci 14:168–174
Lacquaniti F, Ivanenko YP, Zago M (2002) Kinematic control of walking. Arch Ital Biol 140:263–272
Leung J, Moseley A (2003) Impact of ankle-foot orthoses on gait and leg muscle activity in adults with hemiplegia: systematic literature review. Physiotherapy 89:39–55
Maclellan MJ, McFadyen BJ (2010) Segmental control for adaptive locomotor adjustments during obstacle clearance in healthy young adults. Exp Brain Res 202:307–318
Maclellan MJ, Richards CL, Fung J, McFadyen BJ (2013) Use of segmental coordination analysis of nonparetic and paretic limbs during obstacle clearance in community-dwelling persons after stroke. PM R 5:381–391
Nadeau S, Gravel D, Arsenault AB, Bourbonnais D (1999) Plantarflexor weakness as a limiting factor of gait speed in stroke subjects and the compensating role of hip flexors. Clin Biomech (Bristol Avon) 14:125–135
Noble JW, Prentice SD (2008) Intersegmental coordination while walking up inclined surfaces: age and ramp angle effects. Exp Brain Res 189:249–255
Paolucci S, Antonucci G, Grasso MG et al (2003) Functional outcome of ischemic and hemorrhagic stroke patients after inpatient rehabilitation: a matched comparison. Stroke 34:2861–2865
Petersen NT, Butler JE, Marchand-Pauvert V, Fisher R, Ledebt A, Pyndt HS, Hansen NL, Nielsen JB (2001) Suppression of EMG activity by transcranial magnetic stimulation in human subjects during walking. J Physiol 537:651–656
Pijnappels M, Van Wezel BM, Colombo G, Dietz V, Duysens J (1998) Cortical facilitation of cutaneous reflexes in leg muscles during human gait. Brain Res 787:149–153
Raja B, Neptune RR, Kautz SA (2012) Coordination of the non-paretic leg during hemiparetic gait: expected and novel compensatory patterns. Clin Biomech (Bristol, Avon) 27:1023–1030
Sainani KL (2014) Introduction to principal components analysis. PM R 6:275–278
Tyson SF, Kent RM (2013) Effects of an ankle-foot orthosis on balance and walking after stroke: a systematic review and pooled meta-analysis. Arch Phys Med Rehabil 94:1377–1385
Zeni JA Jr, Richards JG, Higginson JS (2008) Two simple methods for determining gait events during treadmill and overground walking using kinematic data. Gait Posture 27:710–714
Acknowledgments
We are grateful to Mark Hemleben, Terry Horn, PhD, and L. Anthony Smith for their assistance and to Stuart A Yablon, MD, for recruiting some of the subjects for this study. This work was supported in part by the Wilson Research Foundation, Jackson, MS, USA.
Conflict of interest
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Chow, J.W., Stokic, D.S. Intersegmental coordination of gait after hemorrhagic stroke. Exp Brain Res 233, 125–135 (2015). https://doi.org/10.1007/s00221-014-4099-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-014-4099-2