Immature Spinal Locomotor Output in Children with Cerebral Palsy

Germana Cappellini1, Yuri P. Ivanenko2, Giovanni Martino1, Michael J. MacLellan3, Angela Sacco4, Daniela Morelli4, Francesco Lacquaniti1,5,2
1Centre of Space Bio-medicine, University of Rome Tor Vergata, Rome, Italy
2Laboratory of Neuromotor Physiology, Istituti di Ricovero e Cura a Carattere Scientifico (IRCCS) Santa Lucia Foundation, Rome, Italy
3School of Kinesiology, Louisiana State University, Baton Rouge, LA, USA
4Department of Pediatric Neurorehabilitation, Istituti di Ricovero e Cura a Carattere Scientifico (IRCCS) Santa Lucia Foundation, Rome, Italy
5Department of Systems Medicine, “University of Rome Tor Vergata”, Rome, Italy

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Achache, 2010, Transmission within several spinal pathways in adults with cerebral palsy, Brain, 133, 1470, 10.1093/brain/awq053

Adolph, 2003, What changes in infant walking and why, Child Dev., 74, 475, 10.1111/1467-8624.7402011

Barliya, 2009, An analytical formulation of the law of intersegmental coordination during human locomotion, Exp. Brain Res., 193, 371, 10.1007/s00221-008-1633-0

Batschelet, 1981, Circular Statistics in Biology

Bax, 2005, Proposed definition and classification of cerebral palsy, April 2005, Dev. Med. Child Neurol., 47, 571, 10.1017/S001216220500112X

Beloozerova, 1993, The role of the motor cortex in the control of accuracy of locomotor movements in the cat, J. Physiol. (Lond.), 461, 1, 10.1113/jphysiol.1993.sp019498

Berger, 2007, Learning and development in infant locomotion, Prog. Brain Res., 164, 237, 10.1016/S0079-6123(07)64013-8

Berger, 1998, Characteristics of locomotor control in children with cerebral palsy, Neurosci. Biobehav. Rev., 22, 579, 10.1016/S0149-7634(97)00047-X

Berger, 1984, Normal and impaired development of children's gait, Hum. Neurobiol., 3, 163

Berger, 1982, Pathophysiology of gait in children with cerebral palsy, Electroencephalogr. Clin. Neurophysiol., 53, 538, 10.1016/0013-4694(82)90066-9

Bernstein, 1967, The Co-ordination and Regulation of Movements

Bertsch, 2004, Evaluation of early walking patterns from plantar pressure distribution measurements. First year results of 42 children, Gait Posture, 19, 235, 10.1016/S0966-6362(03)00064-X

Bianchi, 1998, Individual characteristics of human walking mechanics, Pflugers Arch., 436, 343, 10.1007/s004240050642

Bizzi, 2000, New perspectives on spinal motor systems, Nat. Rev. Neurosci., 1, 101, 10.1038/35039000

Borghese, 1996, Kinematic determinants of human locomotion, J. Physiol. (Lond.), 494, 863, 10.1113/jphysiol.1996.sp021539

Caliñski, 1974, A dendrite method for cluster analysis, Commun. Stat., 3, 1

Cappellini, 2010, Migration of motor pool activity in the spinal cord reflects body mechanics in human locomotion, J. Neurophysiol., 104, 3064, 10.1152/jn.00318.2010

Cavagna, 1983, The mechanics of walking in children, J. Physiol. (Lond.), 343, 323, 10.1113/jphysiol.1983.sp014895

Cheron, 2015, From biomechanics to sport psychology: the current oscillatory approach, Front. Psychol., 6, 1642, 10.3389/fpsyg.2015.01642

Cheron, 2001a, Early emergence of temporal co-ordination of lower limb segments elevation angles in human locomotion, Neurosci. Lett., 308, 123, 10.1016/S0304-3940(01)01925-5

Cheron, 2001b, Development of a kinematic coordination pattern in toddler locomotion: planar covariation, Exp. Brain Res., 137, 455, 10.1007/s002210000663

Cheung, 2012, Muscle synergy patterns as physiological markers of motor cortical damage, Proc. Natl. Acad. Sci. U.S.A., 109, 14652, 10.1073/pnas.1212056109

Chvatal, 2013, Common muscle synergies for balance and walking, Front. Comput. Neurosci., 7, 48, 10.3389/fncom.2013.00048

Crenna, 1998, Spasticity and “spastic” gait in children with cerebral palsy, Neurosci. Biobehav. Rev., 22, 571, 10.1016/S0149-7634(97)00046-8

Damiano, 2015, Muscle synergies: input or output variables for neural control?, Dev. Med. Child Neurol., 57, 1091, 10.1111/dmcn.12843

Damiano, 2000, Muscle force production and functional performance in spastic cerebral palsy: relationship of cocontraction, Arch. Phys. Med. Rehabil., 81, 895, 10.1053/apmr.2000.5579

Dan, 2004, Gait control in spinal palsy, Brain Dev., 26, 463, 10.1016/j.braindev.2004.01.003

Danner, 2015, Human spinal locomotor control is based on flexibly organized burst generators, Brain, 138, 577, 10.1093/brain/awu372

d'Avella, 2006, Control of fast-reaching movements by muscle synergy combinations, J. Neurosci., 26, 7791, 10.1523/JNEUROSCI.0830-06.2006

Davis, 1993, Phasic behavior of EMG signals during gait: use of multivariate statistics, J. Electromyogr. Kinesiol., 3, 51, 10.1016/1050-6411(93)90023-P

Dayanidhi, 2013, Decrease in muscle contraction time complements neural maturation in the development of dynamic manipulation, J. Neurosci., 33, 15050, 10.1523/JNEUROSCI.1968-13.2013

Degelean, 2012, Effect of ankle-foot orthoses on trunk sway and lower limb intersegmental coordination in children with bilateral cerebral palsy, J. Pediatr. Rehabil. Med., 5, 171, 10.3233/PRM-2012-0209

DeJaeger, 2001, The energy cost of walking in children, Pflugers Arch., 441, 538, 10.1007/s004240000443

Dominici, 2011, Locomotor primitives in newborn babies and their development, Science, 334, 997, 10.1126/science.1210617

Dominici, 2007, Control of foot trajectory in walking toddlers: adaptation to load changes, J. Neurophysiol., 97, 2790, 10.1152/jn.00262.2006

Eyre, 1991, Constancy of central conduction delays during development in man: investigation of motor and somatosensory pathways, J. Physiol. (Lond.), 434, 441, 10.1113/jphysiol.1991.sp018479

Eyre, 2001, Evidence of activity-dependent withdrawal of corticospinal projections during human development, Neurology, 57, 1543, 10.1212/WNL.57.9.1543

Forssberg, 1985, Ontogeny of human locomotor control. I. Infant stepping, supported locomotion and transition to independent locomotion, Exp. Brain Res., 57, 480, 10.1007/BF00237835

Forssberg, 1999, Neural control of human motor development, Curr. Opin. Neurobiol., 9, 676, 10.1016/S0959-4388(99)00037-9

Friel, 2012, Using motor behavior during an early critical period to restore skilled limb movement after damage to the corticospinal system during development, J. Neurosci., 32, 9265, 10.1523/JNEUROSCI.1198-12.2012

Friel, 2014, Activity-based therapies for repair of the corticospinal system injured during development, Front. Neurol., 5, 229, 10.3389/fneur.2014.00229

Gerasimenko, 2015, Initiation and modulation of locomotor circuitry output with multisite transcutaneous electrical stimulation of the spinal cord in noninjured humans, J. Neurophysiol., 113, 834, 10.1152/jn.00609.2014

Giszter, 2015, Motor primitives–new data and future questions, Curr. Opin. Neurobiol., 33, 156, 10.1016/j.conb.2015.04.004

Gormley, 2001, Treatment of neuromuscular and musculoskeletal problems in cerebral palsy, Pediatr. Rehabil., 4, 5, 10.1080/13638490151068393

Graham, 2016, Cerebral palsy, Nat. Rev. Dis. Primers, 2, 15082, 10.1038/nrdp.2016.5

Grasso, 2004, Distributed plasticity of locomotor pattern generators in spinal cord injured patients, Brain, 127, 1019, 10.1093/brain/awh115

Grillner, 1981, Control of locomotion in bipeds, tetrapods and fish, Handbook of Physiology: Section 1: The Nervous System, Vol. II, Part. 1 Motor Control, 1179

Hadders-Algra, 2004, General movements: a window for early identification of children at high risk for developmental disorders, J. Pediatr., 145, S12, 10.1016/j.jpeds.2004.05.017

Hadders-Algra, 2014, Early diagnosis and early intervention in cerebral palsy, Front. Neurol., 5, 185, 10.3389/fneur.2014.00185

Hadders-Algra, 1992, Developmental course of general movements in early infancy. II. EMG correlates, Early Hum. Dev., 28, 231, 10.1016/0378-3782(92)90170-L

Hallett, 1975, EMG analysis of patients with cerebellar deficits, J. Neurol. Neurosurg. Psychiatr., 38, 1163, 10.1136/jnnp.38.12.1163

Hanson, 1989, Gait abnormalities and inhibitive casts in cerebral palsy. Literature review, J. Am. Podiatr. Med. Assoc., 79, 53, 10.7547/87507315-79-2-53

Hausdorff, 1999, Maturation of gait dynamics: stride-to-stride variability and its temporal organization in children, J. Appl. Physiol., 86, 1040, 10.1152/jappl.1999.86.3.1040

Hidecker, 2011, Developing and validating the Communication Function Classification System for individuals with cerebral palsy, Dev. Med. Child Neurol., 53, 704, 10.1111/j.1469-8749.2011.03996.x

Himmelmann, 2005, The changing panorama of cerebral palsy in Sweden. IX. Prevalence and origin in the birth-year period 1995-1998, Acta Paediatr., 94, 287, 10.1111/j.1651-2227.2005.tb03071.x

Hodapp, 2009, Changes in soleus H-reflex modulation after treadmill training in children with cerebral palsy, Brain, 132, 37, 10.1093/brain/awn287

Hoellinger, 2013, Biological oscillations for learning walking coordination: dynamic recurrent neural network functionally models physiological central pattern generator, Front. Comput. Neurosci., 7, 70, 10.3389/fncom.2013.00070

Hug, 2012, Smoothing of electromyographic signals can influence the number of extracted muscle synergies, Clin. Neurophysiol., 123, 1895, 10.1016/j.clinph.2012.01.015

Hultborn, 2001, State-dependent modulation of sensory feedback, J. Physiol. (Lond.), 533, 5, 10.1111/j.1469-7793.2001.0005b.x

Hutton, 2002, Effects of cognitive, motor, and sensory disabilities on survival in cerebral palsy, Arch. Dis. Child., 86, 84, 10.1136/adc.86.2.84

Ivanenko, 2005a, Coordination of locomotion with voluntary movements in humans, J. Neurosci., 25, 7238, 10.1523/JNEUROSCI.1327-05.2005

Ivanenko, 2004, Development of pendulum mechanism and kinematic coordination from the first unsupported steps in toddlers, J. Exp. Biol., 207, 3797, 10.1242/jeb.01214

Ivanenko, 2013a, Changes in the spinal segmental motor output for stepping during development from infant to adult, J. Neurosci., 33, 3025a, 10.1523/JNEUROSCI.2722-12.2013

Ivanenko, 2005b, Kinematics in newly walking toddlers does not depend upon postural stability, J. Neurophysiol., 94, 754, 10.1152/jn.00088.2005

Ivanenko, 2007, Development of independent walking in toddlers, Exerc. Sport Sci. Rev., 35, 67, 10.1249/JES.0b013e31803eafa8

Ivanenko, 2002, Control of foot trajectory in human locomotion: role of ground contact forces in simulated reduced gravity, J. Neurophysiol., 87, 3070, 10.1152/jn.2002.87.6.3070

Ivanenko, 2006a, Motor control programs and walking, Neuroscientist, 12, 339, 10.1177/1073858406287987

Ivanenko, 2006b, Spinal cord maps of spatiotemporal alpha-motoneuron activation in humans walking at different speeds, J. Neurophysiol., 95, 602, 10.1152/jn.00767.2005

Ivanenko, 2013b, Trunk orientation, stability, and quadrupedalism, Front. Neurol., 4, 20, 10.3389/fneur.2013.00020

Jankowska, 2008, Spinal interneuronal networks in the cat: elementary components, Brain Res. Rev., 57, 46, 10.1016/j.brainresrev.2007.06.022

Kanemaru, 2014, Jerky spontaneous movements at term age in preterm infants who later developed cerebral palsy, Early Hum. Dev., 90, 387, 10.1016/j.earlhumdev.2014.05.004

Kendall, 2005, Muscles, Testing and Function with Posture and Pain

Lacquaniti, 2012a, Development of human locomotion, Curr. Opin. Neurobiol., 22, 822, 10.1016/j.conb.2012.03.012

Lacquaniti, 2012b, Patterned control of human locomotion, J. Physiol. (Lond.), 590, 2189, 10.1113/jphysiol.2011.215137

La Scaleia, 2014, Spinal motor outputs during step-to-step transitions of diverse human gaits, Front. Hum. Neurosci., 8, 305, 10.3389/fnhum.2014.00305

Lee, 2001, Algorithms for non-negative matrix factorization, Advances in Neural Information Processing Systems, 556

Leonard, 1991, The development of independent walking in children with cerebral palsy, Dev. Med. Child Neurol., 33, 567, 10.1111/j.1469-8749.1991.tb14926.x

MacLellan, 2011, Increased obstacle clearance in people with ARCA-1 results in part from voluntary coordination changes between the thigh and shank segments, Cerebellum, 10, 732, 10.1007/s12311-011-0283-0

MacLellan, 2012, Features of hand-foot crawling behavior in human adults, J. Neurophysiol., 107, 114, 10.1152/jn.00693.2011

Martin, 2005, The corticospinal system: from development to motor control, Neuroscientist, 11, 161, 10.1177/1073858404270843

Martino, 2015, Neuromuscular adjustments of gait associated with unstable conditions, J. Neurophysiol., 114, 2867, 10.1152/jn.00029.2015

Martino, 2014, Locomotor patterns in cerebellar ataxia, J. Neurophysiol., 112, 2810, 10.1152/jn.00275.2014

Massaad, 2010, Reducing the energy cost of hemiparetic gait using center of mass feedback: a pilot study, Neurorehabil. Neural Repair, 24, 338, 10.1177/1545968309349927

Meyns, 2012, Altered arm posture in children with cerebral palsy is related to instability during walking, Eur. J. Paediatr. Neurol., 16, 528, 10.1016/j.ejpn.2012.01.011

Meyns, 2014, Interlimb coordination during forward walking is largely preserved in backward walking in children with cerebral palsy, Clin. Neurophysiol, 125, 552, 10.1016/j.clinph.2013.08.022

Monaco, 2010, Age-related modifications of muscle synergies and spinal cord activity during locomotion, J. Neurophysiol., 104, 2092, 10.1152/jn.00525.2009

Myklebust, 1990, A review of myotatic reflexes and the development of motor control and gait in infants and children: a special communication, Phys. Ther., 70, 188, 10.1093/ptj/70.3.188

Palisano, 2006, Stability of the gross motor function classification system, Dev. Med. Child Neurol., 48, 424, 10.1017/S0012162206000934

Palisano, 1997, Development and reliability of a system to classify gross motor function in children with cerebral palsy, Dev. Med. Child Neurol., 39, 214, 10.1111/j.1469-8749.1997.tb07414.x

Paus, 1999, Structural maturation of neural pathways in children and adolescents: in vivo study, Science, 283, 1908, 10.1126/science.283.5409.1908

Phillips, 1991, Electrophysiologic mapping of the segmental anatomy of the muscles of the lower extremity, Muscle Nerve, 14, 1213, 10.1002/mus.880141213

Prosser, 2010, Trunk and hip muscle activation patterns are different during walking in young children with and without cerebral palsy, Phys. Ther., 90, 986, 10.2522/ptj.20090161

Rosenbaum, 2014, Classification in childhood disability: focusing on function in the 21st century, J. Child Neurol., 29, 1036, 10.1177/0883073814533008

Rudolph, 2000, Dynamic stability after ACL injury: who can hop?, Knee Surg. Sports Traumatol. Arthrosc., 8, 262, 10.1007/s001670000130

Russell, 2000, Improved scaling of the gross motor function measure for children with cerebral palsy: evidence of reliability and validity, Phys. Ther., 80, 873, 10.1093/ptj/80.9.873

Russell, 1989, The gross motor function measure: a means to evaluate the effects of physical therapy, Dev. Med. Child Neurol., 31, 341, 10.1111/j.1469-8749.1989.tb04003.x

Russo, 2014, Dimensionality of joint torques and muscle patterns for reaching, Front. Comput. Neurosci., 8, 24, 10.3389/fncom.2014.00024

Sale, 2014, Environment and brain plasticity: towards an endogenous pharmacotherapy, Physiol. Rev., 94, 189, 10.1152/physrev.00036.2012

Salimi, 2008, Pyramidal tract stimulation restores normal corticospinal tract connections and visuomotor skill after early postnatal motor cortex activity blockade, J. Neurosci., 28, 7426, 10.1523/JNEUROSCI.1078-08.2008

Schepens, 2004, Mechanical work and muscular efficiency in walking children, J. Exp. Biol., 207, 587, 10.1242/jeb.00793

Sharrard, 1955, The distribution of the permanent paralysis in the lower limb in poliomyelitis; a clinical and pathological study, J. Bone Joint. Surg. Br., 37B, 540, 10.1302/0301-620X.37B4.540

Sharrard, 1964, The segmental innervation of the lower limb muscles in man, Ann. R. Coll. Surg. Engl., 35, 106

Shuman, 2016, Repeatability of muscle synergies within and between days for typically developing children and children with cerebral palsy, Gait Posture, 45, 127, 10.1016/j.gaitpost.2016.01.011

Smania, 2011, Improved gait after repetitive locomotor training in children with cerebral palsy, Am. J. Phys. Med. Rehabil., 90, 137, 10.1097/PHM.0b013e318201741e

Steele, 2015, Muscle synergies and complexity of neuromuscular control during gait in cerebral palsy, Dev. Med. Child Neurol, 57, 1176, 10.1111/dmcn.12826

Steele, 2013, The number and choice of muscles impact the results of muscle synergy analyses, Front. Comput. Neurosci., 7, 105, 10.3389/fncom.2013.00105

Stewart, 1992, Electrophysiological mapping of the segmental anatomy of the muscles of the lower extremity, Muscle Nerve, 15, 965

Sutherland, 1993, Common gait abnormalities of the knee in cerebral palsy, Clin. Orthop. Relat. Res., 139

Tang, 2015, Muscle synergy analysis in children with cerebral palsy, J. Neural Eng., 12, 46017, 10.1088/1741-2560/12/4/046017

Tomlinson, 1977, The numbers of limb motor neurons in the human lumbosacral cord throughout life, J. Neurol. Sci., 34, 213, 10.1016/0022-510X(77)90069-7

Torres-Oviedo, 2006, Muscle synergy organization is robust across a variety of postural perturbations, J. Neurophysiol., 96, 1530, 10.1152/jn.00810.2005

Tresch, 2006, Matrix factorization algorithms for the identification of muscle synergies: evaluation on simulated and experimental data sets, J. Neurophysiol., 95, 2199, 10.1152/jn.00222.2005

Vasudevan, 2011, Younger is not always better: development of locomotor adaptation from childhood to adulthood, J. Neurosci., 31, 3055, 10.1523/JNEUROSCI.5781-10.2011

Ward, 2009, Are current measurements of lower extremity muscle architecture accurate?, Clin. Orthop. Relat. Res., 467, 1074, 10.1007/s11999-008-0594-8

Wenger, 2016, Spatiotemporal neuromodulation therapies engaging muscle synergies improve motor control after spinal cord injury, Nat. Med., 22, 138, 10.1038/nm.4025

Wiener-Vacher, 1996, Changes in otolith VOR to off vertical axis rotation in infants learning to walk. Preliminary results of a longitudinal study, Ann. N.Y. Acad. Sci., 781, 709, 10.1111/j.1749-6632.1996.tb15767.x

Williams, 2011, Classification of the reduced vertical component of the ground reaction force in late stance in cerebral palsy gait, Gait Posture, 34, 370, 10.1016/j.gaitpost.2011.06.003

Willoughby, 2009, A systematic review of the effectiveness of treadmill training for children with cerebral palsy, Disabil. Rehabil., 31, 1971, 10.3109/09638280902874204

Winter, 1992, Foot trajectory in human gait: a precise and multifactorial motor control task, Phys. Ther., 72, 45, 10.1093/ptj/72.1.45

Yakovenko, 2002, Spatiotemporal activation of lumbosacral motoneurons in the locomotor step cycle, J. Neurophysiol., 87, 1542, 10.1152/jn.00479.2001

Yakovlev, 1967, The myelogenetic cycles of regional maturation of the brain, Regional Development of the Brain in Early Life, 3

Yang, 2006, Spinal and brain control of human walking: implications for retraining of walking, Neuroscientist, 12, 379, 10.1177/1073858406292151

Yang, 2013, Training to enhance walking in children with cerebral palsy: are we missing the window of opportunity?, Semin. Pediatr. Neurol., 20, 106, 10.1016/j.spen.2013.06.011

Yang, 2015, Characteristics of the developing human locomotor system: Similarities to other mammals, Dev. Psychobiol., 57, 397, 10.1002/dev.21289

Yeo, 2014, The different maturation of the corticospinal tract and corticoreticular pathway in normal brain development: diffusion tensor imaging study, Front. Hum. Neurosci., 8, 573, 10.3389/fnhum.2014.00573

Zelik, 2014, Can modular strategies simplify neural control of multidirectional human locomotion?, J. Neurophysiol., 111, 1686, 10.1152/jn.00776.2013

Zollinger, 2016, External mechanical work and pendular energy transduction of overground and treadmill walking in adolescents with unilateral cerebral palsy, Front. Physiol., 7, 121, 10.3389/fphys.2016.00121