Abstract
The accomplishment of mature locomotor movements relies upon the integrated coordination of the lower and upper limbs and the trunk. Human adults normally swing their arms and a quadrupedal limb coordination persists during bipedal walking despite a strong corticospinal control of the upper extremities that allows to uncouple this connection during voluntary activities. Here we investigated arm–leg coordination during stepping responses on a surface in human neonates. In eight neonates, we found the overt presence of alternating arm–leg oscillations, the arms moving up and down in alternation with ipsilateral lower limb movements. These neonates moved the diagonal limbs together, and the peak of the arm-to-trunk angle (i.e., maximum vertical excursion of the arm) occurred around the end of the ipsilateral stance phase, as it occurs during typical adult walking. Although episodes of arm–leg coordination were sporadic in our sample of neonates, their presence provides significant evidence for a neural coupling between the upper and lower limbs during early ontogenesis of locomotion in humans.
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References
Adolph KE, Vereijken B, Denny MA (1998) Learning to crawl. Child Dev 69:1299–1312. https://doi.org/10.1111/j.1467-8624.1998.tb06213.x
Barbu-Roth M, Anderson DI, Streeter RJ et al (2015) Why does infant stepping disappear and can it be stimulated by optic flow? Child Dev 86:441–455. https://doi.org/10.1111/cdev.12305
Barthelemy D, Nielsen JB (2010) Corticospinal contribution to arm muscle activity during human walking: cortical involvement in rhythmic arm movement. J Physiol 588:967–979. https://doi.org/10.1113/jphysiol.2009.185520
Berens P (2009) CircStat: a MATLAB toolbox for circular statistics. J Stat Softw 31
Burnett CN, Johnson EW (1971) Development of gait in childhood: Part II. Dev Med Child Neurol 13:207–215. https://doi.org/10.1111/j.1469-8749.1971.tb03246.x
de Vries JIP, Visser GHA, Prechtl HFR (1982) The emergence of fetal behaviour. I. Qualitative aspects. Early Human Dev 7:301–322. https://doi.org/10.1016/0378-3782(82)90033-0
Dietz V (2002) Do human bipeds use quadrupedal coordination? Trends Neurosci 25:462–467
Dietz V, Michel J (2009) Human Bipeds use quadrupedal coordination during locomotion. Ann N Y Acad Sci 1164:97–103. https://doi.org/10.1111/j.1749-6632.2008.03710.x
Domellöf E, Rönnqvist L, Hopkins B (2007) Functional asymmetries in the stepping response of the human newborn: a kinematic approach. Exp Brain Res 177:324–335. https://doi.org/10.1007/s00221-006-0675-4
Dominici N, Ivanenko YP, Lacquaniti F (2007) Control of foot trajectory in walking toddlers: adaptation to load changes. J Neurophysiol 97:2790–2801. https://doi.org/10.1152/jn.00262.2006
Dominici N, Ivanenko YP, Cappellini G et al (2011) Locomotor primitives in newborn babies and their development. Science 334:997–999. https://doi.org/10.1126/science.1210617
Donker SF, Beek PJ, Wagenaar RC, Mulder T (2001) Coordination between arm and leg movements during locomotion. J Mot Behav 33:86–102. https://doi.org/10.1080/00222890109601905
Eyre JA, Miller S, Clowry GJ et al (2000) Functional corticospinal projections are established prenatally in the human foetus permitting involvement in the development of spinal motor centres. Brain 123:51–64. https://doi.org/10.1093/brain/123.1.51
Forssberg H (1985) Ontogeny of human locomotor control. I. Infant stepping, supported locomotion and transition to independent locomotion. Exp Brain Res 57:480–493
Freedland RL, Bertenthal BI (1994) Developmental changes in interlimb coordination: transition to hands-and-knees crawling. Psychol Sci 5:26–32. https://doi.org/10.1111/j.1467-9280.1994.tb00609.x
Frigon A (2017) The neural control of interlimb coordination during mammalian locomotion. J Neurophysiol 117:2224–2241. https://doi.org/10.1152/jn.00978.2016
Gerasimenko Y, Gorodnichev R, Machueva E et al (2010) Novel and direct access to the human locomotor spinal circuitry. J Neurosci 30:3700–3708
Grillner S (2006) Biological pattern generation: the cellular and computational logic of networks in motion. Neuron 52:751–766. https://doi.org/10.1016/j.neuron.2006.11.008
Grillner S (2011) Human locomotor circuits conform. Science 334:912–913. https://doi.org/10.1126/science.1214778
Hadders-Algra M, Van Eykern LA, Klip-Van den Nieuwendijk AW, Prechtl HF (1992) Developmental course of general movements in early infancy. II. EMG correlates. Early Hum Dev 28:231–251
Hadders-Algra M, Nakae Y, Van Eykern LA et al (1993) The effect of behavioural state on general movements in healthy full-term newborns. A polymyographic study. Early Hum Dev 35:63–79
Hofsten C, Ronnqvist L (1993) The structuring of neonatal arm movements. Child Dev 64:1046–1057. https://doi.org/10.1111/j.1467-8624.1993.tb04187.x
Ivanenko YP, Dominici N, Cappellini G et al (2013) Changes in the spinal segmental motor output for stepping during development from infant to adult. J Neurosci 33:3025–3036. https://doi.org/10.1523/JNEUROSCI.2722-12.2013
Jackson KM, Joseph J, Wyard SJ (1983) The upper limbs during human walking. Part I: Sagittal movement. Electromyogr Clin Neurophysiol 23:425–434
Juvin L, Le Gal J-P, Simmers J, Morin D (2012) Cervicolumbar coordination in mammalian quadrupedal locomotion: role of spinal thoracic circuitry and limb sensory inputs. J Neurosci 32:953–965. https://doi.org/10.1523/JNEUROSCI.4640-11.2012
Kanemaru N, Watanabe H, Taga G (2012) Increasing selectivity of interlimb coordination during spontaneous movements in 2- to 4-month-old infants. Exp Brain Res 218:49–61. https://doi.org/10.1007/s00221-012-3001-3
Kato M, Hirashima M, Oohashi H et al (2014) Decomposition of spontaneous movements of infants as combinations of limb synergies. Exp Brain Res. https://doi.org/10.1007/s00221-014-3972-3
Kawai M, Savelsbergh GJP, Wimmers RH (1999) Newborns spontaneous arm movements are influenced by the environment. Early Human Dev 54:15–27. https://doi.org/10.1016/S0378-3782(98)00081-4
Kuczynski V, Telonio A, Thibaudier Y et al (2017) Lack of adaptation during prolonged split-belt locomotion in the intact and spinal cat. J Physiol. https://doi.org/10.1113/JP274518
La Scaleia V, Ivanenko YP, Zelik KE, Lacquaniti F (2014) Spinal motor outputs during step-to-step transitions of diverse human gaits. Front Hum Neurosci 8:305. https://doi.org/10.3389/fnhum.2014.00305
Lacquaniti F, Ivanenko YP, Zago M (2012) Development of human locomotion. Curr Opin Neurobiol 22:822–828. https://doi.org/10.1016/j.conb.2012.03.012
Lacquaniti F, Ivanenko YP, d’Avella A et al (2013) Evolutionary and developmental modules. Front Comput Neurosci 7:61. https://doi.org/10.3389/fncom.2013.00061
Ledebt A (2000) Changes in arm posture during the early acquisition of walking. Infant Behav Dev 23:79–89. https://doi.org/10.1016/S0163-6383(00)00027-8
Lüchinger AB, Hadders-Algra M, van Kan CM, de Vries JIP (2008) Fetal onset of general movements. Pediatr Res 63:191–195. https://doi.org/10.1203/PDR.0b013e31815ed03e
MacLellan MJ, Ivanenko YP, Cappellini G et al (2012) Features of hand–foot crawling behavior in human adults. J Neurophysiol 107:114–125. https://doi.org/10.1152/jn.00693.2011
MacLellan MJ, Catavitello G, Ivanenko YP, Lacquaniti F (2017) Planar covariance of upper and lower limb elevation angles during hand–foot crawling in healthy young adults. Exp Brain Res. https://doi.org/10.1007/s00221-017-5060-y
Martin JH (2005) The corticospinal system: from development to motor control. Neuroscientist 11:161–173. https://doi.org/10.1177/1073858404270843
Massaad F, Levin O, Meyns P et al (2014) Arm sway holds sway: locomotor-like modulation of leg reflexes when arms swing in alternation. Neuroscience 258:34–46. https://doi.org/10.1016/j.neuroscience.2013.10.007
McGraw MB (1939) Swimming behavior of the human infant. J Pediatr 15:485–490. https://doi.org/10.1016/S0022-3476(39)80003-8
McGraw MB (1940) Neuromuscular development of the human infant as exemplified in the achievement of erect locomotion. J Pediatr 17:747–771
Meyns P, Bruijn SM, Duysens J (2013) The how and why of arm swing during human walking. Gait Posture 38:555–562. https://doi.org/10.1016/j.gaitpost.2013.02.006
Meyns P, Molenaers G, Desloovere K, Duysens J (2014) Interlimb coordination during forward walking is largely preserved in backward walking in children with cerebral palsy. Clin Neurophysiol 125:552–561. https://doi.org/10.1016/j.clinph.2013.08.022
Murray MP, Mollinger LA, Gardner GM, Sepic SB (1984) Kinematic and EMG patterns during slow, free, and fast walking. J Orthop Res 2:272–280. https://doi.org/10.1002/jor.1100020309
Nathan PW, Smith M, Deacon P (1996) Vestibulospinal, reticulospinal and descending propriospinal nerve fibres in man. Brain 119(Pt 6):1809–1833
Niedźwiedzki G, Szrek P, Narkiewicz K et al (2010) Tetrapod trackways from the early Middle Devonian period of Poland. Nature 463:43–48. https://doi.org/10.1038/nature08623
Niemitz C (2002) Kinematics and ontogeny of locomotion in monkeys and human babies. Zeitschrift für Morphologie Anthropologie 83:383–400. https://doi.org/10.2307/25757620
Patrick SK, Noah JA, Yang JF (2009) Interlimb coordination in human crawling reveals similarities in development and neural control with quadrupeds. J Neurophysiol 101:603–613. https://doi.org/10.1152/jn.91125.2008
Patrick SK, Noah JA, Yang JF (2012) Developmental constraints of quadrupedal coordination across crawling styles in human infants. J Neurophysiol 107:3050–3061. https://doi.org/10.1152/jn.00029.2012
Pavlidis E, Cantalupo G, Cattani L et al (2016) Neonatal seizure automatism and human inborn pattern of quadrupedal locomotion. Gait Posture 49:232–234. https://doi.org/10.1016/j.gaitpost.2016.07.015
Pontzer H, Holloway JH, Raichlen DA, Lieberman DE (2009) Control and function of arm swing in human walking and running. J Exp Biol 212:523–534. https://doi.org/10.1242/jeb.024927
Robinson SR, Kleven GA, Brumley MR (2008) Prenatal development of interlimb motor learning in the rat fetus. Infancy 13:204–228. https://doi.org/10.1080/15250000802004288
Ruder L, Takeoka A, Arber S (2016) Long-distance descending spinal neurons ensure quadrupedal locomotor stability. Neuron 92:1063–1078. https://doi.org/10.1016/j.neuron.2016.10.032
Siekerman K, Barbu-Roth M, Anderson DI et al (2015) Treadmill stimulation improves newborn stepping. Dev Psychobiol 57:247–254. https://doi.org/10.1002/dev.21270
Solopova IA, Selionov VA, Zhvansky DS et al (2016) Human cervical spinal cord circuitry activated by tonic input can generate rhythmic arm movements. J Neurophysiol 115:1018–1030. https://doi.org/10.1152/jn.00897.2015
Sparrow WA (1989) Creeping patterns of human adults and infants. Am J Phys Anthropol 78:387–401. https://doi.org/10.1002/ajpa.1330780307
Sutherland DH, Olshen R, Cooper L, Woo SL (1980) The development of mature gait. J Bone Joint Surg Am 62:336–353
Sylos-Labini F, Ivanenko YP, MacLellan MJ et al (2014) Locomotor-like leg movements evoked by rhythmic arm movements in humans. PLoS One 9:e90775. https://doi.org/10.1371/journal.pone.0090775
Sylos-Labini F, Magnani S, Cappellini G et al (2017) Foot placement characteristics and plantar pressure distribution patterns during stepping on ground in neonates. Front Physiol 8:784. https://doi.org/10.3389/fphys.2017.00784
Teulier C, Sansom JK, Muraszko K, Ulrich BD (2012) Longitudinal changes in muscle activity during infants’ treadmill stepping. J Neurophysiol 108:853–862. https://doi.org/10.1152/jn.01037.2011
Thelen E, Fisher DM (1982) Newborn stepping: an explanation for a” disappearing” reflex. Dev Psychol 18:760
Thelen E, Fisher DM, Ridley-Johnson R, Griffin NJ (1982) Effects of body build and arousal on newborn infant stepping. Dev Psychobiol 15:447–453. https://doi.org/10.1002/dev.420150506
van der Meer A, van der Weel F, Lee D (1995) The functional significance of arm movements in neonates. Science 267:693–695. https://doi.org/10.1126/science.7839147
Varendi H, Porter RH (2001) Breast odour as the only maternal stimulus elicits crawling towards the odour source. Acta Paediatr 90:372–375
Vinay L, Brocard F, Clarac F et al (2002) Development of posture and locomotion: an interplay of endogenously generated activities and neurotrophic actions by descending pathways. Brain Res Rev 40:118–129. https://doi.org/10.1016/S0165-0173(02)00195-9
Wagenaar RC, van Emmerik REA (1994) Dynamics of pathological gait. Hum Mov Sci 13:441–471. https://doi.org/10.1016/0167-9457(94)90049-3
Wannier T, Bastiaanse C, Colombo G, Dietz V (2001) Arm to leg coordination in humans during walking, creeping and swimming activities. Exp Brain Res 141:375–379. https://doi.org/10.1007/s002210100875
Webb D, Tuttle RH, Baksh M (1994) Pendular activity of human upper limbs during slow and normal walking. Am J Phys Anthropol 93:477–489. https://doi.org/10.1002/ajpa.1330930407
Yang JF, Stephens MJ, Vishram R (1998) Infant stepping: a method to study the sensory control of human walking. J Physiol 507:927–937. https://doi.org/10.1111/j.1469-7793.1998.927bs.x
Yang JF, Mitton M, Musselman KE et al (2015) Characteristics of the developing human locomotor system: similarities to other mammals. Dev Psychobiol 57:397–408. https://doi.org/10.1002/dev.21289
Zampagni ML, Brigadoi S, Schena F et al (2011) Idiosyncratic control of the center of mass in expert climbers: control of the center of mass in expert climbers. Scand J Med Sci Sports 21:688–699. https://doi.org/10.1111/j.1600-0838.2010.01098.x
Zehr EP, Duysens J (2004) Regulation of arm and leg movement during human locomotion. Neuroscientist 10:347–361. https://doi.org/10.1177/1073858404264680
Zehr EP, Barss TS, Dragert K et al (2016) Neuromechanical interactions between the limbs during human locomotion: an evolutionary perspective with translation to rehabilitation. Exp Brain Res 234:3059–3081. https://doi.org/10.1007/s00221-016-4715-4
Zelazo PR, Zelazo NA, Kolb S (1972) “Walking” in the newborn. Science 176:314–315
Acknowledgements
We thank Marika Cicchese, Nadia Dominici, Carlo Giannini, Vito Mondì and Tiziana Silei for help with some of the experiments. This work was supported by the Italian Ministry of Health (IRCCS Ricerca corrente), Italian Space Agency (contract no. I/006/06/0), Italian University Ministry (PRIN Grant 2015HFWRYY_002), Lazio Region (INNOVA.1 FILAS—RU 2014_1033), and Horizon 2020 Robotics Program (ICT-23-2014 under Grant Agreement 644727-CogIMon).
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La Scaleia, V., Ivanenko, Y., Fabiano, A. et al. Early manifestation of arm–leg coordination during stepping on a surface in human neonates. Exp Brain Res 236, 1105–1115 (2018). https://doi.org/10.1007/s00221-018-5201-y
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DOI: https://doi.org/10.1007/s00221-018-5201-y