Experimental Brain Research

, Volume 235, Issue 11, pp 3287–3294 | Cite as

Planar covariance of upper and lower limb elevation angles during hand–foot crawling in healthy young adults

  • M. J. MacLellan
  • G. Catavitello
  • Y. P. Ivanenko
  • F. Lacquaniti
Research Article


Habitual quadrupeds have been shown to display a planar covariance of segment elevation angle waveforms in the fore and hind limbs during many forms of locomotion. The purpose of the current study was to determine if humans generate similar patterns in the upper and lower limbs during hand–foot crawling. Nine healthy young adults performed hand–foot crawling on a treadmill at speeds of 1, 2, and 3 km/h. A principal component analysis (PCA) was applied to the segment elevation angle waveforms for the upper (upper arm, lower arm, and hand) and lower (thigh, shank, and foot) limbs separately. The planarity of the elevation angle waveforms was determined using the sum of the variance explained by the first two PCs and the orientation of the covariance plane was quantified using the direction cosines of the eigenvector orthogonal to the plane, projected upon each of the segmental semi-axes. Results showed that planarity of segment elevation angles was maintained in the upper and lower limbs (explained variance >97%), although a slight decrease was present in the upper limb when crawling at 3 km/h. The orientation of the covariance plane was highly limb-specific, consistent with animal studies and possibly related to the functional neural control differences between the upper and lower limbs. These results may suggest that the motor patterns stored in the central nervous system for quadrupedal locomotion may be retained through evolution and may still be exploited when humans perform such tasks.


Quadrupedal locomotion Neural control Coordination 



This research was financially supported by the Italian Ministry of Health (IRCCS Ricerca corrente), Italian Space Agency (COREA Grant 2013-084-R.0), and Horizon 2020 Robotics Program (ICT-23-2014 under Grant Agreement 644727-CogIMon).


  1. Aprigliano F, Martelli D, Micera S, Monaco V (2016) Intersegmental coordination elicited by unexpected multidirectional slipping-like perturbations resembles that adopted during steady locomotion. J Neurophysiol 115:728–740. doi: 10.1152/jn.00327.2015 CrossRefPubMedGoogle Scholar
  2. Barliya A, Omlor L, Giese MA, Flash T (2009) An analytical formulation of the law of intersegmental coordination during human locomotion. Exp Brain Res 193:371–385. doi: 10.1007/s00221-008-1633-0 CrossRefPubMedGoogle Scholar
  3. Bianchi L, Angelini D, Orani GP, Lacquaniti F (1998) Kinematic coordination in human gait: relation to mechanical energy cost. J Neurophysiol 79:2155–2170PubMedGoogle Scholar
  4. Borghese NA, Bianchi L, Lacquaniti F (1996) Kinematic determinants of human locomotion. J Physiol 494(Pt 3):863–879CrossRefPubMedPubMedCentralGoogle Scholar
  5. Catavitello G, Ivanenko YP, Lacquaniti F (2015) Planar covariation of hindlimb and forelimb elevation angles during terrestrial and aquatic locomotion of dogs. PLoS One. doi: 10.1371/journal.pone.0133936 PubMedPubMedCentralGoogle Scholar
  6. Cavagna GA, Thys H, Zamboni A (1976) The sources of external work in level walking and running. J Physiol 262:639–657CrossRefPubMedPubMedCentralGoogle Scholar
  7. 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 137:455–466CrossRefPubMedGoogle Scholar
  8. Courtine G, Schieppati M (2004) Tuning of a basic coordination pattern constructs straight-ahead and curved walking in humans. J Neurophysiol 91:1524–1535. doi: 10.1152/jn.00817.2003 CrossRefPubMedGoogle Scholar
  9. Courtine G et al (2005) Kinematic and EMG determinants in quadrupedal locomotion of a non-human primate (Rhesus). J Neurophysiol 93:3127–3145. doi: 10.1152/jn.01073.2004 CrossRefPubMedGoogle Scholar
  10. 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. doi: 10.1016/S0304-3940(00)00778-3 CrossRefPubMedGoogle Scholar
  11. 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. doi: 10.1152/jn.00945.2009 CrossRefPubMedGoogle Scholar
  12. Dominici N et al (2011) Locomotor primitives in newborn babies and their development. Science 334:997–999. doi: 10.1126/science.1210617 CrossRefPubMedGoogle Scholar
  13. Frigon A (2017) The neural control of interlimb coordination during mammalian locomotion. J Neurophysiol 00978:02016. doi: 10.1152/jn.00978.2016 Google Scholar
  14. 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 126:139–148CrossRefPubMedGoogle Scholar
  15. Grillner S (2011) Neuroscience. Human locomotor circuits conform. Science 334:912–913. doi: 10.1126/science.1214778 CrossRefPubMedGoogle Scholar
  16. Hiebert GW, Whelan PJ, Prochazka A, Pearson KG (1996) Contribution of hind limb flexor muscle afferents to the timing of phase transitions in the cat step cycle. J Neurophysiol 75:1126–1137PubMedGoogle Scholar
  17. Hildebrand M (1967) Symmetrical gaits of primates. Am J Phys Anthropol 26:119–130. doi: 10.1002/ajpa.1330260203 CrossRefGoogle Scholar
  18. Hirsch MA, Westhoff B, Toole T, Haupenthal S, Krauspe R, Hefter H (2005) Association between botulinum toxin injection into the arm and changes in gait in adults after stroke. Mov Disord 20:1014–1020. doi: 10.1002/mds.20499 CrossRefPubMedGoogle Scholar
  19. Ivanenko YP, Poppele RE, Lacquaniti F (2004) Five basic muscle activation patterns account for muscle activity during human locomotion. J Physiol-Lond 556:267–282. doi: 10.1113/jphysiol.2003.057174 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Ivanenko YP, Cappellini G, Dominici N, Poppele RE, Lacquaniti F (2005) Coordination of locomotion with voluntary movements in humans. J Neurosci 25:7238–7253. doi: 10.1523/Jneurosci.1327-05.2005 CrossRefPubMedGoogle Scholar
  21. 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. doi: 10.1152/jn.01308.2007 CrossRefPubMedGoogle Scholar
  22. Lacquaniti F, Grasso R, Zago M (1999) Motor patterns in walking. News Physiol Sci 14:168–174PubMedGoogle Scholar
  23. Leurs F, Bengoetxea A, Cebolla AM, De Saedeleer C, Dan B, Cheron G (2012) Planar covariation of elevation angles in prosthetic gait. Gait Posture 35:647–652. doi: 10.1016/j.gaitpost.2011.12.017 CrossRefPubMedGoogle Scholar
  24. MacLellan MJ, Dupre N, McFadyen BJ (2011) Increased obstacle clearance in people with ARCA-1 results in part from voluntary coordination changes between the thigh and shank segments. Cerebellum 10:732–744. doi: 10.1007/s12311-011-0283-0 CrossRefPubMedGoogle Scholar
  25. MacLellan MJ, Ivanenko YP, Cappellini G, Labini FS, Lacquaniti F (2012) Features of hand-foot crawling behavior in human adults. J Neurophysiol 107:114–125. doi: 10.1152/jn.00693.2011 CrossRefPubMedGoogle Scholar
  26. MacLellan MJ, Ivanenko YP, Catavitello G, La Scaleia V, Lacquaniti F (2013) Coupling of upper and lower limb pattern generators during human crawling at different arm/leg speed combinations. Exp Brain Res 225:217–225. doi: 10.1007/s00221-012-3364-5 CrossRefPubMedGoogle Scholar
  27. Martino G et al (2014) Locomotor patterns in cerebellar ataxia. J Neurophysiol 112:2810–2821. doi: 10.1152/jn.00275.2014 CrossRefPubMedGoogle Scholar
  28. Meyns P, Van Gestel L, Bruijn SM, Desloovere K, Swinnen SP, Duysens J (2012) Is interlimb coordination during walking preserved in children with cerebral palsy? Res Dev Disabil 33:1418–1428. doi: 10.1016/j.ridd.2012.03.020 CrossRefPubMedGoogle Scholar
  29. Nakajima K, Maier MA, Kirkwood PA, Lemon RN (2000) Striking differences in transmission of corticospinal excitation to upper limb motoneurons in two primate species. J Neurophysiol 84:698–709PubMedGoogle Scholar
  30. Noble JW, Prentice SD (2008) Intersegmental coordination while walking up inclined surfaces: age and ramp angle effects. Exp Brain Res 189:249–255. doi: 10.1007/s00221-008-1464-z CrossRefPubMedGoogle Scholar
  31. Ogihara N, Kikuchi T, Ishiguro Y, Makishima H, Nakatsukasa M (2012) Planar covariation of limb elevation angles during bipedal walking in the Japanese macaque. J R Soc Interface 9:2181–2190. doi: 10.1098/rsif.2012.0026 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Ogihara N, Oku T, Andrada E, Blickhan R, Nyakatura JA, Fischer MS (2014) Planar covariation of limb elevation angles during bipedal locomotion in common quails (Coturnix coturnix). J Exp Biol 217:3968–3973. doi: 10.1242/jeb.109355 CrossRefPubMedGoogle Scholar
  33. 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. doi: 10.1152/jn.91125.2008 CrossRefPubMedGoogle Scholar
  34. Righetti L, Nylen A, Rosander K, Iispeert AJ (2015) Kinematic and gait similarities between crawling human infants and other quadruped mammals. Front Neurol. doi: 10.3389/fneur.2015.00017 PubMedPubMedCentralGoogle Scholar
  35. Tan U (2014) Two families with quadrupedalism, mental retardation, no speech, and infantile hypotonia (Uner Tan Syndrome Type-II); a novel theory for the evolutionary emergence of human bipedalism. Front Neurosci 8:84. doi: 10.3389/fnins.2014.00084 CrossRefPubMedPubMedCentralGoogle Scholar
  36. 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. doi: 10.1007/s002210100875 CrossRefPubMedGoogle Scholar
  37. Zehr EP et al (2016) Neuromechanical interactions between the limbs during human locomotion: an evolutionary perspective with translation to rehabilitation. Exp Brain Res 234:3059–3081. doi: 10.1007/s00221-016-4715-4 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Zelenin PV, Deliagina TG, Orlovsky GN, Karayannidou A, Dasgupta NM, Sirota MG, Beloozerova IN (2011) Contribution of different limb controllers to modulation of motor cortex neurons during locomotion. J Neurosci 31:4636–4649. doi: 10.1523/JNEUROSCI.6511-10.2011 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.School of Kinesiology, College of Human Sciences and EducationLouisiana State UniversityBaton RougeUSA
  2. 2.Laboratory of Neuromotor PhysiologySanta Lucia FoundationRomeItaly
  3. 3.Centre of Space Bio-medicineUniversity of Rome Tor VergataRomeItaly
  4. 4.Department of NeuroscienceUniversity of Rome Tor VergataRomeItaly

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