Locomotor-like leg movements evoked by rhythmic arm movements in humans

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Sylos Labini, Francesca ^a,b   Ivanenko, Yuri P ^a   MacLellan, Michael J ^a,c   Cappellini, Germana ^a,b   Poppele, Richard E ^d   Lacquaniti, Francesco ^a,b  

^a IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^b UNIVERSITY OF ROME TOR VERGATA   (Italy)

^c LOUISIANA STATE UNIVERSITY   (United States)

^d UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARM MOVEMENT; ARTICLE; AUTOMATISM; BIOMECHANICS; ELECTROMYOGRAM; FEMALE; HAMSTRING; HUMAN; HUMAN EXPERIMENT; LEG MOVEMENT; LOCOMOTION; MALE; MECHANOTRANSDUCTION; MOTOR COORDINATION; NORMAL HUMAN; TRUNK; VOLUNTARY MOVEMENT; ARM; CLINICAL TRIAL; ELECTROMYOGRAPHY; LEG; MIDDLE AGED; MOVEMENT (PHYSIOLOGY); PERIODICITY; PHYSIOLOGY;

ADULT; ARM; ELECTROMYOGRAPHY; FEMALE; HUMANS; LEG; LOCOMOTION; MALE; MIDDLE AGED; MOVEMENT; PERIODICITY;

EID: 84897477908     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0090775     Document Type: Article

References (70)

1. Murray MP, Sepic SB, Barnard EJ (1967) Patterns of sagittal rotation of the upper limbs in walking. Phys Ther 47: 272-284.
2. 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. (Pubitemid 33071182)
3. Zehr EP, Duysens J (2004) Regulation of Arm and Leg Movement during Human Locomotion. The Neuroscientist 10: 347-361. (Pubitemid 38971214)
4. Blouin J-S, Fitzpatrick RC (2010) Swing those arms: automatic movement controlled by the cerebral cortex. J Physiol 588: 1029-1030.
5. Collins SH, Adamczyk PG, Kuo AD (2009) Dynamic arm swinging in human walking. Proc R Soc B Biol Sci 276: 3679-3688.
6. Barthelemy D, Nielsen JB (2010) Corticospinal contribution to arm muscle activity during human walking. J Physiol 588: 967-979.
7. De Sèze M, Falgairolle M, Viel S, Assaiante C, Cazalets J-R (2008) Sequential activation of axial muscles during different forms of rhythmic behavior in man. Exp Brain Res 185: 237-247. (Pubitemid 351208255)
8. Bruijn SM, Meijer OG, Beek PJ, Dieën JH van (2010) The effects of arm swing on human gait stability. J Exp Biol 213: 3945-3952.
9. Ballesteros ML, Buchthal F, Rosenfalck P (1965) The pattern of muscular activity during the arm swing of natural walking. Acta Physiol Scand 63: 296-310.
10. Hogue RE (1969) Upper-extremity muscular activity at different cadences and inclines during normal gait. Phys Ther 49: 963-972.
11. Ivanenko YP, Poppele RE, Lacquaniti F (2006) Spinal Cord Maps of Spatiotemporal Alpha-Motoneuron Activation in Humans Walking at Different Speeds. J Neurophysiol 95: 602-618. (Pubitemid 44699068)
12. Meyns P, Bruijn SM, Duysens J (2013) The how and why of arm swing during human walking. Gait Posture 38: 555-562.
13. Kuhtz-Buschbeck JP, Jing B (2012) Activity of upper limb muscles during human walking. J Electromyogr Kinesiol 22: 199-206.
14. Nathan PW, Smith M, Deacon P (1996) Vestibulospinal, reticulospinal and descending propriospinal nerve fibres in man. Brain 119: 1809-1833. (Pubitemid 27032616)
15. Falgairolle M, de Seze M, Juvin L, Morin D, Cazalets J-R (2006) Coordinated network functioning in the spinal cord: An evolutionary perspective. J Physiol-Paris 100: 304-316. (Pubitemid 47299193)
16. Patrick SK, Noah JA, Yang JF (2012) Developmental constraints of quadrupedal coordination across crawling styles in human infants. J Neurophysiol 107: 3050-3061.
17. MacLellan MJ, Ivanenko YP, Cappellini G, Sylos Labini F, Lacquaniti F (2012) Features of hand-foot crawling behavior in human adults. J Neurophysiol 107: 114-125.
18. Thibaudier Y, Hurteau M-F (2012) Sensory regulation of quadrupedal locomotion: a top-down or bottom-up control system? J Neurophysiol 108: 709-711.
19. Juvin L, Gal J-PL, 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.
20. Zelenin PV, Deliagina TG, Orlovsky GN, Karayannidou A, Dasgupta NM, et al. (2011) Contribution of Different Limb Controllers to Modulation of Motor Cortex Neurons during Locomotion. J Neurosci 31: 4636-4649.
21. Haridas C, Zehr EP (2003) Coordinated Interlimb Compensatory Responses to Electrical Stimulation of Cutaneous Nerves in the Hand and Foot During Walking. J Neurophysiol 90: 2850-2861. (Pubitemid 37429988)
22. Dietz V (2011) Quadrupedal coordination of bipedal gait: implications for movement disorders. J Neurol 258: 1406-1412.
23. Mezzarane R, Klimstra M, Lewis A, Hundza S, Zehr E (2011) Interlimb coupling from the arms to legs is differentially specified for populations of motor units comprising the compound H-reflex during "reduced" human locomotion. Exp Brain Res 208: 157-168.
24. Massaad F, Levin O, Meyns P, Drijkoningen D, Swinnen SP, et al. (2014) Arm sway holds sway: Locomotor-like modulation of leg reflexes when arms swing in alternation. Neuroscience 258: 34-46.
25. De Kam D, Rijken H, Manintveld T, Nienhuis B, Dietz V, et al. (2013) Arm movements can increase leg muscle activity during submaximal recumbent stepping in neurologically intact individuals. J Appl Physiol 115: 34-42.
26. Zehr EP, Hundza SR, Vasudevan EV (2009) The quadrupedal nature of human bipedal locomotion. Exerc Sport Sci Rev 37: 102-108.
27. Dietz V (2002) Do human bipeds use quadrupedal coordination? Trends Neurosci 25: 462-467. (Pubitemid 35223000)
28. Shik ML, Orlovsky GN (1965) Coordination of the legs during running of the dogs. Biophysics 10: 1148-1159.
29. Miller S, Van Der Burg J, Van Der Meché F (1975) Coordination of movements of the kindlimbs and forelimbs in different forms of locomotion in normal and decerebrate cats. Brain Res 91: 217-237.
30. Yamaguchi T (1986) Descending pathways eliciting forelimb stepping in the lateral funiculus: experimental studies with stimulation and lesion of the cervical cord in decerebrate cats. Brain Res 379: 125-136. (Pubitemid 16034340)
31. Gerasimenko Y, Musienko P, Bogacheva I, Moshonkina T, Savochin A, et al. (2009) Propriospinal Bypass of the Serotonergic System That Can Facilitate Stepping. J Neurosci 29: 5681-5689.
32. Gurfinkel VS, Levik YS, Kazennikov OV, Selionov VA (1998) Locomotor-like movements evoked by leg muscle vibration in humans. Eur J Neurosci 10: 1608-1612.
33. Selionov VA, Ivanenko YP, Solopova IA, Gurfinkel VS (2009) Tonic Central and Sensory Stimuli Facilitate Involuntary Air-Stepping in Humans. J Neurophysiol 101: 2847-2858.
34. Gerasimenko Y, Gorodnichev R, Machueva E, Pivovarova E, Semyenov D, et al. (2010) Novel and direct access to the human locomotor spinal circuitry. J Neurosci Off J Soc Neurosci 30: 3700-3708.
35. Sylos Labini F, Ivanenko YP, Cappellini G, Gravano S, Lacquaniti F (2011) Smooth changes in the EMG patterns during gait transitions under body weight unloading. J Neurophysiol 106: 1525-1536.
36. Ivanenko YP, Sylos Labini F, Cappellini G, Macellari V, McIntyre J, et al. (2011) Gait transitions in simulated reduced gravity. J Appl Physiol 110: 781-788.
37. Sylos-Labini F, Ivanenko YP, Cappellini G, Portone A, Maclellan MJ, et al. (2013) Changes of gait kinematics in different simulators of reduced gravity. J Mot Behav 45: 495-505.
38. Zhang L-Q, Wang G (2001) Dynamic and static control of the human knee joint in abduction-adduction. J Biomech 34: 1107-1115. (Pubitemid 32744660)
39. Riener R, Edrich T (1999) Identification of passive elastic joint moments in the lower extremities. J Biomech 32: 539-544. (Pubitemid 29199987)
40. De Leva P (1996) Adjustments to Zatsiorsky-Seluyanov's segment inertia parameters. J Biomech 29: 1223-1230. (Pubitemid 26302191)
41. 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. (Pubitemid 24104772)
42. Selionov VA, Solopova IA, Zhvansky DS, Karabanov AV, Chernikova LA, et al. (2013) Lack of non-voluntary stepping responses in Parkinson's disease. Neuroscience 235: 96-108.
43. Winter DA (1991) The biomechanics and motor control of human gait: normal, elderly and pathological. Waterloo, Ont.: University of Waterloo Press. 143 p.
44. Passingham RE (1996) Attention to action. Philos Trans R Soc Lond B Biol Sci 351: 1473-1479. (Pubitemid 127738808)
45. Wu T, Kansaku K, Hallett M (2004) How self-initiated memorized movements become automatic: a functional MRI study. J Neurophysiol 91: 1690-1698. (Pubitemid 38339339)
46. Thorpe SKS, Holder RL, Crompton RH (2007) Origin of human bipedalism as an adaptation for locomotion on flexible branches. Science 316: 1328-1331. (Pubitemid 46871652)
47. Cappellini G, Ivanenko YP, Dominici N, Poppele RE, Lacquaniti F (2010) Motor patterns during walking on a slippery walkway. J Neurophysiol 103: 746-760.
48. Shapiro LJ, Raichlen DA (2005) Lateral sequence walking in infant Papio cynocephalus: implications for the evolution of diagonal sequence walking in primates. Am J Phys Anthropol 126: 205-213. (Pubitemid 40144382)
49. Zampagni ML, Brigadoi S, Schena F, Tosi P, Ivanenko YP (2011) Idiosyncratic control of the center of mass in expert climbers. Scand J Med Sci Sports 21: 688-699.
50. 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.
51. Duysens J, Pearson KG (1980) Inhibition of flexor burst generation by loading ankle extensor muscles in walking cats. Brain Res 187: 321-332. (Pubitemid 10094010)
52. Donelan JM, Pearson KG (2004) Contribution of sensory feedback to ongoing ankle extensor activity during the stance phase of walking. Can J Physiol Pharmacol 82: 589-598. (Pubitemid 40065104)
53. Cazalets JR, Bertrand S (2000) Coupling between lumbar and sacral motor networks in the neonatal rat spinal cord. Eur J Neurosci 12: 2993-3002.
54. 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. (Pubitemid 34670686)
55. Balter JE, Zehr EP (2007) Neural Coupling Between the Arms and Legs During Rhythmic Locomotor-Like Cycling Movement. J Neurophysiol 97: 1809-1818. (Pubitemid 46239547)
56. Chiovetto E, Giese MA (2013) Kinematics of the coordination of pointing during locomotion. PloS One 8: e79555.
57. Dietz V, Michel J (2009) Human Bipeds Use Quadrupedal Coordination during Locomotion. Ann N Y Acad Sci 1164: 97-103.
58. Bernstein NA (1967) The co-ordination and regulation of movements. London: Pergamon Press. 226 p.
59. Duysens J, van Wezel BM, van de Crommert HW, Faist M, Kooloos JG (1998) The role of afferent feedback in the control of hamstrings activity during human gait. Eur J Morphol 36: 293-299. (Pubitemid 29148181)
60. Grillner S, Rossignol S (1978) On the initiation of the swing phase of locomotion in chronic spinal cats. Brain Res 146: 269-277. (Pubitemid 8311609)
61. Pang MY, Yang JF (2000) The initiation of the swing phase in human infant stepping: importance of hip position and leg loading. J Physiol 528 Pt 2: 389-404.
62. Orlovsky GN, Deliagina TG, Grillner S, Orlovskii GN, Grillner S (1999) Neuronal control of locomotion: from mollusc to man. Oxford, UK: Oxford University Press. 322 p.
63. Mori S, Kawahara K, Sakamoto T, Aoki M, Tomiyama T (1982) Setting and resetting of level of postural muscle tone in decerebrate cat by stimulation of brain stem. J Neurophysiol 48: 737-748. (Pubitemid 12064698)
64. Ivanenko YP, Wright WG, St George RJ, Gurfinkel VS (2013) Trunk orientation, stability, and quadrupedalism. Front Neurol 4: 20.
65. Edgerton VR, Courtine G, Gerasimenko YP, Lavrov I, Ichiyama RM, et al. (2008) Training Locomotor Networks. Brain Res Rev 57: 241-254. (Pubitemid 350213107)
66. Delwaide PJ, Toulouse P (1981) Facilitation of monosynaptic reflexes by voluntary contraction of muscle in remote parts of the body. Mechanisms involved in the Jendrassik Manoeuvre. Brain J Neurol 104: 701-709.
67. Nardone A, Schieppati M (2008) Inhibitory effect of the Jendrassik maneuver on the stretch reflex. Neuroscience 156: 607-617.
68. Crenna P, Carpinella I, Lopiano L, Marzegan A, Rabuffetti M, et al. (2008) Influence of basal ganglia on upper limb locomotor synergies. Evidence from deep brain stimulation and l-DOPA treatment in Parkinson's disease. Brain 131: 3410-3420.
69. Debaere F, Assche DV, Kiekens C, Verschueren S, Swinnen S (2001) Coordination of upper and lower limb segments: deficits on the ipsilesional side after unilateral stroke. Exp Brain Res 141: 519-529. (Pubitemid 33145109)
70. Meyns P, Van Gestel L, Bruijn SM, Desloovere K, Swinnen SP, et al. (2012) Is interlimb coordination during walking preserved in children with cerebral palsy? Res Dev Disabil 33: 1418-1428.