Brain Advance Access originally published online on February 26, 2004
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Brain, Vol. 127, No. 5, 1019-1034, 2004
© 2004 Guarantors of Brain
doi: 10.1093/brain/awh115
Distributed plasticity of locomotor pattern generators in spinal cord injured patients
1 IRCCS Fondazione Santa Lucia, via Ardeatina 306, 00179 Rome, 2 Institute of Neurology, Catholic University, 00197 Rome, 3 Biomedical Engineering Laboratory, Istituto Superiore di Sanità, 00168 Rome and 4 Department of Neuroscience and Centre of Space Bio-medicine, University of Rome Tor Vergata, Via Montpellier 1, 00133 Rome, Italy
Correspondence to: Professor Francesco Lacquaniti, University of Rome Tor Vergata and IRCCS Fondazione Santa Lucia, via Ardeatina 306, 00179 Rome, Italy E-mail: lacquaniti{at}caspur.it Deceased
Recent progress with spinal cord injured (SCI) patients indicates that with training they can recover some locomotor ability. Here we addressed the question of whether locomotor responses developed with training depend on re-activation of the normal motor patterns or whether they depend on learning new motor patterns. To this end we recorded detailed kinematic and EMG data in SCI patients trained to step on a treadmill with body-weight support (BWST), and in healthy subjects. We found that all patients could be trained to step with BWST in the laboratory conditions, but they used new coordinative strategies. Patients with more severe lesions used their arms and body to assist the leg movements via the biomechanical coupling of limb and body segments. In all patients, the phase-relationship of the angular motion of the different lower limb segments was very different from the control, as was the pattern of activity of most recorded muscles. Surprisingly, however, the new motor strategies were quite effective in generating foot motion that closely matched the normal in the laboratory conditions. With training, foot motion recovered the shape, the step-by-step reproducibility, and the two-thirds power relationship between curvature and velocity that characterize normal gait. We mapped the recorded patterns of muscle activity onto the approximate rostrocaudal location of motor neuron pools in the human spinal cord. The reconstructed spatiotemporal maps of motor neuron activity in SCI patients were quite different from those of healthy subjects. At the end of training, the locomotor network reorganized at both supralesional and sublesional levels, from the cervical to the sacral cord segments. We conclude that locomotor responses in SCI patients may not be subserved by changes localized to limited regions of the spinal cord, but may depend on a plastic redistribution of activity across most of the rostrocaudal extent of the spinal cord. Distributed plasticity underlies recovery of foot kinematics by generating new patterns of muscle activity that are motor equivalents of the normal ones.
Key Words: human paraplegia; muscle synergies; motor equivalence; human locomotion; central pattern generators
Abbreviations: ASIA = American Spinal Injury Association; BF = long head of biceps femoris; BIC = biceps brachii; BWS = body weight support; BWST = body-weight-support on treadmill; CPG = central pattern generator; ES = erector spinae; GCL = gastrocnemius lateralis; GM = gluteus maximus; GT = greater trochanter; IL = ilium; LD = latissimus dorsi; LE = lateral femur epicondyle; LM = lateral malleolus; MAS = Modified Ashworth Scale; MN = motor neuron; OE = external oblique; OI = internal oblique; RAM = middle rectus abdominis; RAS = superior rectus abdominis; RF = rectus femoris; SCI = spinal cord injury; TA = tibialis anterior; TRAP = trapezius; TRIC = triceps brachii; VL = vastus lateralis; VM = fifth metatarso-phalangeal joint; VMA = normalized tolerance area of VM; WISCI = Walking Index for Spinal Cord Injury
Received October 14, 2003. Revised December 18, 2003. Accepted December 19, 2003.
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