Behavior of spinal neurons deprived of supraspinal input

Nature Reviews Neurology - Tập 6 Số 3 - Trang 167-174 - 2010
Volker Dietz1
1Spinal Cord Injury Center, Balgrist University Hospital, Zurich, Switzerland

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Schwab, M. E. & Bartholdi, D. Degeneration and regeneration of axons in the lesioned spinal cord. Physiol. Rev. 76, 319–370 (1996).

Raineteau, O. & Schwab, M. E. Plasticity of motor systems after incomplete spinal cord injury. Nat. Rev. Neurosci. 2, 263–273 (2001).

Deumens, R., Koopmans, G. C. & Joosten, E. A. Regeneration of descending axon tracts after spinal cord injury. Prog. Neurobiol. 77, 57–89 (2005).

Dietz, V. & Curt, A. Neurological aspects of spinal-cord repair: promises and challenges. Lancet Neurol. 5, 688–694 (2006).

Raisman, G. A promising therapeutic approach to spinal cord repair. J. R. Soc. Med. 96, 259–261 (2003).

Barnett, S. C. & Chang, L. Olfactory ensheathing cells and CNS repair: going solo or in need of a friend? Trends Neurosci. 27, 54–60 (2004).

Li, Y., Field, P. M. & Raisman, G. Repair of adult rat corticospinal tract by transplants of olfactory ensheathing cells. Science 277, 2000–2002 (1997).

Ramón-Cueto, A., Cordero, M. I., Santos-Benito, F. F. & Avila, J. Functional recovery of paraplegic rats and motor axon regeneration in their spinal cords by olfactory ensheathing glia. Neuron 25, 425–435 (2000).

Mackay-Sim, A. et al. Autologous olfactory ensheathing cell transplantation in human paraplegia: a 3-year clinical trial. Brain 131, 2376–2386 (2008).

Curt, A. & Dietz, V. Controversial treatments for spinal-cord injuries. Lancet 365, 841 (2005).

Dobkin, B. H., Curt, A. & Guest, J. Cellular transplants in China: observational study from the largest human experiment in chronic spinal cord injury. Neurorehabil. Neural Repair 20, 5–13 (2006).

Dietz, V. Ready for human spinal cord repair? Brain 131, 2240–2242 (2008).

Houle, J. D. & Tessler, A. Repair of chronic spinal cord injury. Exp. Neurol. 182, 247–260 (2003).

Ye, J. H. & Houle, J. D. Treatment of the chronically injured spinal cord with neurotrophic factors can promote axonal regeneration from supraspinal neurons. Exp. Neurol. 143, 70–81 (1997).

Karimi-Abdolrezaee, S., Eftekharpour, E., Wang, J., Morshead, C. M. & Fehlings, M. G. Delayed transplantation of adult neural precursor cells promotes remyelination and functional neurological recovery after spinal cord injury. J. Neurosci. 26, 3377–3389 (2006).

Nomura, H. et al. Delayed implantation of intramedullary chitosan channels containing nerve grafts promotes extensive axonal regeneration after spinal cord injury. Neurosurgery 63, 127–141 (2008).

Klapka, N. et al. Suppression of fibrous scarring in spinal cord injury of rat promotes long-distance regeneration of corticospinal tract axons, rescue of primary motoneurons in somatosensory cortex and significant functional recovery. Eur. J. Neurosci. 22, 3047–3058 (2005).

Guest, J. D., Hiester, E. D. & Bunge, R. P. Demyelination and Schwann cell responses adjacent to injury epicenter cavities following chronic human spinal cord injury. Exp. Neurol. 192, 384–393 (2005).

Dietz, V., Grillner, S., Trepp, A., Hubli, M. & Bolliger, M. Changes in spinal reflex and locomotor activity after a complete spinal cord injury: a common mechanism? Brain 132, 2196–2205 (2009).

Dietz, V. & Müller, R. Degradation of neuronal function following a spinal cord injury: mechanisms and countermeasures. Brain 127, 2221–2231 (2004).

Curt, A., Alkadhi, H., Crelier, G. R., Boendermaker, S. H., Hepp-Reymond, M. C. & Kollias, S. S. Changes of non-affected upper limb cortical representation in paraplegic patients as assessed by fMRI. Brain 125, 2567–2578 (2002).

Halder, P. et al. Preserved aspects of cortical foot control in paraplegia. Neuroimage 31, 692–698 (2006).

Hotz-Boendermaker, S. et al. Preservation of motor programs in paraplegics as demonstrated by attempted and imagined foot movements. Neuroimage 39, 383–394 (2008).

Dietz, V., Colombo, G., Jensen, L. & Baumgartner, L. Locomotor capacity of spinal cord in paraplegic patients. Ann. Neurol. 37, 574–582 (1995).

Dietz, V., Müller, R. & Colombo, G. Locomotor activity in spinal man: significance of afferent input from joint and load receptors. Brain 125, 2626–2634 (2002).

Dobkin, B. H., Harkema, S., Requejo, P. & Edgerton, V. R. Modulation of locomotor-like EMG activity in subjects with complete and incomplete spinal cord injury. J. Neurol. Rehab. 9, 183–190 (1995).

Harkema, S. J. et al. Human lumbosacral spinal cord interprets loading during stepping. J. Neurophysiol. 77, 797–811 (1997).

Andersson, O. & Grillner, S. Peripheral control of the cat's step cycle. II. Entrainment of the central pattern generators for locomotion by sinusoidal hip movements during “fictive locomotion”. Acta Physiol. Scand. 118, 229–239 (1983).

Duysens, J. & Pearson, K. G. Inhibition of flexor burst generation by loading ankle extensor muscles in walking cats. Brain Res. 187, 321–332 (1980).

Pearson, K. G. Proprioceptive regulation of locomotion. Curr. Opin. Neurobiol. 5, 786–791 (1995).

Andersen, O. K., Finnerup, N. B., Spaich, E. G., Jensen, T. S. & Arendt-Nielsen, L. Expansion of nociceptive withdrawal reflex receptive fields in spinal cord injured humans. Clin. Neurophysiol. 115, 2798–2810 (2004).

Hornby, T. G., Rymer, W. Z., Benz, E. N. & Schmit, B. D. Windup of flexion reflexes in chronic human spinal cord injury: a marker for neuronal plateau potentials? J. Neurophysiol. 89, 416–426 (2003).

Conway, B. A. & Knikou, M. The action of plantar pressure on flexion reflex pathways in the isolated human spinal cord. Clin. Neurophysiol. 119, 892–896 (2008).

Schmit, B. D., McKenna-Cole, A. & Rymer, W. Z. Flexor reflexes in chronic spinal cord injury triggered by imposed ankle rotation. Muscle Nerve 23, 793–803 (2000).

Hiersemenzel, L. P., Curt, A. & Dietz, V. From spinal shock to spasticity: neuronal adaptations to a spinal cord injury. Neurology 54, 1574–1582 (2000).

Lavrov, I. et al. Plasticity of spinal cord reflexes after a complete transection in adult rats: relationship to stepping ability. J. Neurophysiol. 96, 1699–1710 (2006).

Valero-Cabré, A., Forés, J. & Navarro, X. Reorganization of reflex responses mediated by different afferent sensory fibers after spinal cord transection. J. Neurophysiol. 91, 2838–2848 (2004).

Jankowska, E., Jukes, M. G., Lund, S. & Lundberg, A. The effect of DOPA on the spinal cord. 6. Half-centre organization of interneurones transmitting effects from the flexor reflex afferents. Acta Physiol. Scand. 70, 389–402 (1967).

Forssberg, H. & Grillner, S. The locomotion of the acute spinal cat injected with clonidine i.v. Brain Res. 50, 184–186 (1973).

Grillner, S. & Zangger, P. On the central generation of locomotion in the low spinal cat. Exp. Brain Res. 34, 241–261 (1979).

Jones, C. A. & Yang, J. F. Reflex behavior during walking in incomplete spinal-cord-injured subjects. Exp. Neurol. 128, 239–248 (1994).

Dietz, V., Quintern, J. & Berger, W. Electrophysiological studies of gait in spasticity and rigidity. Evidence that altered mechanical properties of muscle contribute to hypertonia. Brain 104, 431–449 (1981).

O'Dwyer, N. J., Ada, L. & Neilson, P. D. Spasticity and muscle contracture following stroke. Brain 119, 1737–1749 (1996).

Ibrahim, I. K., Berger, W., Trippel, M. & Dietz, V. Stretch-induced electromyographic activity and torque in spastic elbow muscles. Brain 116, 971–989 (1993).

Lieber, R. L. & Fridén, J. Spasticity causes a fundamental rearrangement of muscle−joint interaction. Muscle Nerve 25, 265–270 (2002).

Dietz, V. & Sinkjaer, T. Spastic movement disorder: impaired reflex function and altered muscle mechanics. Lancet Neurol. 6, 725–733 (2007).

Bennett, D. J., Sanelli, L., Cooke, C. L., Harvey, P. J. & Gorassini, M. A. Spastic long-lasting reflexes in the awake rat after sacral spinal cord injury. J. Neurophysiol. 91, 2247–2258 (2004).

Li, X., Murray, K., Harvey, P. J., Ballou, E. W. & Bennett, D. J. Serotonin facilitates a persistent calcium current in motoneurons of rats with and without chronic spinal cord injury. J. Neurophysiol. 97, 1236–1246 (2007).

Li, Y., Gorassini, M. A. & Bennett, D. J. Role of persistent sodium and calcium currents in motoneuron firing and spasticity in chronic spinal rats. J. Neurophysiol. 91, 767–783 (2004).

Kitzman, P. Alteration in axial motoneuronal morphology in the spinal cord injured spastic rat. Exp. Neurol. 192, 100–108 (2005).

Kitzman, P. Changes in vesicular glutamate transporter 2, vesicular GABA transporter and vesicular acetylcholine transporter labeling of sacrocaudal motoneurons in the spastic rat. Exp. Neurol. 197, 407–419 (2006).

Kakinohana, O. et al. Development of GABA-sensitive spasticity and rigidity in rats after transient spinal cord ischemia: a qualitative and quantitative electrophysiological and histopathological study. Neuroscience 141, 1569–1583 (2006).

Hultborn, H. Changes in neuronal properties and spinal reflexes during development of spasticity following spinal cord lesions and stroke: studies in animal models and patients. J. Rehabil. Med. 35, 46–55 (2003).

Müller, R. & Dietz, V. Neuronal function in chronic spinal cord injury: divergence between locomotor and flexion- and H-reflex activity. Clin. Neurophysiol. 117, 1499–1507 (2006).

Valero-Cabré, A. & Navarro, X. Changes in crossed spinal reflexes after peripheral nerve injury and repair. J. Neurophysiol. 87, 1763–1771 (2002).

de Leon, R. D., Hodgson, J. A., Roy, R. R. & Edgerton, V. R. Locomotor capacity attributable to step training versus spontaneous recovery after spinalization in adult cats. J. Neurophysiol. 79, 1329–1340 (1998).

Edgerton, V. R., de Leon, R. D., Tillakaratne, N., Recktenwald, M. R., Hodgson, J. A. & Roy, R. R. Use-dependent plasticity in spinal stepping and standing. Adv. Neurol. 72, 233–247 (1997).

Hains, B. C., Willis, W. D. & Hulsebosch, C. E. Temporal plasticity of dorsal horn somatosensory neurons after acute and chronic spinal cord hemisection in rat. Brain Res. 970, 238–241 (2003).

García-Alías, G., Barkhuysen, S., Buckle, M. & Fawcett, J. W. Chondroitinase ABC treatment opens a window of opportunity for task-specific rehabilitation. Nat. Neurosci. 12, 1145–1151 (2009).

Edgerton, V. R., de Leon, R. D., Tillakaratne, N., Recktenwald, M. R., Hodgson, J. A. & Roy, R. R. Use-dependent plasticity in spinal stepping and standing. Adv. Neurol. 72, 233–247 (1997).

Dietz, V. Proprioception and locomotor disorders. Nat. Rev. Neurosci. 3, 781–790 (2002).

Maier, I. C. et al. Differential effects of anti-Nogo-A antibody treatment and treadmill training in rats with incomplete spinal cord injury. Brain 132, 1426–1440 (2009).

Dietz, V. Human neuronal control of automatic functional movements: interaction between central programs and afferent input. Physiol. Rev. 72, 33–69 (1992).

Burns, A. S., Lemay, M. A. & Tessler, A. Abnormal spontaneous potentials in distal muscles in animal models of spinal cord injury. Muscle Nerve 31, 46–51 (2005).

Ginsberg, S. D. & Martin, L. J. Axonal transection in adult rat brain induces transsynaptic apoptosis and persistent atrophy of target neurons. J. Neurotrauma 19, 99–109 (2002).

Wu, Y. P. & Ling, E. A. Transsynaptic changes of neurons and associated microglial reaction in the spinal cord of rats following middle cerebral artery occlusion. Neurosci. Lett. 256, 41–44 (1998).

Aisen, M. L., Brown, W. & Rubin, M. Electrophysiologic changes in lumbar spinal cord after cervical cord injury. Neurology 42, 623–626 (1992).

Chang, C. W. Evident transsynaptic degeneration of motor neurons after spinal cord injury: a study of neuromuscular jitter by axonal microstimulation. Am. J. Phys. Med. Rehabil. 77, 118–121 (1998).

Lin, C. S., Macefield, V. G., Elam, M., Wallin, B. G., Engel, S. & Kiernan, M. C. Axonal changes in spinal cord injured patients distal to the site of injury. Brain 130, 985–994 (2007).

Nyboer, V. J. & Johnson, H. E. Electromyographic findings in lower extremities of patients with traumatic quadriplegia. Arch. Phys. Med. Rehabil. 52, 256–259 (1971).

Hara, Y., Akaboshi, K., Masakado, Y. & Chino, N. Physiologic decrease of single thenar motor units in the F-response in stroke patients. Arch. Phys. Med. Rehabil. 81, 418–423 (2000).

Lukacs, M., Vecsei, L. & Beniczky, S. Changes in muscle fiber density following a stroke. Clin. Neurophysiol. 120, 1539–1542 (2009).

Hansen, N. L. et al. Reduction of common synaptic drive to ankle dorsiflexor motoneurons during walking in patients with spinal cord lesion. J. Neurophysiol. 94, 934–942 (2005).

Grillner, S. et al. Neural networks that co-ordinate locomotion and body orientation in lamprey. Trends Neurosci. 18, 270–279 (1995).

DeAngelis, G. C., Ohzawa, I. & Freeman, R. D. Receptive-field dynamics in the central visual pathways. Trends Neurosci. 18, 451–458 (1995).

Tillakaratne, N. J. et al. Use-dependent modulation of inhibitory capacity in the feline lumbar spinal cord. J. Neurosci. 22, 3130–3143 (2002).

Ichiyama, R. M., Broman, J., Edgerton, V. R. & Havton, L. A. Ultrastructural synaptic features differ between alpha- and gamma-motoneurons innervating the tibialis anterior muscle in the rat. J. Comp. Neurol. 499, 306–315 (2006).

de Leon, R. D., Tamaki, H., Hodgson, J. A., Roy, R. R. & Edgerton, V. R. Hindlimb locomotor and postural training modulates glycinergic inhibition in the spinal cord of the adult spinal cat. J. Neurophysiol. 82, 359–369 (1999).

Wirz, M. et al. Effectiveness of automated locomotor training in patients with chronic incomplete spinal cord injury: a multicenter trial. Arch. Phys. Med. Rehabil. 86, 672–680 (2005).

Courtine, G. et al. Recovery of supraspinal control of stepping via indirect propriospinal relay connections after spinal cord injury. Nat. Med. 14, 69–74 (2008).

Courtine, G. et al. Transformation of nonfunctional spinal circuits into functional states after the loss of brain input. Nat. Neurosci. 12, 1333–1342 (2009).

Milanov, I. G. Flexor reflex for assessment of common interneurone activity in spasticity. Electromyogr. Clin. Neurophysiol. 32, 621–629 (1992).

Dietz, V. Do human bipeds use quadrupedal coordination? Trends Neurosci. 25, 462–467 (2002).

Dietz, V., Fouad, K. & Bastiaanse, C. M. Neuronal coordination of arm and leg movements during human locomotion. Eur. J. Neurosci. 14, 1906–1914 (2001).

Michel, J., van Hedel, H. J. & Dietz, V. Obstacle stepping involves spinal anticipatory activity associated with quadrupedal limb coordination. Eur. J. Neurosci. 27, 1867–1875 (2008).

Zehr, E. P., Hesketh, K. L. & Chua, R. Differential regulation of cutaneous and H-reflexes during leg cycling in humans. J. Neurophysiol. 85, 1178–1184 (2001).

Zehr, E. P. & Kido, A. Neural control of rhythmic, cyclical human arm movement: task dependency, nerve specificity and phase modulation of cutaneous reflexes. J. Physiol. 537, 1033–1045 (2001).

Calancie, B., Alexeeva, N., Broton, J. G. & Molano, M. R. Interlimb reflex activity after spinal cord injury in man: strengthening response patterns are consistent with ongoing synaptic plasticity. Clin. Neurophysiol. 116, 75–86 (2005).

Bussel, B., Roby-Brami, A., Yakovleff, A. & Bennis, N. Late flexion reflex in paraplegic patients. Evidence for a spinal stepping generator. Brain Res. Bull. 22, 53–56 (1989).

Pierrot-Deseilligny, E. & Burke, D. The Circuitry of Human Spinal Cord. Its Role in Motor Control and Movement Disorders (Cambridge University Press, Cambridge, 2005).