Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

New perspectives on spinal motor systems

Key Points

  • Traditionally, the spinal cord is assigned a subservient role during the production of movement. This review challenges this idea by presenting evidence that the spinal cord is an active participant in complex functions of motor control.

  • Planning: In contrast to previous models, which suggest that the spinal cord only functions during the final execution of movement, recent experiments have shown that spinal cord neurons are also active during preparation for movement

  • Plasticity: Recent work indicates that spinal motor systems contribute to the functional plasticity of movement. Both the acquisition and expression of motor adaptation require an interaction between spinal and supraspinal systems.

  • Organization: Spinal motor systems have a high degree of organization, suggesting that supraspinal systems must take this organization into account when producing movement. A recent hypothesis is discussed that suggests that spinal motor systems are organized into a small number of behavioural subunits, or `spinal modules', that can be flexibly combined by supraspinal systems to produce a range of movements.

  • These new data are now prompting further investigations of the interaction between spinal and supraspinal systems, and their relative contributions to the complexities of movement.

Abstract

The production and control of complex motor functions are usually attributed to central brain structures such as cortex, basal ganglia and cerebellum. In traditional schemes the spinal cord is assigned a subservient function during the production of movement, playing a predominantly passive role by relaying the commands dictated to it by supraspinal systems. This review challenges this idea by presenting evidence that the spinal motor system is an active participant in several aspects of the production of movement, contributing to functions normally ascribed to `higher' brain regions.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: The involvement of spinal interneurons in the preparation for movement.
Figure 2: The process of motor adaptation following ankle extensor nerve cut.
Figure 3: The characterization of movements by the measurement of isometric force fields.
Figure 4: Summation of force fields by co-stimulation of sites in the frog spinal cord.

Similar content being viewed by others

References

  1. Maier, M. A., Perlmutter, S. I. & Fetz, E. E. Response patterns and force relations of monkey spinal interneurons during active wrist movement. J. Neurophysiol. 80, 2495–2513 (1998).

    Article  CAS  Google Scholar 

  2. Perlmutter, S. I., Maier, M. A. & Fetz, E. E. Activity of spinal interneurons and their effects on forearm muscles during voluntary wrist movements in the monkey. J. Neurophysiol. 80, 2475–2494 (1998).

    Article  CAS  Google Scholar 

  3. Prut, Y. & Fetz, E. E. Primate spinal interneurons show pre-movement instructed delay activity. Nature 401, 590–594 (1999).Describes a surprising result: during the planning phase of a limb movement, some spinal interneurons changed their firing rate — a fact indicating that the spinal cord is involved in movement preparation.

    Article  CAS  Google Scholar 

  4. Alexander, G. E. & Crutcher, M. D. Preparation for movement: neural representations of intended direction in three motor areas of the monkey. J. Neurophysiol. 64, 133–150 (1990).

    Article  CAS  Google Scholar 

  5. Kurata, K. Premotor cortex of monkeys: set- and movement-related activity reflecting amplitude and direction of wrist movement. J. Neurophysiol. 69, 187–200 (1993).

    Article  CAS  Google Scholar 

  6. Tanji, J. & Evarts, E. V. Anticipatory activity of motor cortex neurons in relation to direction of an intended movement. J. Neurophysiol. 39, 1062–1068 (1976).

    Article  CAS  Google Scholar 

  7. Georgopoulos, A. P., Crutcher, M. D. & Schwartz, A. B. Cognitive motor processes. III. motor cortical prediction of movement direction during an instructed delay period. Exp. Brain Res. 75, 183–194 ( 1989).

    Article  CAS  Google Scholar 

  8. Weinrich, M. & Wise, S. P. The premotor cortex of the monkey . J. Neurosci. 2, 1329– 1345 (1982).

    Article  CAS  Google Scholar 

  9. Alexander, G. E. Selective neuronal discharge in monkey putamen reflects intended direction of planned limb movements. Exp. Brain Res. 67, 623–634 (1987).

    Article  CAS  Google Scholar 

  10. Jankowska, E. Interneuronal relay in spinal pathways from proprioceptors. Prog. Neurobiol. 38, 335–378 ( 1992).

    Article  CAS  Google Scholar 

  11. Baldissera, F., Hultborn, H. & Illert, M. in Handbook of Physiology Vol. II The Nervous System (eds Brookhart, J. B. & Mountcastle, V. B.) 509–595 (American Physiological Society, Bethesda, 1981).

    Google Scholar 

  12. Bosco, G. & Poppele, R. E. Temporal features of directional tuning by spinocerebellar neurons: relation to limb geometry. J. Neurophysiol. 75, 1647–1658 (1996).

    Article  CAS  Google Scholar 

  13. Bosco, G. Poppele, R. E. & Eian, J. Reference frames for spinal proprioception: limb endpoint based or joint-level based? J. Neurophysiol. 83, 2931–2945 (2000).

    Article  CAS  Google Scholar 

  14. Bosco, G. & Poppele, R. E. Reference frames for spinal proprioception: kinematics based or kinetics based? J. Neurophysiol. 83, 2946–2955 (2000).

    Article  CAS  Google Scholar 

  15. Mussa-Ivaldi, F. A. Do neurons in the motor cortex encode movement direction? An alternative hypothesis . Neurosci. Lett. 15, 106– 111 (1988).

    Article  Google Scholar 

  16. Alstermark, B. & Lundberg, A. in Muscle Afferents and Spinal Control of Movement 327–359 (Oxford, New York: Pergamon Press, 1992).

    Google Scholar 

  17. Pierrot-Deseilligny, E. Transmission of the cortical command for human voluntary movement through cervical propriospinal premotoneurons. Prog. Neurobiol. 48, 489–517 (1996).

    Article  CAS  Google Scholar 

  18. Maier, M. A., Illert, M., Kirkwood, P. A., Nielsen, J. & Lemon, R. N. Does a C3–C4 propriospinal system transmit corticospinal excitation in the primate? An investigation in the macaque monkey. J. Physiol. (Lond.) 511, 191–212 (1998).

    Article  CAS  Google Scholar 

  19. Alstermark, B., Isa, T., Ohki, Y. & Saito, Y. Disynaptic pyramidal excitation in forelimb motoneurons mediated via C3–C4 propriospinal neurons in the macaca fuscata. J. Neurophysiol. 82, 3580–3585 (1999).

    Article  CAS  Google Scholar 

  20. Kawato, M. & Wolpert, D. Internal models for motor control . Novartis Found. Symp. 218, 291– 304 (1998).

    CAS  Google Scholar 

  21. Kawato, M. Internal models for motor control and trajectory planning. Curr. Opin. Neurobiol. 9, 718–727 (1999).

    Article  CAS  Google Scholar 

  22. Mussa-Ivaldi, F. A. Modular features of motor control and learning. Curr. Opin. Neurobiol. 9, 713–717 ( 1999).

    Article  CAS  Google Scholar 

  23. Kawato, M., Furukawa, K. & Suzuki, R. A hierarchical neural-network model for control and learning of voluntary movement. Biol. Cybern. 57, 169–185 (1987).

    Article  CAS  Google Scholar 

  24. Thoroughman, K. A. & Shadmehr, R. Electromyographic correlates of learning an internal model of reaching movements. J. Neurosci. 19, 8573–8588 (1999).

    Article  CAS  Google Scholar 

  25. Pearson, K. G. Neural adaptation in the generation of rhythmic behavior. Annu. Rev. Physiol. 62, 723–753 (2000).

    Article  CAS  Google Scholar 

  26. Whelan, P. J., Hiebert, G. W. & Pearson, K. G. Plasticity of the extensor group I pathway controlling the stance to swing transition in the cat. J. Neurophysiol. 74, 2782–2787 (1995).

    Article  CAS  Google Scholar 

  27. Whelan, P. J. & Pearson, K. G. Plasticity in reflex pathways controlling stepping in the cat. J. Neurophysiol. 78 , 1643–1650 (1997).

    Article  CAS  Google Scholar 

  28. Pearson, K. G., Fouad, K. & Misiaszek, J. E. Adaptive changes in motor activity associated with functional recovery following muscle denervation in walking cats. J. Neurophysiol. 82, 370–381 (1999).Describes the temporal evolution of changes in the muscle activation patterns during locomotion following nerve section in the cat, providing strong evidence for the updating of an internal model for limb movement.

    Article  CAS  Google Scholar 

  29. Fouad, K. & Pearson, K. G. Modification of group I field potentials in the intermediate nucleus of the cat spinal cord after chronic axotomy of an extensor nerve. Neurosci. Lett. 236, 9–12 (1997).

    Article  CAS  Google Scholar 

  30. Carrier L., Brustein E. & Rossignol, S. Locomotion of the hindlimbs after neurectomy of ankle flexors in intact and spinal cats: model for the study of locomotor plasticity . J. Neurophysiol. 77, 1979– 1993 (1997).Clearly illustrates the principle that functional motor adaptation to muscle denervation involves distributed plasticity across several regions of the nervous system, including the spinal cord.

    Article  CAS  Google Scholar 

  31. Rossignol, S. in Handbook of Physiology (eds Rowell, L. B. &. Sheperd, J. T.) 173–216 (American Physiological Society, Bethesda,1996).

    Google Scholar 

  32. Grillner, S. in Handbook of Physiology Vol. II (eds Brookhart, J. B. & Mountcastle, V. B) 1179–1236 (American Physiological Society, Bethesda, 1981).

    Google Scholar 

  33. Drew, T., Jiang, W., Kably, B. & Lavoie, S. Role of the motor cortex in the control of visually triggered gait modifications. Can. J. Physiol. Pharmacol. 74, 426– 442 (1996).

    CAS  PubMed  Google Scholar 

  34. Armstrong, D. M., Apps, R. & Marple-Horvat, D. E. Aspects of cerebellar function in relation to locomotor movements. Prog. Brain Res. 114, 401– 421 (1997).

    Article  CAS  Google Scholar 

  35. Wolpaw, J. R. Acquisition and maintenance of the simplest motor skill: investigation of CNS mechanisms. Med. Sci. Sports Exerc. 26, 1475–1479 (1994).

    Article  CAS  Google Scholar 

  36. Schouenborg, J., Holmberg, H. & Weng, H. R. Functional organization of the nociceptive withdrawal reflexes. II. changes of excitability and receptive fields after spinalization in the rat. Exp. Brain Res. 90, 469– 478 (1992).

    Article  CAS  Google Scholar 

  37. Schouenborg, J. & Weng, H. R. Sensorimotor transformation in a spinal motor system. Exp. Brain Res. 100, 170–174 (1994).

    Article  CAS  Google Scholar 

  38. Levinsson, A., Luo, X. L., Holmberg, H. & Schouenborg, J. Developmental tuning in a spinal nociceptive system: effects of neonatal spinalization. J. Neurosci. 19, 10397–10403 (1999).Demonstration that withdrawal reflexes, although ultimately supported by spinal systems, require an interaction between spinal and supraspinal systems during development for their normal expression.

    Article  CAS  Google Scholar 

  39. Holmberg, H. & Schouenborg, J. Developmental adaptation of withdrawal reflexes to early alteration of peripheral innervation in the rat . J. Physiol. (Lond.) 495, 399– 409 (1996).

    Article  Google Scholar 

  40. Holmberg, H., Schouenborg, J., Yu, Y. B. & Weng, H. R. Developmental adaptation of rat nociceptive withdrawal reflexes after neonatal tendon transfer. J. Neurosci. 17, 2071– 2078 (1997).

    Article  CAS  Google Scholar 

  41. Levinsson, A., Garwicz, M. & Schouenborg, J. Sensorimotor transformation in cat nociceptive withdrawal reflex system. Eur. J. Neurosci. 11, 4327 –4332 (1999).

    Article  CAS  Google Scholar 

  42. Stein, P. S. G. & Smith, J. L. in Neurons, Networks, and Motor Behavior (eds Stein, P. S. G., Grillner, S., Selverston, A. I. & Stuart, D. G.) 61–73 (MIT Press, Cambridge, Massachusetts, 1997).

    Google Scholar 

  43. Jordan, L. in Neurobiological Basis of Human Locomotion. (eds Shimamura, M., Grillner, S. & Edgerton, V. R.) 3–20 (Japan Scientific Societies, Tokyo, 1991).

    Google Scholar 

  44. Buford, J. A. & Smith, J. L. Adaptive control for backward quadrupedal walking. II. Hindlimb muscle synergies. J. Neurophysiol. 64, 756–766 (1990).

    Article  CAS  Google Scholar 

  45. Kiehn, O. & Kjaerulff, O. Spatiotemporal characteristics of 5-HT and dopamine-induced rhythmic hindlimb activity in the in vitro neonatal rat. J. Neurophysiol. 75, 1472–1482 (1996).

    Article  CAS  Google Scholar 

  46. Robertson, G. A., Mortin, L. I., Keifer, J. & Stein, P. S. G. Three forms of the scratch reflex in the spinal turtle: central generation of motor patterns. J. Neurophys. 53, 1517 –1534 (1985).

    Article  CAS  Google Scholar 

  47. Cheng, J. et al. Identification, localization, and modulation of neural networks for walking in the mudpuppy (Necturus maculatus) spinal cord. J. Neurosci. 18, 4295–4304 (1998).

    Article  CAS  Google Scholar 

  48. Bizzi, E., Mussa-Ivaldi, F. A. & Giszter, S. F. Computations underlying the production of movement: a biological perspective. Science 253, 287 –291 (1991).The authors identify a discrete map of motor outputs in the spinal cord. The vectorial combination of motor outputs derived from activation across different areas of the spinal cord provides a remarkable mechanism for producing a vast repertoire of motor behaviours.

    Article  CAS  Google Scholar 

  49. Bizzi, E., Giszter, S. F., Loeb, E., Mussa-Ivaldi, F. A. & Saltiel, P. Modular organization of motor behavior in the frog's spinal cord. Trends Neurosci. 18, 442– 446 (1995).

    Article  CAS  Google Scholar 

  50. Loeb, E. P., Giszter, S. F., Saltiel, P., Bizzi, E. & Mussa-Ivaldi, F. A. Outputs of motor behavior: an experimental and modeling study. J. Cogn. Neurosci. 12, 78–97 (2000).

    Article  CAS  Google Scholar 

  51. Giszter, S. F., Mussa-Ivaldi, F. A. & Bizzi, E. Convergent force fields organized in the frog's spinal cord. J. Neurosci. 13, 467– 491 (1993).

    Article  CAS  Google Scholar 

  52. Saltiel, P., Tresch, M. C. & Bizzi, E. Spinal cord modular organization and rhythm generation: an NMDA iontophoretic study in the frog. J. Neurophysiol. 80, 2323–2339 (1998). Tonic or rhythmically alternating forces elicited by chemical micro-stimulation of spinal interneurons cluster along the same few directions. The rhythms of specific force compositions are topographically related to the corresponding tonic forces. This suggests a use of the spinal cord modules in central pattern generation.

    Article  CAS  Google Scholar 

  53. Tresch, M. C. & Bizzi, E. Responses to spinal microstimulation in the chronically spinalized rat and their relationship to spinal systems activiated by low threshold cutaneous stimulation. Exp. Brain Res. 129, 401–416 ( 1999).

    Article  CAS  Google Scholar 

  54. Mussa-Ivaldi, F. A., Giszter, S. F. & Bizzi, E. Linear combinations of primitives in vertebrate motor control. Proc. Natl Acad. Sci. USA 91, 7534 –7538 (1994).

    Article  CAS  Google Scholar 

  55. Tresch, M. C., Saltiel, P. & Bizzi, E. The construction of movement by the spinal cord. Nature Neurosci. 2, 162–167 (1999).Uses a computational analysis to show that the production of withdrawal reflexes in the frog can be explained as the combination of a small number of spinally encoded muscle synergies.

    Article  CAS  Google Scholar 

  56. Kargo, W. & Giszter, S. F. Rapid correction of aimed movements by summation of force-field primitives. J. Neurosci. 20, 409–426 (2000). The hindlimb wipe reflex was reconstructed as a sequence of force field activations. Trajectory correction to an obstacle was accomplished by the superimposition of a further force field, which corresponds to the recruitment of a specific group of muscles whose activity co-varies according to obstacle parameters.

    Article  CAS  Google Scholar 

  57. d'Avella, A. & Bizzi, E. Low dimensionality of supraspinally induced force fields. Proc. Natl Acad. Sci. USA 95, 7711–7714 (1998).

    Article  CAS  Google Scholar 

  58. Pearson, K. G. & Collins, D. F. Reversal of the influence of group Ib afferents from plantaris on activity in medial gastrocnemius muscle during locomotor activity. J. Neurophysiol. 70, 1009–1017 (1993).

    Article  CAS  Google Scholar 

  59. Gossard, J. P., Brownstone, R. M., Barajon, I. & Hultborn, H. Transmission in a locomotor-related group Ib pathway from hindlimb extensor muscles in the cat. Exp. Brain Res. 98, 213–228 (1994).

    Article  CAS  Google Scholar 

  60. Guertin, P., Angel, M. J., Perreault, M. C. & McCrea, D. A. Ankle extensor group I afferents excite extensors throughout the hindlimb during fictive locomotion in the cat. J. Physiol. (Lond.) 487, 197–209 (1995).

    Article  CAS  Google Scholar 

  61. Angel, M. J., Guertin, P., Jimenez, T. & McCrea, D. A. Group I extensor afferents evoke disynaptic EPSPs in cat hindlimb extensor motorneurones during fictive locomotion. J. Physiol. (Lond.) 494, 851–861 (1996).

    Article  CAS  Google Scholar 

  62. McCrea, D. A. Neuronal basis of afferent-evoked enhancement of locomotor activity. Ann. NY Acad. Sci. 860, 216–225 (1998).

    Article  CAS  Google Scholar 

  63. Barbeau, H. et al. Tapping into spinal circuits to restore motor function. Brain Res. Rev. 30, 27–51 (1999).

    Article  CAS  Google Scholar 

  64. Barbeau, H. & Rossignol, S. Recovery of locomotion after chronic spinalization in the adult cat. Brain Res. 412, 84–95 (1987).

    Article  CAS  Google Scholar 

  65. Chau, C., Barbeau, H. & Rossignol, S. Early locomotor training with clonidine in spinal cats . J. Neurophysiol. 79, 392– 409 (1998).

    Article  CAS  Google Scholar 

  66. Chau, C., Barbeau, H. & Rossignol, S. Effects of intrathecal alpha1- and alpha2-noradrenergic agonists and norepinephrine on locomotion in chronic spinal cats. J. Neurophysiol. 79, 2941–2963 (1998).

    Article  CAS  Google Scholar 

  67. 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).

    Article  CAS  Google Scholar 

  68. De Leon, R. D., Hodgson, J. A., Roy, R. R. & Edgerton, V. R. Retention of hindlimb stepping ability in adult spinal cats after the cessation of step training. J. Neurophysiol. 81, 85 –94 (1999).

    Article  CAS  Google Scholar 

  69. Brustein, E. & Rossignol, S. Recovery of locomotion after ventral and ventrolateral spinal lesions in the cat. II. Effects of noradrenergic and serotoninergic drugs. J. Neurophysiol. 81, 1513–1530 (1999).

    Article  CAS  Google Scholar 

  70. Barbeau, H., Ladouceur, M., Norman, K. E., Pepin, A. & Leroux, A. Walking after spinal cord injury: evaluation, treatment, and functional recovery. Arch. Phys. Med. Rehabil. 80, 225–235 ( 1999).

    Article  CAS  Google Scholar 

  71. Behrman, A. L. & Harkema, S. J. Locomotor training after human spinal cord injury: A series of case studies. Phys. Ther. 80, 688–700 ( 2000).

    CAS  PubMed  Google Scholar 

  72. Wernig, A., Muller, S., Nanassy, A. & Cagol, E. Laufband therapy based on `rules of spinal locomotion' is effective in spinal cord injured persons. Eur. J. Neurosci. 7, 823– 829 (1995).

    Article  CAS  Google Scholar 

  73. Wernig, A., Nanassy, A. & Muller, S. Laufband (treadmill) therapy in incomplete paraplegia and tetraplegia. J. Neurotrauma 16, 719– 726 (1999).

    Article  CAS  Google Scholar 

  74. Mushahwar, V. K., Collins, D. F. & Prochazka, A. Spinal cord microstimulation generates functional limb movements in chronically implanted cats. Exp. Neurol. 163, 422–429 (2000).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We are grateful to Ole Kiehn for comments on an earlier version of this review. Work in the Bizzi laboratory is supported by the NIH.

Author information

Authors and Affiliations

Authors

Related links

Related links

ENCYCLOPEDIA OF LIFE SCIENCES

Motor neurons and spinal control of movement

Glossary

INTERNAL MODEL

A representation used by the nervous system to account for the properties of the motor apparatus and the environment. Such properties could include features of the limbs, such as their lengths and their masses, and could also include features of an object to be manipulated.

SET-RELATED ACTIVITY

Neuronal activity that reflects the behavioural `set' of the animal, which can include information about a planned movement or about the state of readiness of the animal.

PARALYSED DECEREBRATE PREPARATIONS

Eliminates movement of the animal. This mechanical stabilization can be accomplished by the application of paralytic agents. This paralysis is often accompanied by a precollicular decerebration in which all brain regions rostral to the superior colliculus are removed.

SUPRASPINAL SYSTEMS

The many regions of the brain that interact with the spinal cord. These systems either receive sensory information from the spinal cord or transmit information to the spinal cord.

DORSAL SPINOCEREBELLAR TRACT

A system of neurons located within the spinal cord, which receive, among other information, sensory information from muscle afferents in the limb and transmit this information to the cerebellum.

VISUALLY GUIDED REACHING

Movements of the arm that are regulated by visual feedback of the target and of the limb.

GLYCINE-MEDIATED INHIBITION

In the spinal cord, neuronal inhibition is largely mediated by the neurotransmitter glycine. This inhibition can be blocked by the neuroconvulsant strychnine.

MOTOR PERTURBATION

A procedure that results in the disturbance of the normal characteristics of movement. Such perturbations could be induced by the application of a torque pulse during the movement, an alteration in the visual feedback from the limb, or the denervation of a muscle.

KINEMATIC AND DYNAMIC PROPERTIES

Kinematic properties describe the visible aspects of the limb, such as the length of the links, the angles of the joints, or the position of the hand. Dynamic properties describe the forces and torques produced that underlie visible movement.

FEEDFORWARD ANTICIPATORY ACTIVATION

A movement or muscle activation pattern that corrects for a predicted perturbation before the actual perturbation. This is in contrast to a feedback activation which is a response to the sensory signals resulting from the perturbation.

SPINALIZATION

A surgical separation of the spinal cord from the rest of the brain.

SPINAL INTERNEURONAL SYSTEMS

The set of neurons within the spinal cord that are involved in processing information transmitted to the spinal cord, either from the periphery or from supraspinal systems.

UNIT BURST GENERATORS

Grillner's hypothesis for the spinal production of behaviour. Each spinal `unit' is proposed to control a small set of synergist muscles acting around specific joints, which can be coupled in many ways to produce a range of rhythmic behaviours.

WIPING REFLEX

The scratch reflex in the frog in which an irritant is removed from different regions of the body by limb movements that `wipe' the irritant off the skin.

VESTIBULAR STIMULATION

The vestibular system senses changes in head orientation, which are produced by head movements or changes in the position of the head with respect to gravity.

PRINCIPLE COMPONENTS

A computational analysis that can be used to assess the dimensionality of a data set.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bizzi, E., Tresch, M., Saltiel, P. et al. New perspectives on spinal motor systems. Nat Rev Neurosci 1, 101–108 (2000). https://doi.org/10.1038/35039000

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1038/35039000

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing