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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.

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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.

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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.

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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.

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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

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