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  • Review Article
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Proprioception and locomotor disorders

Key Points

  • Locomotion in mammals depends on central pattern generators — networks of spinal interneurons that can produce rhythmic outputs independently of any modulatory input. However, the spinal activity pattern is influenced by inputs from peripheral afferents, brainstem nuclei and cortical motor centres. Central pattern generators must select the appropriate inputs at each stage of movement and according to external conditions.

  • Afferent inputs that influence gait include the short-latency stretch reflex, which is mediated by excitatory monosynaptic connections between sensory fibres and motor neurons. This reflex is thought to compensate for small ground irregularities and is initiated when muscle stretch is detected by muscle spindles (the output of which is carried by type 1a fibres). The stretch reflex is modulated over the step cycle, with potential functional consequences.

  • Other afferent inputs, which mediate polysynaptic reflexes, converge on spinal interneurons, where they are integrated with descending information. The information from afferent receptors such as Golgi organs and skin mechanoceptors is carried by different fibre classes. Polysynaptic reflexes produce compensatory responses during locomotion that involve synergistic activation of muscle groups in both legs.

  • The polysynaptic reflex system probably integrates two important sources of afferent information: those related to load and to hip-joint position. In cats, either of these sources of afferent information can lead to entrainment of the rhythm or resetting of locomotor activity.

  • Understanding normal locomotion is essential for developing and applying therapeutic approaches to movement disorders. To achieve these goals, it is also necessary to distinguish between abnormalities caused by the primary lesion (for example, stroke) and those that arise from secondary, compensatory motor changes. In spasticity, for example, impaired supraspinal drive is partly compensated for by the development of spastic muscle tone.

  • The aim of rehabilitation should focus on an improvement of function by taking advantage of the plasticity of neuronal centres. It is more important to improve function than to correct isolated clinical signs. In addition, it is vital to develop consistent and meaningful clinical tests that assess function as well as (or instead of) isolated motor changes.

Abstract

Advances in our understanding of movement control allow us to define more precisely the requirements for the rehabilitation of patients with movement disorders. Most purposeful, complex movements are programmed in the central nervous system (CNS) and adapted by proprioceptive feedback. The selection of and interaction between different sources of afferent input is task dependent. Simple stretch reflexes are thought to be involved primarily in the control of focal movement. For more complex motor behaviours such as locomotion, afferent input related to load and hip-joint position probably has an important role in the proprioceptive contribution to the activation pattern of the leg muscles. There is increasing evidence that movement disorders such as spasticity and Parkinson's disease involve the defective use of afferent input in combination with secondary compensatory processes. This has implications for therapy, which should be directed to take advantage of the plasticity of the CNS.

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Figure 1: The stretch reflex of the calf muscles is differentially gated during locomotion.
Figure 2: Schematic drawing of the neuronal mechanisms involved in human gait.
Figure 3: Schematic of the mechanisms that contribute to spastic paresis and spastic movement disorder.
Figure 4: Data from three patients with incomplete paraplegia after spinal cord injury.

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Acknowledgements

I thank B. Gähwiler for helpful comments and R. Jurd for correcting the English. The Swiss National Science Foundation and the International Research Institute of Paraplegia supported this work.

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DATABASES

OMIM

Parkinson's disease

FURTHER INFORMATION

American Spinal Injury Association 

Encyclopedia of Life Sciences

bipedalism

central pattern generators

locomotion

motor system organization

nervous control of movement

proprioceptive sensory feedback

spinal reflexes

tetrapod walking and running

Volker Dietz's lab

Glossary

CENTRAL PATTERN GENERATOR

A neural circuit that produces self-sustaining patterns of behaviour independently of sensory input.

SPINALIZATION

Surgical separation of the spinal cord from the brain.

SPINAL STRETCH REFLEX

Also known as the short-latency reflex, this is the simplest reflex known. Muscle stretch is detected by muscle spindles, the afferent (Ia) fibres of which monosynaptically (and oligosynaptically) excite the motor neurons that innervate the same muscle, leading to muscle contraction.

H-REFLEX

Also known as the Hoffmann reflex. The H-reflex results from electrical stimulation of sensory (Ia) fibres, which arise from muscle spindles, leading (as in the spinal stretch reflex) to a monosynaptic excitation of motor neurons that innervate the same muscle.

DECEREBRATE

Describes an animal in which the spine and hindbrain have been isolated surgically from higher cortical inputs.

TRANSCRANIAL MAGNETIC STIMULATION

(TMS). A technique that is used to induce a transient interruption of normal activity in a relatively restricted area of the brain. It is based on the generation of a strong magnetic field near the area of interest, which, if changed rapidly enough, will induce an electric field that is sufficient to stimulate neurons.

DRIVEN GAIT ORTHOSIS

A motorized exoskeleton that is applied to the legs of a person with locomotor disorder — for example, paraplegia — and imposes physiological stepping movements.

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Dietz, V. Proprioception and locomotor disorders. Nat Rev Neurosci 3, 781–790 (2002). https://doi.org/10.1038/nrn939

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