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Intermanual coordination: From behavioural principles to neural-network interactions

Key Points

  • What are the rules that govern interlimb and intermanual coordination? Temporal and spatial parameters constrain the coordination of limb movements, reflecting a basic synchronization tendency. But this tendency can be overcome, indicating the existence of plastic changes that are associated with skill learning.

  • Spatial constraints on interlimb coordination become apparent when drawing lines of different amplitude or orientation with each hand. In such cases, the movement of one hand interferes with that of the other, presumably by the exchange of information through the corpus callosum. Similarly, temporal constraints become apparent when performing movements with each hand at different frequencies, as a similar interference is observed.

  • The acquisition of new coordination patterns should be considered against the background of default coordination modes. In other words, the learning of new coordination patterns must overcome the intruding nature of the pre-existing patterns and the tendency towards phase and frequency synchronization.

  • Two frameworks have provided the theoretical foundations for the principles of interlimb coordination. Dynamic pattern theory aims for a mathematical formalization of the coordination principles, modelling rhythmic movements as a system of coupled nonlinear oscillators. Neural crosstalk argues that interactions occur between command streams within a highly linked neural medium, giving rise to patterns of mutual interference between concurrent limb motions at different stages of movement. Although both perspectives have developed independently, they are not necessarily incompatible.

  • The prevailing approach to the neural basis of intermanual coordination is to allocate it to a single locus — the supplementary motor area. But recent evidence points to a more distributed network that includes regions such as the primary sensory and motor cortices, the premotor area and the cingulate motor area. The distributed nature of this network accounts for disruptions of interlimb coordination in several movement disorders.

  • Many questions still remain unresolved in the field of interlimb coordination, such as establishing the specific roles of the different brain areas that constitute the distributed network, and the balance between neuronal excitation and inhibition in the generation of movement patterns.

Abstract

Locomotion in vertebrates and invertebrates has a long history in research as the most prominent example of interlimb coordination. However, the evolution towards upright stance and gait has paved the way for a bewildering variety of functions in which the upper limbs interact with each other in a context-specific manner. The neural basis of these bimanual interactions has been investigated in recent years on different scales, ranging from the single-cell level to the analysis of neuronal assemblies. Although the prevailing viewpoint has been to assign bimanual coordination to a single brain locus, more recent evidence points to a distributed network that governs the processes of neural synchronization and desynchronization that underlie the rich variety of coordinated functions. The distributed nature of this network accounts for disruptions of interlimb coordination across various movement disorders.

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Figure 1: Basic coordination constraints: the egocentric and allocentric principles.
Figure 2: Differences in directional interference in a patient with resections of the corpus callosum, before and after surgery.
Figure 3: Patterns of directional interference within egocentric workspace.
Figure 4: Performance of the 90° out-of-phase task during 1:1 frequency locking.
Figure 5: Techniques that are used to study the neural basis of interlimb coordination.

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Acknowledgements

Support for the present study was provided by a grant from the Research Council of Katholieke Universiteit Leuven, Belgium, and by the Flanders Fund for Scientific Research. The comments of M. Wiesendanger, D. J. Serrien, N. Wenderoth, F. Debaere and J. Duysens on a previous draft of the manuscript are highly appreciated.

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DATABASES

OMIM

Huntington's disease

Parkinson's disease

FURTHER INFORMATION

Encyclopedia of Life Sciences

bipedalism

central pattern generators

locomotion

nervous control of movement

Sherrington, Charles Scott

Glossary

CENTRAL PATTERN GENERATOR

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

NEAR-INFRARED SPECTROSCOPY

A form of optical imaging that uses arrays of lasers and detectors to measure changes in the absorption of near-infrared light caused by neural activation.

TOURETTE'S SYNDROME

A rare disorder that is thought to be caused by abnormalities of the basal ganglia. It is characterized by facial and vocal tics, and less frequently by verbal profanities.

EFFERENCE COPY

A copy of the motor command that is sent back to the central nervous system to inform it of the executed movement.

LOCAL FIELD POTENTIAL

The summated electrical current in the vicinity of the recording electrode — current that is generated by a large population of neurons.

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Swinnen, S. Intermanual coordination: From behavioural principles to neural-network interactions. Nat Rev Neurosci 3, 348–359 (2002). https://doi.org/10.1038/nrn807

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