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  • Review Article
  • Published:

The motor infrastructure: from ion channels to neuronal networks

Key Points

  • The motor system is the only external output channel of the brain. Various networks at different levels of the nervous system coordinate a multitude of motor patterns, such as eye or hand movements, or those that underlie respiration, locomotion or posture. Together, these networks provide a 'motor infrastructure' that is used by the nervous system to generate the movement repertoire of an organism or a species. Some networks are present at birth, whereas others mature during development to become modified and perfected through learning.

  • Whereas the presence of networks coordinating movements has long been established, the intrinsic function of these networks in vertebrates has only recently started to be unravelled. The lamprey locomotor network is one of the few vertebrate networks that is well understood.

  • The basic burst-generating core of the network consists of populations of glutamatergic excitatory interneurons, which excite each other through NMDA (N-methyl-D-aspartate) and AMPA (α-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid) receptors. They also activate a group of motor neurons and glycinergic neurons that inhibit antagonistic burst-generating populations. This organization results in alternating activity in groups of motor neurons.

  • Burst generation and termination in a population is determined by the background excitatory drive and the different ion channel subtypes that are expressed. Ca2+- and voltage-activated ion channels, such as Ca2+-dependent K+ channels, NMDA receptors, Ca2+ channel subtypes and K+ channels (Kv3), have an important role. A sensory overlay can also influence burst onset and termination. Local inhibitory interneurons with ipsilateral axons are not required for burst generation but might, under some conditions, influence burst termination.

  • G-protein-coupled receptors contribute to the fine tuning of the network activity, although they need not be activated for burst generation to occur. Some modulator/transmitter neurons are activated as part of the network operation (acting through 5-HT (5-hydroxytryptamine, serotonin), GABA (γ-aminobutyric acid) and metabotropic glutamate receptors), whereas others provide an independent input (including 5-HT, cholecystokinin and peptide YY(PYY)). They act by modulating different subtypes of ion channels in the soma, or by modifying synaptic efficacy at the pre- or postsynaptic level. For example, tachykinins can produce short or long-term changes.

  • The detailed analysis of the network has been possible through extensive modelling at the ion channel, cell, network and neuromechanical levels in close interaction with the experimental analyses.

  • Vertebrate locomotion, whether swimming, walking or flying, requires a complex motor pattern involving hundreds of muscles, controlled through brainstem command centres that regulate the level of activity in spinal cord networks, which generate the detailed pattern of muscle activity. The neural control system has been remarkably well conserved through vertebrate evolution.

Abstract

The vertebrate motor system is equipped with a number of neuronal networks that underlie different patterns of behaviour, from simple protective reflexes to complex movements. The current challenge is to understand the intrinsic function of these networks: that is, the cellular basis of motor behaviour. In one vertebrate model system, the lamprey, it has been possible to make the connection between different subtypes of ion channels and transmitters and their roles at the cellular and network levels. It is therefore possible to link the role of certain genes or molecules to motor behaviour in this system.

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Figure 1: The motor infrastructure.
Figure 2: Similarities of locomotor pattern generation in an intact lamprey and an isolated spinal cord.
Figure 3: Locomotor network of the lamprey.
Figure 4: The roles of the slow afterhyperpolarization (sAHP) and KCa channels at the single cell and network level.
Figure 5: Factors controlling burst onset and termination.
Figure 6: Modelling the lamprey locomotor network.
Figure 7: Effects on the central pattern generator (CPG) of sensory input from stretch receptors activated during the movement.
Figure 8: Intersegmental coordination in the lamprey.

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Acknowledgements

I would like to acknowledge The Swedish Research Council, European Union and the Wallenberg Foundations for continuous support, and P. Wallén, A. El Manira and R. Hill for critical reading of the manuscript and for a stimulating and creative interaction over many years.

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FURTHER INFORMATION

Encyclopedia of Life Sciences

central pattern generators

motor neurons and spinal control of movement

motor system organization

Glossary

CENTRAL PATTERN GENERATOR

A neural circuit that produces patterns of behaviour independently of sensory input, for instance the pattern of activity in different motor neurons that results in respiration or locomotion.

SACCADIC EYE MOVEMENTS

A rapid eye movement (with speeds of up to 800 degrees per second) that brings the point of maximal visual acuity — the fovea — to the image of interest.

DIENCEPHALIC LOCOMOTOR REGION

Area corresponding to ventral thalamus, which contains neurons that project to reticulospinal neurons, and that thereby can activate the spinal locomotor networks.

MESOPONTINE LOCOMOTOR REGION

Area located at the border between mesencephalon and pons (mesopontine), which contains neurons that project to reticulospinal neurons, and thereby can activate the spinal locomotor networks. This area is often referred to as the mesencephalic locomotor region.

VENTRAL THALAMUS

Nucleus in diencephalon that sends axonal glutamatergic projections to reticulospinal neurons, thereby eliciting locomotor activity. Ventral thalamus should not be confused with the dorsal thalamus, which projects to pallium (corresponding to cortex) as in mammals.

SPIKE-FREQUENCY ADAPTATION

A decrease in the rate of action potentials fired by a neuron under prolonged depolarization.

LEAK CURRENT

Ionic current produced by ion channels that are open at resting membrane potential. They are usually voltage insensitive and often permeable to K+.

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Grillner, S. The motor infrastructure: from ion channels to neuronal networks. Nat Rev Neurosci 4, 573–586 (2003). https://doi.org/10.1038/nrn1137

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