Synchronous cortical oscillatory activity during motor action

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Abstract

Oscillations of the motor cortex interact with similar activity of the spinal motoneuron pool in the 15–30 Hertz frequency range. Recent observations have demonstrated how this interaction affects the firing of single corticospinal neurons. The interaction, reflected as corticomuscular coherence, occurs for both distal and proximal muscles and it constitutes one connection in a larger web of oscillatory interactions, including several other motor areas in the cortex, thalamus, and cerebellum. New results cast light on the possible functional significance of this interaction. The rhythmic interaction may reveal interesting information in several motor disorders, including essential tremor, Parkinson’s disease, myoclonus epilepsy, and mirror movements.

Introduction

Oscillatory activity in the motor areas of the human central nervous system (CNS) is particularly prominent in the primary sensorimotor area, where activities of around 20 and 10 Hz can be seen, especially during rest. The finding that the 20-Hz activity can be expressed in similar oscillatory activity in the spinal motoneurons (Figure 1) has recently attracted widespread interest (for earlier reviews see Hari and Salenius [1] and Mima and Hallett [2]). The connection between central and peripheral motor rhythms began to be elucidated by studies of synchronisation of single motor units in different muscles 3., 4., but the first direct demonstration of an oscillatory cortex–muscle interaction was provided by magnetoencephalography (MEG) in 1995 [5]. Since then, a growing number of studies have probed the details of this connection, both in healthy subjects and in various patient groups. The detailed mechanism of the interaction (here, for simplicity, called corticomuscular interaction or coherence) has been successfully studied in animal experiments, but why and how the interaction arises is still partly enigmatic. Here, we discuss recent findings that spread light on the topography, mechanism, modulation and function of corticomuscular rhythmic interaction.

Section snippets

The topography of an oscillating motor network

The interactions of rhythms between the motor cortex and the spinal motoneurons have been investigated mainly for distal limb muscles, especially for hand muscles that have both a large representation in the motor cortex and a high number of direct corticospinal neurons (Figure 2). Still, rhythmic cortex–muscle interaction does also occur for proximal hand muscles [6], and even for paraspinal and abdominal muscles in the trunk. However, the coherence is weaker in trunk than it is in limb

Corticomuscular coherence — single neuron studies

The results of several studies, which apply different time-lag analyses, indicate that corticomuscular coherence around 20 Hz arises through the transmission of oscillatory activity from the (primary) motor cortex to the spinal motoneurons 6., 17., 18., 19., 20.. In macaque monkeys, the firing pattern of identified pyramidal tract neurons (PTNs) follows the rhythmic activity of the motor cortex, as reflected by local field potentials (LFPs) [8]. Synchrony between PTNs is strongest during the

Modulation of corticomuscular coherence

The strength of motor rhythms and of rhythmic interaction varies with variations in motor activity: corticomuscular coherence is typically strongest during static phases of a motor task and is reduced or abolished with the beginning of a movement. It is, however, still unclear to what extent the rhythmic interaction depends on sensory input. Two studies have recently probed this question by inducing temporary deafferentation. Fisher et al. [25] measured coherence between EMGs from different

Corticomuscular coherence: functional significance

Interaction between peripheral and central motor rhythms does not serve any obvious purpose in the intricate flow of events that shape and constitute the planning and execution of motor tasks. For example, corticomuscular coherence may be minimal in healthy subjects who possess excellent motor skills. Despite that, the epiphenomenon interpretation of the corticomuscular coherence has been challenged.

During a hold-ramp-hold task (see Figure 3c for a schematic of the task), corticomuscular

Physiological and essential tremor

Although spectral analysis of the normal EMG typically reveals rhythmic activity, this activity is not necessarily reflected in mechanical oscillations of the limbs. Such mechanical oscillations may, however, occur both in normal subjects 14.••, 38. and in various motor disorders.

Physiological tremor consists of at least two components: one generated by mechanical oscillations reflecting the limbs’ resonance frequency, and another (in the 6–15 Hz range), putatively originating from the CNS. This

Conclusions

The recent focus on rhythmic cortical activity in the exploration of motor function has revealed a web of oscillatory connections, not only between the periphery and the centre of the CNS but also within the brain. The oscillatory connections appear frequency specific and exhibit systematic modulatory patterns related to the patterns of motor output and sensory input. The rhythmic interaction is often consistently changed in motor disorders, thereby revealing interesting features of motor

References and recommended reading

Papers of particular interest, published within the annual period of review, have been highlighted as:

  • of special interest

  • ••

    of outstanding interest

Acknowledgements

Supported by the Academy of Finland.

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