Synchronous cortical oscillatory activity during motor action
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.
References (59)
- et al.
Oscillatory interaction between human motor cortex and trunk muscles during isometric contraction
Neuroimage
(2001) - et al.
Electrocorticogram-electromyogram coherence during isometric contraction of hand muscle in human
Clin Neurophysiol
(2000) - et al.
Synchronization in monkey motor cortex during a precision grip task. II. Effect of oscillatory activity on corticospinal output
J Neurophysiol
(2003) - et al.
Synchrony between neurons with similar muscle fields in monkey motor cortex
Neuron
(2003) - et al.
Modulation of cortex-muscle oscillatory interaction by ischaemia-induced deafferentation
Neuroreport
(2003) - et al.
Gamma oscillation by synaptic inhibition in a hippocampal interneuronal network model
J Neurosci
(1996) - et al.
Involvement of the sensorimotor cortex in physiological force and action tremor
Neuroreport
(2001) - et al.
Tremor-correlated cortical activity in essential tremor
Lancet
(2001) - et al.
Dopamine dependency of oscillations between subthalamic nucleus and pallidum in Parkinson’s disease
J Neurosci
(2001) - et al.
Intermuscular coherence in Parkinson’s disease: effects of subthalamic nucleus stimulation
Neuroreport
(2001)
Abnormal corticomuscular and intermuscular coupling in high-frequency rhythmic myoclonus
Brain
Phase relationships between cortical and muscle oscillations in cortical myoclonus: electrocorticographic assessment in a single case
Clin Neurophysiol
Rhythmical corticomotor communication
Neuroreport
Corticomuscular coherence: a review
J Clin Neurophysiol
The frequency content of common synaptic inputs to motoneurones studied during voluntary isometric contraction in man
J Physiol
Changes in motor unit synchronization following central nervous lesions in man
J Physiol
Synchronization between motor cortex and spinal motoneuronal pool during the performance of a maintained motor task in man
J Physiol
Cortical control of human motoneuron firing during isometric contraction
J Neurophysiol
Coherent oscillations in monkey motor cortex and hand muscle EMG show task-dependent modulation
J Physiol
Three-dimensional integration of brain anatomy and function to facilitate intraoperative navigation around the sensorimotor strip
Hum Brain Mapp
Organization of cortical activities related to movement in humans
J Neurosci
Increased synchronization of cortical oscillatory activities between human supplementary motor and primary sensorimotor areas during voluntary movements
J Neurosci
Coherence between cerebellar thalamus, cortex and muscle in man: cerebellar thalamus interactions
Brain
The neural basis of intermittent motor control in humans
Proc Natl Acad Sci USA
The cerebral oscillatory network of parkinsonian resting tremor
Brain
Synchronization tomography: a method for three-dimensional localization of phase synchronized neuronal populations in the human brain using magnetoencephalography
Phys Rev Lett
Cortical correlate of the Piper rhythm in humans
J Neurophysiol
Cortico-muscular synchronization during isometric muscle contraction in humans as revealed by magnetoencephalography
J Physiol
Information flow from the sensorimotor cortex to muscle in humans
Clin Neurophysiol
Cited by (168)
Diverse beta burst waveform motifs characterize movement-related cortical dynamics
2023, Progress in NeurobiologyTemporal profiles of cortical oscillations in novice performers for goal-directed aiming in a shooting task
2023, Biological PsychologyDisrupted cortico-peripheral interactions in motor disorders
2021, Clinical Neurophysiology