The initiation of voluntary movements by the supplementary motor area

Summary The hypothesis is formulated that in all voluntary movements the initial neuronal event is in the supplementary motor areas (SMA) of both cerebral hemispheres.Experimental support is provided by three lines of evidence. 1. In voluntary movements many neurones of the SMA are activated probably up to 200 ms before the pyramidal tract discharge. 2. Investigations of regional cerebral blood flow by the radioactive Xenon technique reveal that there is neuronal activity in the SMA of both sides during a continual series of voluntary movements, and that this even occurs when the movement is thought of, but not excuted. 3. With voluntary movement there is initiation of a slow negative potential (the readiness potential, RP) at up to 0.8 s before the movement. The RP is maximum over the vertex, i.e. above the SMA, and is large there even in bilateral Parkinsonism when it is negligible over the motor cortex.An account is given of the SMA, particularly its connectivities to the basal ganglia and the cerebellum that are active in the preprogramming of a movement. The concept of motor programs is described and related to the action of the SMA. It is proposed that each mental intention acts on the SMA in a specific manner and that the SMA has an inventory and the addresses of stored subroutines of all learnt motor programs. Thus by its neuronal connectivities the SMA is able to bring about the desired movement.There is a discussion of the manner in which the mental act of intention calls forth neural actions in the SMA that eventually lead to the intended movement. Explanation is given on the basis of the dualist-interactionist hypothesis of mind-brain liaison. The challenge is to the physicalists to account for the observed phenomena in voluntary movement.Dedicated to Prof. Richard Jung on the occasion of his 70th birthday     

Readiness potentials preceding spontaneous motor acts: voluntary vs. involuntary control.

Libet et al. (1983) developed a method to compare the onset time of a readiness potential (RP) with the onset time of the corresponding intention to perform a spontaneous voluntary motor act. In relation to the onset of the RP, the time of conscious intention to move followed 350 msec later. From these results Libet (1985) concluded that the cerebral initiation of a spontaneous voluntary act begins unconsciously. We investigated the alternative interpretation that with the instruction to pay attention to feelings of 'wanting to move,' automatic and normally unconscious motor acts might have been brought to a level of conscious awareness. Therefore we conducted 3 kinds of experiment. In the first, RPs were measured from subjects performing unconscious movements. The second experiment was a replication of Libet's study while the third was a resting condition in which subjects looked for intentions to move introspectively. The results showed that RPs beginning approximately 500 msec before movement onset can be obtained with unconsciously as well as consciously performed spontaneous motor acts. The different scalp distributions of the two types of RP indicate that unconscious movements can be attributed to the activation of a contralateral process (lateral premotor system (LPS), primary motor cortex), whereas voluntary spontaneous motor acts seemed to be predominated by the medial premotor system (MPS). It is proposed that in the Libet situation focused attention on internal events led to the conscious detection of a normally unconscious process. This resulted in the activation of the MPS, especially the supplementary motor area (SMA), which released the starting signal for the execution of the motor act. We believe that the activation of the SMA and the urge to move occurred at the same time.     

Gilles de la Tourette syndrome and voluntary movement: a functional MRI study

Tourette syndrome (TS) is hypothesised to be caused by an abnormal organization of movement control. The aim of this study was to use functional magnetic resonance imaging to study motor cortex activation in a TS patient. Usual and unusual self-paced voluntary movements were performed. The TS patient displayed supplementary motor area (SMA) activation during both tasks. This activation reflects a continuous use of the SMA to perform the voluntary motor movements required in both tasks. Moreover, the absence of tics during the execution of these voluntary motor tasks suggests that tic activity may be suppressed by additional mental effort.     

Activation of supplementary motor areas during voluntary movements in man studied by measurement of focal cerebral blood flow (author's transl)]

Focal activation in the cerebral cortex during different motility and language tests in 52 patients examined by arteriography was studied by measuring focal cerebral blood flow (fCBF) by means of an apparatus of high resolution. A sterotactic or functional approach demonstrated that the upper premotor activation previously noted in certain types of movement, corresponds to supplementary motor area (SMA). A retrospective study of 157 maps of fCBF recorded during motor or verbal behaviour, compared to 90 recordings in subjects at rest, showed that SMA is involved in most voluntary movements, either verbal or non-verbal. An analysis of the results suggests that SMA acts during the establishment of new motor programs, and in the control of pre-established automatic activities, in response to internal and external stimuli.     

The role of the supplementary motor area in externally timed movement: the influence of predictability of movement timing

A significant role in the planning and preparation for voluntary movement has been ascribed to secondary motor areas located on the medial wall of the cerebral hemispheres, and in particular to the supplementary motor area (SMA). Within the SMA, rostral and caudal subdivisions have been described, and differential roles have been attributed to these regions in relation to movement planning, preparation and execution. We have used functional magnetic resonance imaging (fMRI) to investigate the role of the SMA in the timing of movement execution, by recording the fMRI signal from mesial pre-motor areas and primary sensorimotor cortex (SM1) during the execution of a simple motor task externally cued at predictable (regular) and unpredictable (irregular) time intervals. The mean rate of movement was matched in both experiments. There was a greater activation of caudal than rostral SMA with both predictably and unpredictably cued movements, and a doubling of the signal when the timing of the motor response was unpredictable. In contrast, there was no difference in the activation of primary sensorimotor cortex with the two tasks. The data demonstrate that the caudal SMA has an important role in the execution of externally cued movements. The results also suggest a greater role for this region in the performance of unpredictably timed compared with predictably timed movements, however a model is proposed (based on electrophysiological data) which shows how the difference in functional signal in these two situations can be explained on the basis of a difference in the time course of neuronal activation in the SMA, rather than in the overall degree of activation.     

What is the Bereitschaftspotential?

Since discovery of the slow negative electroencephalographic (EEG) activity preceding self-initiated movement by Kornhuber and Deecke [Kornhuber HH, Deecke L. Hirnpotential?nderungen bei Willkurbewegungen und passiven Bewegungen des Menschen: Bereitschaftspotential und reafferente Potentiale. Pflugers Archiv 1965;284:1-17], various source localization techniques in normal subjects and epicortical recording in epilepsy patients have disclosed the generator mechanisms of each identifiable component of movement-related cortical potentials (MRCPs) to some extent. The initial slow segment of BP, called 'early BP' in this article, begins about 2 s before the movement onset in the pre-supplementary motor area (pre-SMA) with no site-specificity and in the SMA proper according to the somatotopic organization, and shortly thereafter in the lateral premotor cortex bilaterally with relatively clear somatotopy. About 400 ms before the movement onset, the steeper negative slope, called 'late BP' in this article (also referred to as NS'), occurs in the contralateral primary motor cortex (M1) and lateral premotor cortex with precise somatotopy. These two phases of BP are differentially influenced by various factors, especially by complexity of the movement which enhances only the late BP. Event-related desynchronization (ERD) of beta frequency EEG band before self-initiated movements shows a different temporospatial pattern from that of the BP, suggesting different neuronal mechanisms for the two. BP has been applied for investigating pathophysiology of various movement disorders. Volitional motor inhibition or muscle relaxation is preceded by BP quite similar to that preceding voluntary muscle contraction. Since BP of typical waveforms and temporospatial pattern does not occur before organic involuntary movements, BP is used for detecting the participation of the 'voluntary motor system' in the generation of apparently involuntary movements in patients with psychogenic movement disorders. In view of Libet et al.'s report [Libet B, Gleason CA, Wright EW, Pearl DK. Time of conscious intention to act in relation to onset of cerebral activity (readiness-potential). The unconscious initiation of a freely voluntary act. Brain 1983;106:623-642] that the awareness of intention to move occurred much later than the onset of BP, the early BP might reflect, physiologically, slowly increasing cortical excitability and, behaviorally, subconscious readiness for the forthcoming movement. Whether the late BP reflects conscious preparation for intended movement or not remains to be clarified.     

The Kugelberg lecture. Brain mechanisms of voluntary motor commands--a review.

At a time when both electrical and magnetic stimulation of the human brain are being used to assess cortical motor outflow in man, it is important to re-examine the organization of the motor areas of the cerebral cortex, the evidence which exists about the structures that are activated by epicortical stimulation, the nature of the projections from the cerebral cortex to lower motor centers, the physiological influences that are exerted on motoneurons and interneurons by these descending pathways and the relevance of all of these for the control of voluntary movement. This review examines the relationships of neuronal activities in some motor regions of the cerebral cortex to movement performance as revealed by recording of neuronal discharges during self-paced movements performed by conscious monkeys, and the relevance of these observations to the understanding of mechanisms of voluntary control of skilled movement performance in man. It documents detailed information about the precise connections made by descending cortico-motoneuronal fibers in the monkey and proposes a relationship between the analogous structural arrangements in man and the voluntary control of skilled movement. Comparison of some of the general propositions which derive from studies of cortico-motoneuronal commands in the monkey with the EMG results from magnetic stimulation in man leads to the suggestion that direct monosynaptic excitatory effects may be relevant to the control of both proximal and distal muscles in man. Electrical recordings of the neuronal activities of individual cells in strategic cytoarchitectonic areas of the monkey's cerebral cortex also provide a neurophysiological correlate of observations on regional cerebral blood flow and regional metabolism as these are studied in human subjects performing movement tasks. Hence it is possible to explain the involvement of supplementary motor areas of both hemispheres in the organization of the time-ordered commands for manual tasks. A deficit in bimanual coordination is evident in monkeys with a unilateral lesion of the supplementary motor area and this deficit mimics the disorder of voluntary control of bimanual manipulation reported in man.     

Impaired movement-related potentials in acute frontal traumatic brain injury.

OBJECTIVE: Focal brain lesions due to traumatic brain injury (TBI) do not only lead to functional deficits in the lesion area, but also disturb the structurally intact neuronal network connected to the lesion site. Therefore we hypothesized dysfunctions of the cortical motor network after frontal TBI. The movement related potential (MRP) is an EEG component related to voluntary movement consisting of the Bereitschaftspotential (BP), the negative slope (NS), and the motor potential (MP). The aim of our study was to demonstrate alterations in the movement related cortical network in the acute stage after TBI by comparing our patients' MRPs to those of a healthy control group. METHODS: EEGs of 22 patients with magnetic resonance imaging defined contusions of the prefrontal cortex were recorded within 8 weeks after TBI. We further recruited a healthy control group. The paradigm consisted of self-paced abductions of the right index finger. RESULTS: Compared to healthy controls, the BP in the patient group was significantly reduced and its onset delayed. Moreover, an enhanced contribution of the postrolandic hemisphere ipsilateral to the movement and a reduced contribution of the left frontal cortex, ipsilateral to the lesion in the majority of the patients, were observed during motor execution (MP). CONCLUSIONS: Anatomical connections between the prefrontal cortex and the supplementary motor area (SMA) are known to exist. We suggest that prefrontal lesions lead to reduced neuronal input into the SMA. This deficit in the preparatory motor network may cause the reduced BPs in our patients. Moreover, an increased need for attentional resources might explain the enhanced motor potentials during movement execution. In conclusion, we demonstrated altered MRPs in the acute stage after frontal TBI, which are a consequence of disturbed neuronal networks involved in the preparation and execution of voluntary movements.     

Simple and complex movements in a patient with infarction of the right supplementary motor area

The role played by the supplementary motor area (SMA) in the higher-level organization of motor behaviour (motor programming) has been highlighted by the study of cerebral blood flow during voluntary movements in normal humans. We present a detailed physiological investigation from a patient with a right SMA lesion and show that the right SMA plays a role in programming simultaneous and sequential movements in both arms, though the contralateral arm was the more severely impaired. In addition, we obtained evidence to suggest that the precentral motor cortex may be more responsive to peripheral perturbations when the modulating influence of the SMA is absent. In view of the similarity of the physiological findings in this subject to those in patients with Parkinson's disease, we suggest that the defect of motor programming in Parkinson's disease is likely to reflect functional deafferentation of the SMA.     

Cortex, basal ganglia and cerebellum in motor control.

For voluntary movement, function generators are necessary that are located in the brain-stem, cerebellum and basal ganglia. Following lesions of these generators, voluntary movements are impaired while stimulus-dependent movements are still possible. This discussion also applies to speech production. The motor function generators cooperate with the whole cerebral cortex since both tactical adaptation to the environment and strategic guidance by the motivation system contribute to voluntary action. The motor cortex plays an epicritical role, adding advanced tactile and proprioceptive guidance for those movements that need this kind of regulation, especially the fine finger movements which depend entirely on the motor cortex. The complexity of the cerebral potentials preceding voluntary movement corresponds to the activity of several motor subsystems acting in concert.     

Activation of Pre–Supplementary Motor Area (SMA) and SMA Proper During Unimanual and Bimanual Complex Sequences: An Analysis Using Functional Magnetic Resonance Imaging

Several functional imaging studies have shown that the extent of activation and percentage change in cerebral blood flow in the supplementary motor area (SMA) during a bimanual mirror performance of a simple repetitive movement are almost identical to those during a unimanual movement. The aim of this study was to investigate whether this finding was also applicable to a more complex movement. Eight right-handed, healthy volunteers performed unimanually (with their right and left hands) and bimanually (in a mirror fashion) thumb-finger opposition in a nonconsecutive order (index-middle-index-ring-index-little-index-middle ... fingers). The SMA proper was more activated during the bimanual movement than the unimanual movement with either hand. This is in accordance with the hypothesis that bimanual movement, even in a mirror fashion, is more difficult than unimanual movement when the task is complex but not when the task is simple. Pre-SMA was inconsistently activated. The results suggest that the SMA proper plays an active role in executive processing during bimanual mirror performance of complex movements.     

Neurophysiology of unimanual motor control and mirror movements.

In humans, execution of unimanual motor tasks requires a neural network that is capable of restricting neuronal motor output activity to the primary motor cortex (M1) contralateral to the voluntary movement by counteracting the default propensity to produce mirror-symmetrical bimanual movements. The motor command is transmitted from the M1 to the contralateral spinal motoneurons by a largely crossed system of fast-conducting corticospinal neurons. Alteration or even transient dysfunction of the neural circuits underlying movement lateralization may result in involuntary mirror movements (MM). Different models exist, which have attributed MM to unintended motor output from the M1 ipsilateral to the voluntary movement, functionally active uncrossed corticospinal projections, or on a combination of both. Over the last two decades, transcranial magnetic stimulation (TMS) proved as a valuable, non-invasive neurophysiological tool to investigate motor control in healthy volunteers and neurological patients. The contribution of TMS and other non-invasive electrophysiological techniques to characterize the neural network responsible for the so-called 'non-mirror transformation' of motor programs and the various mechanisms underlying 'physiological' mirroring, and congenital or acquired pathological MM are the focus of this review.     

Hemispherical asymmetry in human SMA during voluntary simple unilateral movements. An fMRI study

Functional magnetic resonance imaging (fMRI) was used to test the hypothesis of a prevailing role of left supplementary motor area (SMA) during voluntary right and left finger movements, in line with subjects' right hand preference. fMRI responses were quantified using task-related percent increase of the signal from statistically activated voxels in primary somatosensory (S1), primary motor (M1), and SMA cortical regions. Regional analysis comprised both extension and intensity of statistically activated groups of voxels. Results replicated previous fMRI evidence. Right M1 and S1 were much more activated during left rather than right movements, whereas such a difference was less evident in left M1 and S1. A novel finding consisted in an analogous functional hemispherical asymmetry in left and right SMA. Strikingly, left SMA activation did not differ statistically during right (contralateral) vs. left (ipsilateral) movements. It was concluded that, in right-handed subjects, left SMA plays a prevailing role in the control of voluntary movements.     

The role of motor cortex in the pathophysiology of voluntary movement deficits associated with parkinsonism.

The characteristic motor deficits of parkinsonism result from dysfunction of the nigrostriatal dopaminergic system of the basal ganglia. These subcortical deficits must ultimately be expressed at the cortical and spinal motoneuron levels to result in the difficulty with initiation and execution of movements seen in parkinsonism. This article describes the neuronal activity of two motor cortical regions, the primary motor cortex (MI) and supplementary motor area (SMA), which receive the majority of basal ganglia outputs related to movement control through the ventral lateral thalamus. The kinematics and electromyographic characteristics of stimulus-initiated and self-initiated normal and parkinsonian movements are described, and the possible relation of SMA and MI task-related neuronal activity to the parkinsonian movement deficits is reviewed.     

Human supplementary motor area: a role in voluntary movements and its clinical significance]

There were two hypotheses of functions of supplementary motor area (SMA): supplementary vs. supramotor, in 1980s. Clinically, SMA can develop a very intractable seizure focus characterized by unique ictal motor symptoms, and its dysfunction is also strongly related to the cardinal clinical features in patients with Parkinson's disease and dystonia. In patients with intractable partial seizures arising from the mesial frontal area who needed clinically chronic implantation of the subdural electrode grids for 1-2 weeks prior to the focus resection, we recorded movement-related cortical potentials or Bereitschaftspotentials (BPs) prior to the voluntary movements. As the results, 1) SMA proper, a caudal part of SMA showed a somatotopy of BP generators in accordance with each part of the voluntary movements in the body, 2) bilateral SMAs were involved in each side of the body movements equally, and the amplitude did not differ from one in the contralateral primary motor area (MI), and thus it proved that SMA proper played as a significant role in preparation for voluntary movements as MI. Furthermore, we clarified the functional significance of pre-SMA with regard to sensorimotor integration, decision making, repetitive rate of voluntary movements, voluntary motor inhibition and negative motor response. Clinically we also clarified the pathophysiology of SMA seizures, and impairment of SMA function in Parkinson's disease and dystonia. We look forward to clinical application of brain potentials from SMA in the field of brain-computer interface such as assessment and restorative approach in patients with spinal cord injury, paraplegia or motor neuron disease.     

Dipole source analysis suggests selective modulation of the supplementary motor area contribution to the readiness potential

The readiness potential preceding voluntary movement is modulated by the mode of movement selection, i.e. it has a higher amplitude preceding freely selected than before prescribed movements (Praamstra, P., Stegeman, D.F., Horstink, M.W.I.M., Brunia, C.H.M. and Cools, A.R. Movement-related potentials preceding voluntary movement are modulated by the mode of movement selection. Exp. Brain Res., 1995, 103: 429–439). One cortical area that is likely to be involved in this modulation is the supplementary motor area (SMA). Recent attempts to elucidate the neural generators of the readiness potential using spatiotemporal dipole source analysis, however, failed to establish a significant SMA contribution to the readiness potential. This might be explained by a failure of the proposed analyses to discriminate between SMA and motor cortex contributions to the readiness potential. We applied a dipole source analysis approach that better separates these overlapping source activities. The resulting source model includes an SMA source generating premovement activity consistent with evidence from intracranial recordings in humans. The SMA source accounts almost completely for the modulation of the readiness potential by different modes of movement selection. On the basis of these results, the relation between scalp-recorded movement-related activity, intracranially recorded potentials, and findings from functional imaging studies of voluntary movement, appears more transparent than suggested by previous dipole source analyses of premovement potentials.     

Delayed experience of volition in Gilles de la Tourette syndrome

Gilles de la Tourette's syndrome (TS) is a neuropsychiatric movement disorder characterised by the presence of multiple tics. Tics have an unusual, intermediate status between voluntary and involuntary movements. This ambiguity might involve not just a disorder of movement generation but also an abnormality of voluntary experience. Here the experience of voluntary movements in adult patients with TS is investigated and compared with healthy controls. A group of adult TS patients and age matched control participants estimated the time of conscious intention to perform a simple keypress movement and movement onset. Patients with TS showed a delayed experience of intention relative to controls whereas estimates of the actual movement onset were similar for patients and controls. These data suggest an abnormal experience of volition in patients with TS. Delayed volition could either be an additional intrinsic feature of the syndrome or it could reflect a cognitive strategy to limit motor excitability, and thus tic generation, during voluntary action.     

Movement-related potential measures of different modes of movement selection in Parkinson's disease

Movement-related potentials were recorded preceding self-paced voluntary movements in patients with Parkinson's disease and in healthy subjects of the same age group. We compared the Readiness Potential preceding joystick movements in a fixed direction and preceding joystick movements in freely selected directions. In normal subjects the Readiness Potential amplitude was higher preceding freely selected movements than preceding movements in a fixed direction. The Readiness Potential in Parkinson patients failed to be modified by the different modes of movement selection. The modulation of the Readiness Potential by different ways of preparing for movement might be due to the supplementary motor area (SMA) being more strongly engaged by tasks requiring internal control of movements than by tasks that are externally structured. The results suggest that this task-dependent variation of SMA activity is reduced in Parkinson's disease. A failing capacity to adapt SMA activity to different task demands has previously been suggested by evidence from positron emission tomography studies using similar tasks.     

Human supplementary motor area: a role in voluntary movements and its clinical significance]

Clinically, seizures from supplementary motor area (SMA) are characterized by asymmetric bilateral tonic posturing without loss of awareness, and its dysfunction is also strongly related to the clinical cardinal features in patients with Parkinson's disease and dystonia. By investigating Bereitschaftspotentials (BPs) from SMA, the following normal functions are elucidated. 1) SMA proper, a caudal part of SMA showed a somatotopy of BP generators in accordance with each part of the voluntary movements in the body, 2) bilateral SMAs were involved in each side of the body movements equally, and the amplitude did not differ from one in the contralateral primary motor area (MI), 3) pre-SMA was strongly related sensorimotor integration, decision making, repetitive rate of voluntary movements, voluntary motor inhibition and negative motor response. We look forward to clinical application of brain potentials from SMA in the field of brain-computer interface such as assessment and restorative approach in patients with spinal cord injury, paraplegia or motor neuron disease.     

The somatotopic organization of the supplementary motor area: intracortical microstimulation mapping

The somatotopic organization of the supplementary motor area (SMA) is commonly held to consist of a rostrocaudal sequence of orofacial, forelimb, and hindlimb representations. Recently, however, this somatotopy has been questioned. Studies of regional cerebral blood flow in humans and the movements evoked by intracortical electrical stimulation in cynomolgus monkeys have been unable to reveal evidence of distinct orofacial, forelimb, and hindlimb representations rostrocaudally situated along the medial cortex of the hemisphere. Partly on the basis of those results, it has been suggested that the SMA functions as a nontopographically organized "higher-order" motor center. The present study reexamines SMA organization by observing stimulation-evoked movements. The medial frontal cortex of 2 rhesus monkeys was mapped using a modified intracortical microstimulation technique. We observed a forelimb representation mainly on the medial surface of the hemisphere in both animals. Rostral or rostrolateral to the forelimb representation, depending on the individual, we evoked orofacial movements (including eye movements). Hindlimb movements were evoked from tissue overlapping, but largely caudal to, the forelimb representation. Thus, we conclude that there is a clear rostrocaudal progression of orofacial, forelimb, and hindlimb movement representations in the SMA.