Gait apraxia after bilateral supplementary motor area lesion

OBJECTIVES: The study aimed at addressing the issue of the precise nature of gait apraxia and the cerebral dysfunction responsible for it. METHODS: The case of a patient, affected by a bilateral infarction limited to a portion of the anterior cerebral artery territory is reported. The patient's ability to walk was formally assessed by means of a new standardised test. RESULTS: Due to an anomaly within the anterior cerebral artery system, the patient's lesion was centred on the supplementary motor regions of both hemispheres. He presented with clear signs of gait apraxia that could not be accounted for by paresis or other neurological deficits. No signs of any other form of apraxia were detected. CONCLUSIONS: The clinical profile of the patient and the analysis of 49 cases from previous literature suggest that gait apraxia should be considered a clinical entity in its own right and lesions to the supplementary motor areas are responsible for it.     

Apraxia and the supplementary motor area

Anatomical, electrophysiological, and cerebral blood flow studies suggest that the supplementary motor area (SMA) may be important for programming certain skilled motor acts of the limbs. However, to our knowledge, abnormalities of complex distal motor behavior following SMA lesions have not been reported. We have studied two patients with left mesial hemisphere infarctions that included the SMA. These patients had bilateral ideomotor apraxia for transitive limb movements without buccofacial apraxia. The observations suggest that the types of skilled motor acts programmed by the left SMA are learned transitive limb movements.     

Foot, face and hand representation in the human supplementary motor area

The ability to localize the limb representation in the supplementary motor area (SMA) would be useful in planning surgical ablation of medial frontal lobe tumours. We investigated the relationship between the anatomy of the SMA and the functional representation of fingers, toes, and lips using fMRI in healthy volunteers. There was a significant difference between the location of the different body parts in the SMA, with a rostro-caudal location of the face, hand and foot areas. Limb representation was located in an area spanning < 1 cm rostral and 1 cm caudal to the paracentral sulcus. These results support the somatotopic organization of the human SMA and suggest that the paracentral sulcus represents a landmark for body representation.     

Ictal SPECT in supplementary motor area seizures

OBJECTIVES: We used ictal single photon emission computed tomography (SPECT) to clarify the propagation pathways of epileptic discharges in patients with supplementary motor area (SMA) seizure. METHODS: In four patients (four males, age range, 18-27 years) with SMA seizures, SPECT studies by radioisotope 99mTc-ECD were performed as a preoperative evaluation. Two of the patients remained seizure-free after complete resection of the focal cortical dysplasia on magnetic resonance (MR) images including epileptic foci. In the other two patients, MR images were normal, but subdural electrode monitoring allowed for verifying the ictal onset in the left SMA. After partial resection of the SMA including epileptic foci, these patients experienced a significant (>90%) reduction of seizure frequency. Regional cerebral blood flow (rCBF) measurements obtained under ictal and interictal conditions were compared on a voxel-by-voxel basis by means of the SPM99 paired t-test option (uncorrected p<0.001). RESULTS: Significant increases in rCBF under ictal conditions were identified in the bilateral anterior cingulate cortex (ACC), the globus pallidus ipsilateral to epileptic foci and the contralateral cerebellar hemisphere. The right ACC included a cluster with a submaximum in the right primary sensorimotor area. DISCUSSION: In patients with SMA seizures, the hyperperfusion areas of ictal SPECT did not localize within the SMA but spread to the adjacent cortex such as the ACC and sensorimotor cortex ipsilateral to epileptic foci. Additionally, the epileptic discharges propagated to the remote areas such as the globus pallidus and cerebellum. We caution that ictal SPECT localization in patients with SMA seizures is not always concordant to epileptic focus but reveals already spread seizure activities.     

Ictal SPECT in supplementary motor area seizures

Abstract

Objectives: We used ictal single photon emission computed tomography (SPECT) to clarify the propagation pathways of epileptic discharges in patients with supplementary motor area (SMA) seizure.

Methods: In four patients (four males, age range, 18–27 years) with SMA seizures, SPECT studies by radioisotope 99mTc-ECD were performed as a preoperative evaluation. Two of the patients remained seizure-free after complete resection of the focal cortical dysplasia on magnetic resonance (MR) images including epileptic foci. In the other two patients, MR images were normal, but subdural electrode monitoring allowed for verifying the ictal onset in the left SMA. After partial resection of the SMA including epileptic foci, these patients experienced a significant (>90%) reduction of seizure frequency. Regional cerebral blood flow (rCBF) measurements obtained under ictal and interictal conditions were compared on a voxel-by-voxel basis by means of the SPM99 paired t-test option (uncorrected p<0.001).

Results: Significant increases in rCBF under ictal conditions were identified in the bilateral anterior cingulate cortex (ACC), the globus pallidus ipsilateral to epileptic foci and the contralateral cerebellar hemisphere. The right ACC included a cluster with a submaximum in the right primary sensorimotor area.

Discussion: In patients with SMA seizures, the hyperperfusion areas of ictal SPECT did not localize within the SMA but spread to the adjacent cortex such as the ACC and sensorimotor cortex ipsilateral to epileptic foci. Additionally, the epileptic discharges propagated to the remote areas such as the globus pallidus and cerebellum. We caution that ictal SPECT localization in patients with SMA seizures is not always concordant to epileptic focus but reveals already spread seizure activities.     

Sensory motor mismatch within the supplementary motor area in the dystonic monkey

Dystonia, a movement disorder characterized by abnormal postures, is associated in primary forms of the disease with subtle proprioceptive troubles and aberrant somatotopic representation in the somatosensory cortex (SC). However, it is unclear whether these sensory features are a causal phenomenon or a consequence of dystonia. The supplementary motor area proper (SMAp), a premotor cortical region, receives strong inputs from both the SC and basal ganglia. We hypothesized that disruption in sensory-motor integration within the SMAp may play a part in the pathophysiology of dystonia. Using a model of secondary dystonia obtained by 3-nitropropionic acid intoxication in rhesus monkeys, we first provide evidence that the SMAp was overexcitable in dystonic animals. Second, we show that proprioceptive inputs processed by SMAp neurons were dramatically increased with wider sensory receptive fields and a mismatch between sensory inputs and motor outputs. These findings suggest that abnormal sensory inputs impinging upon SMAp neurons play a critical role in the pathophysiology of dystonia.     

The neuronal activity in the supplementary motor area of primates

The functional role of the supplementary motor area (SMA) has been largelyunknown for the 30 years since its definition. However, recent work employing the technique of single cell recording from behaving primates offers important clues as to how activity in this area takes part in controlling motor performance. Whereas SMA activity is not as related to execution of simple movements as that in the precentral motor cortex, SMA neurons respond strongly to motor instructions that determine the way animals have to respond to forthcoming sensory signals.     

Speech arrest and supplementary motor area seizures

A right-handed man had recurrent episodes of speech arrest that were focal epileptic seizures. A metastatic adenocarcinoma was identified and removed from the left supplementary motor area. The similarity of these rare seizures to transient ischemic attacks may lead to an erroneous and hazardous misdiagnosis.     

Role of the supplementary motor area in motor deficit following medial frontal lobe surgery

OBJECTIVE: Patients undergoing surgical resection of medial frontal lesions may present a transient postoperative deficit that remains largely unpredictable. The authors studied the role of the supplementary motor area (SMA) in the occurrence of this deficit using fMRI. METHODS: Twenty-three patients underwent a preoperative fMRI before resection of medial frontal lesions. Tasks included self-paced flexion/extension of the left and right hand, successively. Preoperative fMRI data were compared with postoperative MRI data and with neurologic outcome. RESULTS: Following surgery, 11 patients had a motor deficit from which all patients recovered within a few weeks or months. The deficit was similar across patients, consisting of a global reduction in spontaneous movements contralateral to the operated side with variable severity. SMA activation was observed in all patients. The deficit was observed when the area activated in the posterior part of the SMA (SMA proper) was resected. CONCLUSIONS: fMRI is able to identify the area at risk in the SMA proper whose resection is highly related to the occurrence of the motor deficit. The clinical characteristics of this deficit support the role of the SMA proper in the initiation and execution of the movement.     

Clinical consequences of corticectomies involving the supplementary motor area in man

Three patients with well-mapped, circumscribed ablations of the medial part of the frontal lobe are reported. A specific clinical evolution in 3 stages was observed: (1) post-operatively there was global akinesia, more prominent contralaterally, with an arrest of speech; (2) recovery occurred suddenly but even then there was severe reduction of spontaneous motor activity contralaterally, an emotional type facial palsy and a reduction of spontaneous speech; (3) long after the operation the only sequela was disturbance of the alternating movements of the hands. The anatomical basis of these disorders appears to be a lesion of the supplementary motor area (SMA). Three main points have been discussed, namely: (1) the nature of the motor disorder which may be a disturbance of the function of the SMA in initiating and sustaining spontaneous and automatic motor activity; (2) the nature of the arrest of speech which appears not to be aphasic; the studies reported in the present paper do not support a left cerebral dominance for the SMA as suggested by previous studies; (3) the method of clinical examination appears to be important in distinguishing between spontaneous and voluntary motor and speech performance. Differences in method may account for differences between our findings and those reported in previous studies.     

The efferent and afferent connections of the supplementary motor area

The efferent and afferent connections of the supplementary motor area (SMA) were studied in 6 squirrel monkeys using [3H]leucine and horseradish peroxidase, respectively. Efferent projections, common to all leucine-injected animals, were found to the cortical areas 9,8,44,4,2,5,7,24 and 23. Subcortically , efferents were found to the putamen, caudate nucleus, claustrum, the thalamic nuclei reticularis, ventrialis anterior, ventralis lateralis, medialis dorsalis, centralis lateralis, paracentralis , centrum medianum, parafascicularis, centralis superior lateralis, centralis inferior and lateralis posterior, the subthalamic nucleus, field H of Forel, nuel . ruber, reticular formation of midbrain, pons and medulla, the pontine gray and nucl . reticularis tegmenti pontis. Afferent connections exist with the cortical areas 9,8,6,44,4,1,2,5,7, 24 and 23, insula, fronto-parietal operculum and superior temporal sulcus. Subcortical afferent connections exist with the claustrum, nucleus of the diagonal band, nucl . basalis Meynert, basolateral amygdaloid nucleus, the thalamic nuclei ventralis anterior, ventralis lateralis, medialis dorsalis, centralis lateralis, paracentralis , centrum medianum, centralis superior lateralis, centralis inferior, lateralis posterior and pulvinaris , the posterior hypothalamus, ventral tegmental area, nucl . ruber pars parvicellularis , reticular formation of midbrain and pons, locus coeruleus and nucl . centralis superior Bechterew. The projections are discussed with respect to the possible role SMA plays in the voluntary initiation of motor actions.     

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     

The initiation of voluntary movements by the supplementary motor area

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 executed. 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.     

Non-paralytic motor disturbances and speech disorders: the role of the supplementary motor area

A right-handed patient with a lesion demonstrated by CT to involve the right medial frontal cortex is described. He exhibited a strong contralateral grasp reflex, motor perseveration and the presence of purposeful movements that appeared to be dissociated from conscious volition. In addition, there was a disorder of speech consisting of a lack of spontaneous speech production, with preserved ability to imitate. It is suggested that these disorders are due to damage to the supplementary motor area.     

Corticospinal and corticorubral projections from the supplementary motor area in the monkey

Neurons that were antidromically invaded from either pyramidal tract (PT) stimulation or red nucleus (RN) stimulation were studied in the anterior portion of the supplementary motor cortex of anaesthetized rhesus monkeys. The conduction velocity of 58 PT neurons ranged from 11 to 63 m/sec while those of the 29 RN neurons ranged from 10 to 38 m/sec. None of the neurons were found to be antidromically invaded from both stimulation sites. Thus, the corticorubral projection from the SMA does not appear to consist primarily of PT axon collaterals. There appeared to be a trend towards spatial segregation of the PT and RN neurons in the monkey cortex, the RN neurons tended to be located nearer the pial surface than the PT neurons, which tend to have somata nearer the subcortical while matter.     

Bereitschaftspotential in patients with unilateral lesions of the supplementary motor area.

In the present study, an attempt was made to examine the sensitivity of the Bereitschaftspotential (BP) preceding simple finger movement in revealing pathophysiological patterns of premovement cortical activity in patients with chronic unilateral lesions of the supplementary motor area (SMA). Usually, in healthy subjects, BP has a clear maximum in Cz with larger amplitudes than in Ccon (located over the motor cortex, contralateral to the performing hand). In the patients, amplitudes did not differ between Cz and Ccon. This effect of the lesion on BP topography, was found in movements of either side. However, intraindividual comparisons revealed that the reduction of the BP in Cz (relative to Ccon) was larger for movements contralateral to the SMA lesion than for those ipsilateral of it.