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.     

Reorganization of the motor cortex in a patient with congenital hemiparesis and mirror movements

Abnormal branching of corticospinal fibers from the unaffected motor cortex is responsible for mirror movements in patients with congenital hemiparesis, but it is unknown which mechanisms enable these patients to lateralize motor activity. Using multiunit electromyographic analysis and transcranial magnetic stimulation, the authors provide evidence for nonbranched crossed and uncrossed corticospinal projections and intracortical inhibition of the mirror hand. They propose that this remarkable reorganization of the unaffected motor cortex helps these patients to reduce mirror movements.     

Central motor pathways in patients with mirror movements.

Central motor pathways were investigated in three patients with congenital mirror movements using magnetic motor cortex stimulation. Response thresholds, amplitudes and latencies were normal. The projection of the corticomotoneuronal pathways was assessed by placing the coil over the vertex and comparing the size of responses in the first dorsal interosseous (FDI) muscles evoked by anticlockwise and clockwise [corrected] coil currents. In normal subjects, right FDI responses are larger with anticlockwise currents than with clockwise [corrected] currents at the same stimulation strength and vice versa. In two out of three patients with congenital mirror movements, this sensitivity of response amplitude to coil current direction was reversed. The third patient with congenital mirror movements and a fourth patient with acquired mirror movements had responses which were normally sensitive to current direction. These findings support the hypothesis that some cases of congenital mirror movements may be due to abnormal projection of corticomotoneuronal pathways.     

Congenital mirror movements: a clue to understanding bimanual motor control

Mirror movements (MM) are involuntary movements of one side of the body that accompany and mirror intentional movements on the opposite side. Physiological MM can occur during normal childhood development, probably owing to corpus callosum immaturity. Pathological congenital MM may be clinically isolated or part of a complex congenital syndrome, including Kallmann syndrome, Klippel-Feil syndrome, and congenital hemiplegia. Congenital isolated MM are usually familial. Recently, heterozygous mutations of the DCC gene, with autosomal dominant inheritance, were shown to cause some cases of MM. The pathogenesis of congenital MM may involve (i) abnormal interhemispheric inhibition between the two motor cortices; (ii) functional alteration of motor planning and motor execution; and/or (iii) abnormal persistence of the ipsilateral corticospinal tract. Fundamental and clinical research is providing novel insights into the complex underlying molecular pathways, and recent experimental work has identified several mechanisms that may mediate the motor network dysfunction. In this review, we analyze clinical, genetic, neurophysiologic, and neuroimaging data on congenital MM, and discuss how this knowledge may improve our understanding of bimanual motor control.     

Role of the ipsilateral motor cortex in mirror movements.

The mechanism of mirror movements in two patients was investigated; one with congenital mirror movement, the other with schizencephaly. Transcranial magnetic stimulation on one side elicited motor evoked potentials (MEPs) in their thenar muscles on both sides with almost the same latencies, minimal thresholds, and cortical topographies. During voluntary contraction of the thenar muscle on one side, contralateral transcranial magnetic stimulation induced a silent period not only on the voluntary contraction side but on the mirror movement side and of the same duration. By contrast, ipsilateral transcranial magnetic stimulation elicited MEPs without silent periods in both muscles. With intended unilateral finger movements, an H2(15)O-PET activation study showed that the regional cerebral blood flow increased predominantly in the contralateral sensorimotor cortex, as seen in normal subjects, although mirror movements occurred. It is considered that the ipsilateral motor cortex plays a major part in the generation of mirror movements, which may be induced through the ipsilateral uncrossed corticospinal tract.     

Bilateral mirror writing movements (mirror dystonia) in a patient with writer's cramp: functional correlates.

A recent prospective analysis on writer's cramp showed that up to 44.6% of patients in a series of 65 presented mirror dystonia, defined as involuntary movements of the resting hand, abnormal posture, tremor, and jerks occurring while writing with the opposite hand. A clinical case is presented, with videotape evidence of right-handed writer's cramp, with mirror movements elicited while writing using either hand. Functional magnetic resonance imaging studies are compared both to those of a normal patient and to those from a patient with writer's cramp but lacking mirror dystonia. Widespread bilateral activation of cortical motor areas contralateral to the mirror movements in patients with writer's cramp and mirror movements suggests, that bilateral activation of the primary motor cortex may account for the appearance of these mirror movements. Further studies need to be conducted to determine whether mirror movements in dystonic patients appear as a result of loss of intra- and/or interhemispheric cortical inhibition or are simply a consequence of the sustained effort these patients need to exert while writing using a dystonic hand.     

Concurrent bilateral projection and activation of motor cortices in a patient with congenital mirror movements: A TMS study

Objectives

Mirror movements (MMs) are unintended and unnecessary movements accompanying voluntary activity in homologous muscles on the opposite side of the body, particularly in distal arm muscles. Congenital MMs may be sporadic or familial. Several mechanisms have been proposed to explain persistent congenital MMs. Hypothesis 1 assumes the existence of an ipsilateral corticospinal pathway, and Hypothesis 2 the activation of both motor cortices. We report a new case of congenital mirror movements in a healthy woman.

Methods

Electromyographic recordings and focal transcranial magnetic stimulation (TMS) were used for neurophysiological evaluation.

Results

Voluntary contraction of either abductor pollicis brevis (APB) elicited mirror activation of the other APB. Focal TMS of either M1 elicited motor evoked potential (MEP) of normal latency and amplitude in both resting APB. TMS of the left cortex upon maximal contraction of the right APB and mirror contraction of the left APB produced interhemispheric inhibition (IHI) in the former and silent period (SP) in the later.

Conclusions

The electrophysiological evaluation using transcranial magnetic stimulation provides evidence of the concurrent action of both mechanisms in this patient.

Significance

The combination of more than one hypothesis could be more appropriate for understanding the underlying mechanism in some MM cases.     

Abnormal projection of corticospinal tracts in a patient with congenital mirror movements

A 31 year-old woman with familial congenital mirror movements not associated with other neurological defects underwent a detailed neurophysiological evaluation including: voluntary electromyographic activity recorded from upper limbs in response to acoustic stimuli, motor evoked potentials from the thenar muscles to focal transcranial magnetic stimulation, F waves from upper extremities, scalp somatosensory evoked potentials and long-latency responses from thenar muscles to electric stimulation of the median nerve. The results were consistent with the presence of fast-conducting pathways connecting each hand motor cortex with both contra- and ipsilateral spinal motoneurones.

Résumé

Une femme de 31 ans, qui présentait des mouvements « en miroird'origine familiale congénitale, en l'absence d'autres déficits neurologiques, a été soumise à une évaluation neurophysiologique détaillée comprenant: l'activité électromyographique (EMG) dans le muscle court abducteur du pouce en réponse à des stimulations auditives; les réponses EMG dans les muscles de l'éminence thénar par stimulation magnétique transcrânienne focale du cortex moteur; les potentiels évoqués somes-thésiques corticaux; les ondes F et les réponses EMG à longue latence dans l'éminence thénar par stimulation du nerf médian. Les résultats sont compatibles avec la présence de voies motrices à conduction rapide qui joignent l'aire de représentation de la main dans le cortex moteur primaire aux motoneurones spinaux aussi bien contralatéraux que ipsilatéraux.     

Bilateral motor cortex output with intended unimanual contraction in congenital mirror movements

In congenital mirror movements (MM), it is unclear whether the "mirror" motor cortex (M1) produces output during intended unimanual movements. In two patients with MM, the cortical silent period (CSP) was abnormally short after focal transcranial magnetic stimulation (TMS) of either M1, but simultaneous bilateral TMS led to significant CSP lengthening. Thus, it is likely that the shortened CSP after unilateral TMS is caused by output from the nonstimulated M1, suggesting that both M1 produce output with intended unimanual movements in patients with MM.     

Hand motor cortex activation in a patient with congenital mirror movements: a study of the silent period following focal transcranial magnetic stimulation

Motor evoked potentials (MEPs) to focal transcranial magnetic stimulation (TMS) have demonstrated that abnormal ipsilateral corticospinal projections are active in patients with congenital mirror movements. In addition, movement-related potentials and PET suggest that an abnormal pattern of motor cortex activation could be associated with an anomaly of the corticospinal tracts. In the present study the silent period (SP) following focal TMS was investigated in a woman with familial congenital mirror movements. Recordings were made from both the abductor pollicis brevis (APB) muscles. When focal TMS was delivered during an intended contralateral APB muscle contraction, MEP and SP were bilaterally recorded and SP was significantly shorter than the contralateral SP observed in normal controls. An abnormal bilateral activation of the hand motor cortex can explain our findings. The non-stimulated motor cortex causes an early partial recovery of the background EMG activity when the stimulated motor cortex is still inhibited (beginning as soon as the transcallosal and the short-lasting segmental inhibition are both complete.     

Congenital mirror movements.

In this report are described seven patients assessed clinically and neuropsychologically in whom mirror movements affecting predominantly the hands occurred as a congenital disorder. These mirror movements, representing a specific type of abnormal synkinesia, may arise as a hereditary condition, in the presence of a recognisable underlying neurological abnormality, and sporadically, and the seven patients provide more or less satisfactory examples of each of these three groups. Despite the apparent uniformity of the disorder, the heterogeneity and variability may be marked, examples in some of our patients including the pronounced increase in tone that developed with arm movement, and the capacity for modulation of the associated movement by alteration of neck position and bio-feedback. Various possible mechanisms are considered; these include impaired cerebral inhibition of unwanted movements, and functioning of abnormal motor pathways. Emphasis has been placed on the putative role of the direct, crossed corticomotoneurone pathways and on the unilateral and bilateral cerebral events that precede movement.     

Neurophysiological investigation of congenital mirror movements in a patient with agenesis of the corpus callosum

We describe a patient with complete agenesis of the corpus callosum and congenital mirror movements in which primary motor cortex (M1) excitability of both hemispheres was assessed with transcranial magnetic stimulation. Voluntary contraction of the index finger was associated with bilateral electromyographic activity in the first dorsal interosseus muscle. Motor-evoked potentials of identical latencies were produced bilaterally after unilateral M1 stimulation. Measures of intracortical inhibition and facilitation were within normal limits bilaterally although a shorter contralateral silent period was found for both hemispheres. Taken together, the current data suggest a pattern of M1 excitability very similar to that found in patients with congenital mirror movements and no other motor abnormality.     

Functional electrical stimulation in control of motor output and movements.

In patient with damaged upper motor neurones we show the therapeutic effect of electrical stimulation (called FES) of peripheral mixed nerves on the restoration of motor activity and movements. The results of neurophysiological, kinesiological and clinical observations are presented. We discuss the possible mechanisms, especially the spinal ones, which are fundamental for such a rhythmic activity as gait. We discuss them also from the point of view of activation of proprioceptive feedback mechanisms and of achieved sensory reinforcement influencing the spinal reflex mechanisms as well as the preserved supraspinal integrated activity which contributes to the long-term FES effect. The stimulation modes, the control of stimuli in relation to the needs of individual patients (hemiplegia in adults, paraparesis, cerebral palsy in children and multiple sclerosis) as well as the motor deficit are discussed. We conclude that the electronic system used for this purpose represents a functionally active orthotic aid with therapeutic effects.     

Persistent mirror movements for over sixty years: the underlying mechanisms in a cerebral palsy patient.

OBJECTIVE: To determine the mechanisms underlying the mirroring of distal movements in both upper and lower limbs present in one individual from birth. METHODS: Transcranial magnetic stimulation (TMS), magnetic resonance imaging (MRI), functional magnetic resonance imaging (fMRI), voluntary and reflexly evoked electromyograms (EMG) and force measurements were used to obtain information about the motor pathways responsible for the mirror movements. RESULTS: MRI showed a significant loss of brain tissue from one hemisphere and fMRI indicated a significant functional reorganization had taken place. An obligatory mirroring of voluntary movement on the sound side occurs on the affected side, but some independent movement can be produced on the affected side, if enabled by weak contractions on the sound side. TMS mapping revealed bilateral projections from one hemisphere and virtually absent projections from the primary motor cortex of the other hemisphere. Spinal reflexes were restricted to the stimulated side. Transcortical reflexes were evoked bilaterally from the sound side, but not from the affected side. CONCLUSIONS: The physiological and imaging data are consistent with a mirroring from the intact motor cortex via the supplementary motor area. SIGNIFICANCE: Mirror movements in this individual represent a major cortical reorganization and a partial solution to the neonatal loss of substantial amounts of brain tissue.     

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.