Hemispheric asymmetry of ipsilateral motor cortex activation during unimanual motor tasks: further evidence for motor dominance.

OBJECTIVES: To test to which extent the increase in ipsilateral motor cortex excitability during unimanual motor tasks shows hemispheric asymmetry. METHODS: Six right-handed healthy subjects performed one of several motor tasks of different complexity (including rest) with one hand (task hand) while the other hand (non-task hand) was relaxed. Focal transcranial magnetic stimulation was applied to the motor cortex ipsilateral to the task hand and the amplitude of the motor evoked potential (MEP) in the non-task hand was measured. In one session, the task hand was the right hand, in the other session it was the left hand. The effects of motor task and side of the task hand were analyzed. Spinal motoneuron excitability was assessed using F-wave measurements. RESULTS: Motor tasks, in particular complex finger sequences, resulted in an increase in MEP amplitude in the non-task hand. This increase was significantly less when the right hand rather than the left hand was the task hand. This difference was seen only in muscles homologous to primary task muscles. The asymmetry could not be explained by changes in F-wave amplitudes. CONCLUSIONS: Hemispheric asymmetry of ipsilateral motor cortex activation either supports the idea that, in right handers, the left motor cortex is more active in ipsilateral hand movements, or alternatively, that the left motor cortex exerts more effective inhibitory control over the right motor cortex than vice versa. We suggest that hemispheric asymmetry of ipsilateral motor cortex activation is one property of motor dominance of the left motor cortex.     

Motor cortex hand area and speech: implications for the development of language

Recently a growing body of evidence has suggested that a functional link exists between the hand motor area of the language dominant hemisphere and the regions subserving language processing. We examined the excitability of the hand motor area and the leg motor area during reading aloud and during non-verbal oral movements using transcranial magnetic stimulation (TMS). During reading aloud, but not before or afterwards, excitability was increased in the hand motor area of the dominant hemisphere. This reading effect was found to be independent of the duration of speech. No such effect could be found in the contralateral hemisphere. The excitability of the leg area of the motor cortex remained unchanged during reading aloud. The excitability during non-verbal oral movements was slightly increased in both hemispheres. Our results are consistent with previous findings and may indicate a specific functional connection between the hand motor area and the cortical language network.     

Abnormal motor cortex excitability during linguistic tasks in adductor‐type spasmodic dysphonia

In healthy subjects (HS), transcranial magnetic stimulation (TMS) applied during ‘linguistic’ tasks discloses excitability changes in the dominant hemisphere primary motor cortex (M1). We investigated ‘linguistic’ task‐related cortical excitability modulation in patients with adductor‐type spasmodic dysphonia (ASD), a speech‐related focal dystonia. We studied 10 ASD patients and 10 HS. Speech examination included voice cepstral analysis. We investigated the dominant/non‐dominant M1 excitability at baseline, during ‘linguistic’ (reading aloud/silent reading/producing simple phonation) and ‘non‐linguistic’ tasks (looking at non‐letter strings/producing oral movements). Motor evoked potentials (MEPs) were recorded from the contralateral hand muscles. We measured the cortical silent period (CSP) length and tested MEPs in HS and patients performing the ‘linguistic’ tasks with different voice intensities. We also examined MEPs in HS and ASD during hand‐related ‘action‐verb’ observation. Patients were studied under and not‐under botulinum neurotoxin‐type A (BoNT‐A). In HS, TMS over the dominant M1 elicited larger MEPs during ‘reading aloud’ than during the other ‘linguistic’/‘non‐linguistic’ tasks. Conversely, in ASD, TMS over the dominant M1 elicited increased‐amplitude MEPs during ‘reading aloud’ and ‘syllabic phonation’ tasks. CSP length was shorter in ASD than in HS and remained unchanged in both groups performing ‘linguistic’/‘non‐linguistic’ tasks. In HS and ASD, ‘linguistic’ task‐related excitability changes were present regardless of the different voice intensities. During hand‐related ‘action‐verb’ observation, MEPs decreased in HS, whereas in ASD they increased. In ASD, BoNT‐A improved speech, as demonstrated by cepstral analysis and restored the TMS abnormalities. ASD reflects dominant hemisphere excitability changes related to ‘linguistic’ tasks; BoNT‐A returns these excitability changes to normal.     

Visual cortex excitability increases during visual mental imagery--a TMS study in healthy human subjects

Previous neuroimaging studies provided evidence that visual mental imagery relies, in part, on the primary visual cortex. We hypothesized that, analogous to the finding that motor imagery increases the excitability of motor cortex, visual imagery should increase visual cortex excitability, as indexed by a decrease in the phosphene threshold (PT). In order to test visual cortex excitability, the primary visual cortex was stimulated with transcranial magnetic stimulation (TMS), so as to elicit phosphenes in the right lower visual quadrant. Subjects performed a visual imagery task and an auditory control task. We applied TMS with increasing intensity to determine the PT for each subject. Independent of the quadrant in which subjects placed their visual images, imagery decreased PT compared to baseline PT; in contrast, the auditory task did not change PT. These findings demonstrate for the first time a short-term, task-dependent modulation of PT. These results constitute evidence that early visual areas participate in visual imagery processing.     

Changes of muscle excitability of the hand contralateral to a task performing one: a transcranial magnetic stimulation study]

It used to be considered that unilateral movements of distal limb parts are associated only with contralateral motor cortical activity. Recent neuroimaging studies, however, suggest that the motor cortex ipsilateral to a task-performing hand is also activated, and that motor patterns in one hand affect the degree of the activity of the ipsilateral motor cortex. If so, muscles of the hand contralateral to a task-performing one may change those excitability depending on types of tasks. We studied eight subjects who performed three different finger tasks by one hand: (a) pinch, (b) sequential finger opposition, and (c) tactile discrimination. Transcranial magnetic stimulation was delivered by a figure eight coil over the hemisphere ipsilateral to a task-performing hand. Motor evoked potentials and background electromyographic activities were recorded from the opponens pollicis muscle contralateral to the stimulated hemisphere. On average, the motor evoked potentials were larger during tactile discrimination task than those at rest in either hand (p < 0.01). Background electromyographic activities in the left hand increased significantly during right hand tactile discrimination task (p < 0.01), whilst those in the right hand did not change during the left hand performance (p > 0.05). These findings suggest the followings: (1) the hand muscle contralateral to a task performing one changes its excitability depending on types of tasks; and (2) increment of excitability of the left hand muscle associated with right hand tactile discrimination is greater than that of the right hand one in association with the same task by the left hand, thus supporting the idea that there is a functional asymmetry between the right and left motor cortex in respect of motor performance.     

Neural topography and content of movement representations

We have used implicit motor imagery to investigate the neural correlates of motor planning independently from actual movements. Subjects were presented with drawings of left or right hands and asked to judge the hand laterality, regardless of the stimulus rotation from its upright orientation. We paired this task with a visual imagery control task, in which subjects were presented with typographical characters and asked to report whether they saw a canonical letter or its mirror image, regardless of its rotation. We measured neurovascular activity with fast event-related fMRI, distinguishing responses parametrically related to motor imagery from responses evoked by visual imagery and other task-related phenomena. By quantifying behavioral and neurovascular correlates of imagery on a trial-by-trial basis, we could discriminate between stimulus-related, mental rotation-related, and response-related neural activity. We found that specific portions of the posterior parietal and precentral cortex increased their activity as a function of mental rotation only during the motor imagery task. Within these regions, the parietal cortex was visually responsive, whereas the dorsal precentral cortex was not. Response- but not rotation-related activity was found around the left central sulcus (putative primary motor cortex) during both imagery tasks. Our study provides novel evidence on the topography and content of movement representations in the human brain. During intended action, the posterior parietal cortex combines somatosensory and visuomotor information, whereas the dorsal premotor cortex generates the actual motor plan, and the primary motor cortex deals with movement execution. We discuss the relevance of these results in the context of current models of action planning.     

No evidence for a substantial involvement of primary motor hand area in handedness judgements: a transcranial magnetic stimulation study

Twelve right-handed volunteers were asked to judge the laterality of a hand stimulus by pressing a button with one of their toes. Judgements were based on two-dimensional drawings of the back or palm of a right or left hand at various orientations. Suprathreshold single-pulse transcranial magnetic stimulation (TMS) was given to the left primary motor hand area (M1-HAND) at 0, 200, 400, 600, 800 or 1000 ms after stimulus onset to probe the functional involvement of the dominant left M1 at various stages of handedness recognition. We found that mean reaction times and error rates increased with angle of rotation depending on the actual biomechanical constraints of the hand but suprathreshold TMS had no influence on task performance regardless of the timing of TMS. However, the excitability of the corticomotor output from the left M1-HAND was modulated during the reaction. Judging left hand drawings was associated with an attenuation of motor-evoked potentials 300-100 ms before the response, whereas judging right hand drawings facilitated the motor-evoked potentials only immediately before the response. These effects were the same for pictures of backs and palms and were independent of the angle of rotation. The failure of TMS to affect task performance suggests that there is no time window during which the M1-HAND makes a critical contribution to mental rotation of the hand. The modulation of motor-evoked potentials according to the laterality of the stimulus indicates a secondary effect of the task on corticomotor excitability that is not directly related to mental rotation itself.     

Effector-independent representations of simple and complex imagined finger movements: a combined fMRI and TMS study

Kinesthetic motor imagery and actual execution of movements share a common neural circuitry. Functional magnetic resonance imaging was used in 12 right-handed volunteers to study brain activity during motor imagery and execution of simple and complex unimanual finger movements of the dominant and the nondominant hand. In the simple task, a flexible object was rhythmically compressed between thumb, index and middle finger. The complex task was a sequential finger-to-thumb opposition movement. Premotor, posterior parietal and cerebellar regions were significantly more active during motor imagery of complex movements than during mental rehearsal of the simple task. In 10 of the subjects, we also used transcranial magnetic brain stimulation to examine corticospinal excitability during the same motor imagery tasks. Motor-evoked potentials increased significantly over values obtained in a reference condition (visual imagery) during imagery of the complex, but not of the simple movement. Imagery of finger movements of either hand activated left dorsal and ventral premotor areas and the supplementary motor cortex regardless of task complexity. The effector-independent activation of left premotor areas was particularly evident in the simple motor imagery task and suggests a left hemispherical dominance for kinesthetic movement representations in right-handed subjects.     

Lateralization of motor excitability during observation of bimanual signs

Viewing another person's hand actions enhances excitability in an observer's left and right primary motor (M1) cortex. We aimed to determine whether viewing communicative hand actions alters this bilateral sensorimotor resonance. Using single-pulse transcranial magnetic stimulation (TMS), we measured excitability in the left and right M1 while right-handed non-signing participants observed bimanual communicative hand actions, i.e., meaningful signs in British Sign Language. TMS-induced motor evoked potentials were recorded from hand muscles during sign observation before and after teaching the participants to associate meanings with half of the signs. Before this teaching, when participants did not know that the presented hand actions were signs, excitability of left and right M1 was modulated equally. After learning the meanings of half the signs, excitability of the left, but not right, M1 was significantly enhanced. This left-lateralized enhancement of M1 excitability occurred during observation of signs with known and unknown meanings. The findings suggest that awareness of the communicative nature of another person's hand actions strengthens sensorimotor resonance in the left M1 cortex and alters hemispheric balance during action observation.     

Cerebral compensation during motor imagery in Parkinson's disease

In neurodegenerative disorders, neural damage can trigger compensatory mechanisms that minimize behavioural impairments. Here, we aimed at characterizing cerebral compensation during motor imagery in Parkinson's disease (PD), while controlling for altered motor execution and sensory feedback. We used a within-patient design to compare the most and least affected hand in 19 right-handed PD patients with markedly right-lateralized symptoms. We used a motor imagery (MI) task in which the patients were required to judge the laterality of hand images, rotated either in a lateral or in a medial orientation with respect to the body sagittal plane. This design allowed us to compare cerebral activity (using fMRI) evoked by MI of each hand separately, while objectively monitoring task performance. Reaction times and parieto-premotor activity increased in a similar manner as a function of stimulus rotation during motor imagery of left and right hands. However, patients were markedly slower when judging images of the affected hand in lateral orientations, and there was a corresponding increase in activity in the right extrastriate body area (EBA) and occipito-parietal cortex during mental rotation of the affected hand. Furthermore, these regions increased their connectivity towards the left PMd for right (affected) hands in a lateral orientation. We infer that, in strongly lateralized PD patients, motor imagery of the most-affected hand exploits additional resources in extrastriate visual areas. These findings characterize the cerebral bases of the increased dependence on visual information processing during the generation of motor plans in PD, pointing to its compensatory role.     

Switching attention and resolving interference: fMRI measures of executive functions

Is there a single executive process or are there multiple executive processes that work together towards the same goal in some task? In these experiments, we use counter switching and response inhibition tasks to examine the neural underpinnings of two cognitive processes that have often been identified as potential executive processes: the switching of attention between tasks, and the resolution of interference between competing task responses. Using functional magnetic resonance imaging (fMRI), for both event-related and blocked design tasks, we find evidence for common neural areas across both tasks in bilateral parietal cortex (BA 40), left dorsolateral prefrontal cortex (DLPFC; BA 9), premotor cortex (BA 6) and medial frontal cortex (BA 6/32). However, we also find areas preferentially involved in the switching of attention between mental counts (BA 7, BA 18) and the inhibition of a prepotent motor response (BA 6, BA 10), respectively. These findings provide evidence for the separability of cognitive processes underlying executive control.     

Walking the talk--speech activates the leg motor cortex

Speech may have evolved from earlier modes of communication based on gestures. Consistent with such a motor theory of speech, cortical orofacial and hand motor areas are activated by both speech production and speech perception. However, the extent of speech-related activation of the motor cortex remains unclear. Therefore, we examined if reading and listening to continuous prose also activates non-brachiofacial motor representations like the leg motor cortex. We found corticospinal excitability of bilateral leg muscle representations to be enhanced by speech production and silent reading. Control experiments showed that speech production yielded stronger facilitation of the leg motor system than non-verbal tongue-mouth mobilization and silent reading more than a visuo-attentional task thus indicating speech-specificity of the effect. In the frame of the motor theory of speech this finding suggests that the system of gestural communication, from which speech may have evolved, is not confined to the hand but includes gestural movements of other body parts as well.     

Towards unravelling task-related modulations of neuroplastic changes induced in the human motor cortex

Stimulation with weak electrical direct currents has been shown to be capable of inducing stimulation-polarity-dependent prolonged diminutions or elevations of cortical excitability, most probably elicited by a hyper- or depolarization of resting membrane potentials. The aim of the present study was to test if cognitive task and motor exercise practiced during the stimulation are able to modify transcranial direct current stimulation-induced plasticity in the left primary motor cortex in 12 healthy subjects. Motor evoked potentials were recorded before and after 10 min of anodal and cathodal transcranial direct current stimulation. In Experiment 1, subjects were required to sit passively during the stimulation, in Experiment 2 the subject's attention was directed towards a cognitive test and in Experiment 3 subjects were instructed to push a ball in their right hand. Both the cognitive task and motor exercise modified transcranial direct current stimulation-induced plasticity; when performing the cognitive task during stimulation the motor cortex excitability was lower after anodal stimulation and higher after cathodal stimulation, compared with the passive condition. When performing the motor exercise, the motor cortex excitability was lower after both anodal and cathodal stimulation, compared with the passive condition. Our results show that transcranial direct current stimulation-induced plasticity is highly dependent on the state of the subject during stimulation.     

Observation-execution matching and action inhibition in human primary motor cortex during viewing of speech-related lip movements or listening to speech

One influential theory posits that language has evolved from gestural communication through observation-execution matching processes in the mirror neuron system (MNS). This theory predicts that observation of speech-related lip movements or even listening to speech would result in effector and task specific increase of the excitability of the corresponding motor representations in the primary motor cortex (M1), since actual movement execution is known be effector and task specific. In addition, effector and task specific inhibitory control mechanisms should be important to prevent overt motor activation during observation of speech-related lip movements or listening to speech. We tested these predictions by applying focal transcranial magnetic stimulation to the left M1 of 12 healthy right-handed volunteers and measuring motor evoked potentials (MEPs) and short-interval intracortical inhibition (SICI) in a lip muscle, the right orbicularis oris (OO), vs. a hand muscle, the right first dorsal interosseus (FDI). We found that MEP and SICI increased only in the OO but not in the FDI during viewing of speech-related lip movements or listening to speech. These changes were highly task specific because they were absent when lip movements non-related to speech were viewed. Finally, the increase in MEP amplitude in the OO correlated inversely with accuracy of speech perception, i.e. the MEP increase was directly related to task difficulty. The MEP findings support the notion that observation-execution matching is an operating process in the putative human MNS that might have been fundamental for evolution of language. Furthermore, the SICI findings provide evidence that inhibitory mechanisms are recruited to prevent unwanted overt motor activation during action observation.     

Reaction time differences between left- and right-handers during mental rotation of hand pictures

During mental rotation tasks using hand pictures, right-handers make left–right judgements by mentally rotating their own hand to an orientation of the presented hand image. Although strategy difference for the tasks between left- and right-handers has been suggested, the strategy of left-handers has been incompletely understood. In the present study we compared differences in reaction times between 15 left-handed and 16 right-handed normal individuals during a mental rotation task using simple hand pictures. Participants were required to identify pictures of a hand presented in four orientations (upright, counterclockwise rotated, clockwise rotated, and inverted) as either a right or a left hand. Right-handers recognised a right hand faster than a left hand, whereas no significant difference was seen for left-handers. Both left- and right-handers recognised a right hand faster than a left hand in counterclockwise-rotated images, and recognised a left hand faster than a right hand in clockwise-rotated images. The findings suggest that the differences in the reaction times between left- and right-handers depend on a laterality balance of hand motor skills. During mental rotation task using simple hand pictures, left-handers may mentally simulate their own hand to match the stimulus image as similar to right-handers.     

Beyond variability: Subjective timing and the neurophysiology of motor cognition

Background

Movement simulation helps increasing the chances to reach goals. A cognitive task used to study the neuro-behavioral aspects of movement simulation is mental rotation: people mentally re-orient rotated pictures of hands. However, the involvement of the primary motor cortex (M1) in mental rotation is largely controversial.

Basal ganglia-premotor dysfunction during movement imagination in writer's cramp

The pathophysiology of idiopathic focal hand dystonia (writer's cramp) is characterized by deficient inhibitory basal ganglia function and altered cortical sensorimotor processing. To explore if this is already a primary finding in dystonia for internal movement simulation independent of dystonic motor output or abnormal sensory input, we investigated the neural correlates of movement imagination and observation in patients with writer's cramp. Event-related fMRI was applied during kinesthetic motor imagery of drawing simple geometric figures (imagination task) and passively observing videos of hands drawing identical figures (observation task). Compared with healthy controls, patients with writer's cramp showed deficient activation of the left primary sensorimotor cortex, mesial and left dorsal premotor cortex, bilateral putamen, and bilateral thalamus during motor imagery. No significant signal differences between both groups were found during the observation task. We conclude that internal movement simulation and planning as tested during imagination of hand movements appear to be dysfunctional in patients with writer's cramp, whereas visual signal processing and observation-induced activation are unaffected. Deficient basal ganglia-premotor activation could be a correlate of impaired basal ganglia inhibition and focusing during the selection of motor programs in dystonia. This finding seems to be an intrinsic deficit, as it is found during motor imagery in the absence of dystonic symptoms. ? 2012 Movement Disorder Society.     

Action verbs and the primary motor cortex: a comparative TMS study of silent reading, frequency judgments, and motor imagery

Single pulse transcranial magnetic stimulation (TMS) was applied to the hand area of the left primary motor cortex or, as a control, to the vertex (STIMULATION: TMS(M1) vs. TMS(vertex)) while right-handed volunteers silently read verbs related to hand actions. We examined three different tasks and time points for stimulation within the same experiment: subjects indicated with their left foot when they (i) had finished reading, (ii) had judged whether the corresponding movement involved a hand rotation after simulating the hand movement, and (iii) had judged whether they would frequently encounter the action verb in a newspaper (TASK: silent reading, motor imagery, and frequency judgment). Response times were compared between TMS(M1) and TMS(vertex), both applied at different time points after stimulus onset (DELAY: 150, 300, 450, 600, and 750 ms). TMS(M1) differentially modulated task performance: there was a significant facilitatory effect of TMS(M1) for the imagery task only (about 88 ms), with subjects responding about 10% faster (compared to TMS(vertex)). In contrast, response times for silent reading and frequency judgments were unaffected by TMS(M1). No differential effect of the time point of TMS(M1) was observed. The differential effect of TMS(M1) when subjects performed a motor imagery task (relative to performing silent reading or frequency judgments with the same set of verbs) suggests that the primary motor cortex is critically involved in processing action verbs only when subjects are simulating the corresponding movement. This task-dependent effect of hand motor cortex TMS on the processing of hand-related action verbs is discussed with respect to the notion of embodied cognition and the associationist theory.     

Functional connectivity between cortical hand motor and language areas during recovery from aphasia

Previous data indicate that in healthy subjects, there is a connectivity between cortical areas for hand movement and language on the left hemisphere. This link is possibly mediated by the so-called mirror neuron system. The present study investigated the functional relationship between linguistic and hand movement processing in patients who were recovering from post-stroke aphasia. The excitability of the right- and left-hand motor cortex during language production in patients who were recovering from post-stroke aphasia and age-matched controls was investigated. As control, phonation was investigated. Hand motor cortex excitability was assessed with Motor Evoked Potentials which were elicited by Transcranial Magnetic Stimulation (TMS). In patients, reading aloud enhanced the excitability of the right hemispheric hand motor cortex, whereas phonation had no effect on hand motor cortex excitability. In the control group, an increased excitability of the left hemispheric hand motor system was found during reading aloud in accordance with previous data. The present data suggest a functional connectivity between regions mediating hand movements and reading. This may indicate that the right hemisphere participates in language processing as far as involved in single word reading in patients recovering from aphasia. The coactivation between cerebral representations of hand movements and language may be used therapeutically for aphasia rehabilitation.     

Facilitation of implicit motor learning by weak transcranial direct current stimulation of the primary motor cortex in the human

Transcranially applied weak direct currents are capable of modulating motor cortical excitability in the human. Anodal stimulation enhances excitability, cathodal stimulation diminishes it. Cortical excitability changes accompany motor learning. Here we show that weak direct currents are capable of improving implicit motor learning in the human. During performance of a serial reaction time task, the primary motor cortex, premotor, or prefrontal cortices were stimulated contralaterally to the performing hand. Anodal stimulation of the primary motor cortex resulted in increased performance, whereas stimulation of the remaining cortices had no effect. We conclude that the primary motor cortex is involved in the acquisition and early consolidation phase of implicit motor learning.