Distinct cortical areas for motor preparation and execution in human identified by Bereitschaftspotential recording and ECoG-EMG coherence analysis.

OBJECTIVE: To clarify the cortical areas involved in motor preparation and execution by investigating Bereitschaftspotentials (BPs) and electrocorticogram-electromyogram (ECoG-EMG) coherence from subdural electrodes placed around the rolandic area. METHODS: BPs and ECoG-EMG coherence were investigated for presurgical evaluation in a patient with cavernoma in the left frontal lobe. BPs were recorded in association with the tongue, right hand and right foot movements. ECoG-EMG coherence was calculated in association with weak muscle contraction of the right hand. RESULTS: Two cortical areas related to voluntary motor control were identified; one in the primary hand motor area, which generated surface-negative BPs with hand movements and showed significant coherence of ECoG with EMG of the contralateral hand muscle, and the other in the ventral rolandic area posterior to the central sulcus, which generated surface-positive BPs with voluntary movements of multiple sites (hand, tongue and foot) but did not show any ECoG-EMG coherence. CONCLUSIONS: It is postulated that the former area represents the primary motor area involved in both motor preparation and execution, and the latter area represents the non-primary motor area involved in motor preparation. SIGNIFICANCE: BP recording combined with ECoG-EMG coherence analysis could reveal the functional roles of motor cortices and the reorganization induced by structural brain lesion.     

Sensory tricks modulate corticocortical and corticomuscular connectivity in cervical dystonia

ObjectiveTo examine interactions between cortical areas and between cortical areas and muscles during sensory tricks in cervical dystonia (CD).MethodsThirteen CD patients and thirteen age-matched healthy controls performed forewarned reaction time tasks, sensory tricks, and two tasks replicating aspects of the tricks (moving necks/arms). Control subjects mimicked sensory tricks. Corticocortical and corticomuscular coherence values were calculated from surface electrodes placed over motor, premotor, and sensory cortical areas and dystonic muscles.ResultsDuring initial preparation (after the warning stimulus), the only between-task difference was found in the γ-band corticocortical coherence (higher during tricks than during voluntary neck movements). With movements (before/after the imperative stimulus), the γ-band coherence of CD patients significantly increased during tricks but decreased during voluntary movements, while opposite trends were observed in healthy subjects. Additionally, the α- and β-band coherence decreased in healthy subjects during movements. Between the two patient subgroups (typical vs. forcible tricks), only those with typical tricks showed significant decrease in corticomuscular coherence during tricks.ConclusionsObserved changes in the corticocortical coherence suggest that sensory tricks improve cortical function, which reduces corticomuscular connectivity and the dystonia.SignificanceWe demonstrated that sensory tricks fundamentally affect sensorimotor integration in CD, both in movement preparation and execution.     

The neural substrate of gesture recognition

Previous studies have linked action recognition with a particular pool of neurons located in the ventral premotor cortex, the posterior parietal cortex and the superior temporal sulcus (the mirror neuron system). However, it is still unclear if transitive and intransitive gestures share the same neural substrates during action-recognition processes. In the present study, we used event-related functional magnetic resonance imaging (fMRI) to assess the cortical areas active during recognition of pantomimed transitive actions, intransitive gestures, and meaningless control actions. Perception of all types of gestures engaged the right pre-supplementary motor area (pre-SMA), and bilaterally in the posterior superior temporal cortex, the posterior parietal cortex, occipitotemporal regions and visual cortices. Activation of the posterior superior temporal sulcus/superior temporal gyrus region was found in both hemispheres during recognition of transitive and intransitive gestures, and in the right hemisphere during the control condition; the middle temporal gyrus showed activation in the left hemisphere when subjects recognized transitive and intransitive gestures; activation of the left inferior parietal lobe and intraparietal sulcus (IPS) was mainly observed in the left hemisphere during recognition of the three conditions. The most striking finding was the greater activation of the left inferior frontal gyrus (IFG) during recognition of intransitive actions. Results show that a similar neural substrate, albeit, with a distinct engagement underlies the cognitive processing of transitive and intransitive gestures recognition. These findings suggest that selective disruptions in these circuits may lead to distinct clinical deficits.     

Activation of motor pathways during observation and execution of hand movements

Some neural properties of "motor resonance"--the subliminal activation of the motor system when observing actions performed by others--are investigated in humans. Two actions performed with the right hand are observed by experimental subjects: a finalized (transitive) action (reaching for and grasping a ball) and an intransitive action (cyclic up-and-down oscillation of the hand), while the H-reflex and Transcranial Magnetic Stimulation techniques are utilized to test the excitability of the observer's motor pathways to hand and forearm muscles (first dorsal interosseus, flexor digitorum superficialis, flexor carpi radialis). Results indicate that motor resonance: (1) is mainly mediated by the primary motor cortex; (2) involves the same forearm muscles as used in the execution of the observed movement; (3) is also recorded in the homologous muscles of the arm contralateral to the one observed; and (4) is evoked by both transitive and intransitive movements of the human hand, but not by similar movements of inanimate objects. The similarities and discrepancies between the resonant response in humans and the properties of monkey "mirror neurons" are discussed.     

Left inferior parietal representations for skilled hand-object interactions: evidence from stroke and corticobasal degeneration

Patients with ideomotor apraxia (IM) are frequently more impaired in the production and imitation of object-related (transitive) than non-object-related, symbolic (intransitive) gestures, but reasons for this dissociation, and its anatomical underpinnings, remain unclear. Our theoretical model of praxis (Buxbaum, 2001) postulates that left inferior parietal lobe (IPL) gesture representations store information about postures and movements of the body and hand for skillful manipulation of familiar objects; in contrast, bilateral fronto-parietal dynamic calculations provide constantly-updated information about the current position and movement of the body and hand for both familiar and novel, transitive and intransitive movements. This account predicts distinct patterns of IM in patients with left IPL damage versus bilateral fronto-parietal involvement. Consistent with predictions, 16 stroke patients with left IPL damage were more impaired with transitive than intransitive gestures, whereas 4 patients with bilateral fronto-parietal damage due to corticobasal degeneration (CBD) were not [F (1, 18) = 8.5 p < .01]. Additionally, the hand posture component of transitive gestures was the most impaired aspect of gesture in CVA, but tended to be the least impaired aspect of gesture in CBD [F (3, 54) = 5.1, p < .005]. Finally, CVA patients were more impaired with transitive hand postures than meaningless or intransitive hand postures, whereas CBD patients showed the opposite pattern. These data indicate that the left IPL mediates representations of skilled hand-object interactions, as distinct from dynamic coding of the body in space, and suggest that the IPL maps between representations of object identity in the ventral stream and spatial body representations mediated by the dorsal system.     

Motor execution and imagination networks in post-stroke dystonia

Reorganization of motor execution and imagination networks was studied in six patients with unilateral dystonia secondary to a subcortical stroke and compared with seven control subjects using fMRI. Patients performed imagined and real auditory-cued hand movements. Movements of the dystonic hand resulted in overactivity in bilateral motor, premotor, and prefrontal cortex, insula, precuneus, and cerebellum, in parietal areas and the striatum contralateral to the lesion. Movements of the unaffected hand resulted in overactivity in bilateral preSMA, prefrontal, and parietal areas, insula and cerebellum, the ipsilateral premotor cortex and the contralateral striatum to the lesion. Mental representation of movements with each hand resulted in overactivity in bilateral parietal, premotor and prefrontal areas. These results suggest that execution and mental representation of movement are altered in these patients.     

The involvement of monkey premotor cortex neurones in preparation of visually cued arm movements

Some neurones in macaque postarcuate premotor area modulate their firing frequency in relation to motor tasks which require visual information. We previously reported that a large proportion of these neurones modulate during execution of a detour reaching task in which the movement phase was separated in time from the phase in which the monkey received a visual cue for the movement required to retrieve a food reward. A large proportion of task-related neurones (75%) modulated during this 'visual' phase, in which no task-related movements were made. This modulation was related to the position of the food reward, which served as the visual cue. Most of these neurones were located in cortical area 6, close to the arcuate curvature and its spur, but also more caudally in area 4 and rostrally in area 8. In the present chronic recording experiments in monkeys, several variations of the original task were used in order to test whether the 'visual'-related neuronal modulation could be involved in preparation of the upcoming movement. This modulation is unlikely to be related to any eye or arm movements occurring during the visual phase or to changes in environmental illumination. Neither can it be related to the presence of the visual cue in a particular part of the visual field, since the pattern of neuronal modulation was similar when a cue with a fixed position was used. This modulation was, however, contingent upon the occurrence of food retrieval during the subsequent 'movement phase', since it was abolished or diminished during presentation of a 'food-reward' which the monkey did not retrieve. For several neurones, modulation pattern during the visual phase depended on whether the food reward was to be retrieved with a gross hand movement or with relatively independent finger movements. It is likely, therefore, that neurones in the postarcuate premotor cortex are involved in preparation for arm movements with the help of visual cues. The results are discussed in view of corticocortical pathways which might be involved in transmission of visual information from visual areas through parietal association areas and premotor cortex to the primary motor cortex.     

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.     

Right hemisphere contributions to imitation tasks

Humans imitate biological movements faster than non-biological movements. The faster response has been attributed to an activation of the human mirror neuron system, which is thought to match observation and execution of actions. However, it is unclear which cortical areas are responsible for this behavioural advantage. Also, little is known about the timing of activations. Using whole-head magnetoencephalography we recorded neuronal responses to single biological finger movements and non-biological dot movements while the subjects were required to perform an imitation task or an observation task, respectively. Previous imaging studies on the human mirror neurone system suggested that activation in response to biological movements would be stronger in ventral premotor, parietal and superior temporal regions. In accordance with previous studies, reaction times to biological movements were faster than those to dot movements in all subjects. The analysis of evoked magnetic fields revealed that the reaction time benefit was paralleled by stronger and earlier activation of the left temporo-occipital cortex, right superior temporal area and right ventral motor/premotor area. The activity patterns suggest that the latter areas mediate the observed behavioural advantage of biological movements and indicate a predominant contribution of the right temporo-frontal hemisphere to action observation–execution matching processes in intransitive movements, which has not been reported previously.     

Parietal cortex coding of limb posture: In search of the body-schema

Computational theories of motor control propose that the brain uses ‘forward’ models of the body to ensure accurate control of movements. Forward ‘dynamic’ models are thought to generate an estimate of the next motor state for an upcoming movement: thereby providing a dynamic representation of the current postural configuration of the body that can be utilised during movement planning and execution. We used event-related functional magnetic resonance imaging [fMRI] to investigate brain areas involved in maintaining and updating the postural representations of the upper limb that participate in the control of reaching movements. We demonstrate that the neural correlates for executing memory-guided reaching movements to unseen target locations that were defined by arm posture, are primarily within regions of the superior parietal lobule [SPL]: including an area of the medial SPL identified as the human homologue of the ‘parietal reach region’ [PRR]. Using effective connectivity analyses we show that signals that influence the BOLD response within this area originate within premotor areas of the frontal lobe, including premotor cortex and the supplementary motor area. These data are consistent with the view that the SPL maintains an up-to-date estimate of the current postural configuration of the arm that is used during the planning and execution of reaching movements.     

Distribution of slow cortical potentials preceding self-paced hand and hindlimb movements in the premotor and motor areas of monkeys

Surface negative-depth positive, slowly increasing potentials prior to self-paced hand and hindlimb movements were recorded in the dorsal aspect of the motor and premotor cortices with chronically implanted electrodes. It was shown that the potentials were recorded in the contralateral forelimb motor area prior to hand movements but were hardly seen in the hindlimb motor area. On hindlimb movements, the contralateral hindlimb motor area showed the premovement potentials, whereas the forelimb motor area revealed little or no premovement potentials. The contralateral premotor cortex was shown to induce the premovement potentials in its wider areas and participate in both of hand and hindlimb movements in a similar fashion, with predominances in its dorsolateral portion for hand movements and in its dorsomedial portion for hindlimb movements respectively. In the hemisphere ipsilateral to the moving hand, the relatively large premovement slow potentials emerged frequently also in the premotor cortex, whereas only the small potential was obtained from the forelimb motor area. These results suggest that the premotor cortex (area 6) participates in the more general and associative organization of motor function than the motor cortex (area 4) which represents the specialized role in the motor performance.     

Short-term learning of a visually guided power-grip task is associated with dynamic changes in EEG oscillatory activity.

OBJECTIVE: Performing a motor task after a period of training has been associated with reduced cortical activity and changes in oscillatory brain activity. Little is known about whether learning also affects the neural network associated with motor preparation and post movement processes. Here we investigate how short-term motor learning affects oscillatory brain activity during the preparation, execution, and post-movement stage of a force-feedback task. METHODS: Participants performed a visually guided power-grip tracking task. EEG was recorded from 64 scalp electrodes. Power and coherence data for the early and late stages of the task were compared. RESULTS: Performance improved with practice. During the preparation for the task alpha power was reduced for late experimental blocks. A movement execution-related decrease in beta power was attenuated with increasing task practice. A post-movement increase in alpha and lower beta activity was observed that decreased with learning. Coherence analysis revealed changes in cortico-cortical coupling with regard to the stage of the visuomotor task and with regard to learning. Learning was variably associated with increased coherence between contralateral and/or ipsilateral frontal and parietal, fronto-central, and occipital brain regions. CONCLUSIONS: Practice of a visuomotor power-grip task is associated with various changes in the activity of a widespread cortical network. These changes might promote visuomotor learning. SIGNIFICANCE: This study provides important new evidence for and sheds new light on the complex nature of the brain processes underlying visuomotor integration and short-term learning.     

Topography of scalp-recorded motor potentials in human finger movements

Four distinct negative events were identified in the averaged, scalp-recorded EEGs of normal subjects before and after the onset of self-paced, voluntary finger movements; reaction-time movements and passive movements were also studied. These events are the peak of the negative slope (NS'), the initial slope of motor potential (isMP), the parietal peak of motor potential (ppMP), and the frontal peak of motor potential (fpMP). For self-paced movements, NS' and isMP occurred before the onset of electromyographic (EMG) activity, and ppMP and fpMP occurred after the onset of EMG activity. NS' had a wide distribution, covering the parietal region with slight contralateral predominance. The isMP mapped focally over the contralateral hand motor area on the scalp. The location of ppMP was similar to that of isMP. The fpMP was localized anterior and medial to motor cortex with a contralateral preponderance and possible location over the supplementary motor area. The isMP and fpMP also were identified in the recordings of reaction-time movements, but only the fpMP persisted in the recordings of passive movements. The isMP appears to reflect activation of the cortical cells in the hand area of motor cortex for the execution of voluntary movement, and the fpMP appears to reflect proprioceptive feedback from the periphery.     

Activation of cortical and cerebellar motor areas during executed and imagined hand movements: an fMRI study.

Brain activation during executed (EM) and imagined movements (IM) of the right and left hand was studied in 10 healthy right-handed subjects using functional magnetic resonance imagining (fMRI). Low electromyographic (EMG) activity of the musculi flexor digitorum superficialis and high vividness of the imagined movements were trained prior to image acquisition. Regional cerebral activation was measured by fMRI during EM and IM and compared to resting conditions. Anatomically selected regions of interest (ROIs) were marked interactively over the entire brain. In each ROI activated pixels above a t value of 2.45 (p<0.01) were counted and analyzed. In all subjects the supplementary motor area (SMA), the premotor cortex (PMC), and the primary motor cortex (M1) showed significant activation during both EM and IM; the somatosensory cortex (S1) was significantly activated only during EM. Ipsilateral cerebellar activation was decreased during IM compared to EM. In the cerebellum, IM and EM differed in their foci of maximal activation: Highest ipsilateral activation of the cerebellum was observed in the anterior lobe (Larsell lobule H IV) during EM, whereas a lower maximum was found about 2-cm dorsolateral (Larsell lobule H VII) during IM. The prefrontal and parietal regions revealed no significant changes during both conditions. The results of cortical activity support the hypothesis that motor imagery and motor performance possess similar neural substrates. The differential activation in the cerebellum during EM and IM is in accordance with the assumption that the posterior cerebellum is involved in the inhibition of movement execution during imagination.     

Regional cerebral blood flow changes in human brain related to ipsilateral and contralateral complex hand movements – a PET study

The purpose of this study was to investigate the cortical motor areas activated in relation to unilateral complex hand movements of either hand, and the motor area related to motor skill learning. Regional cerebral blood flow (rCBF) was measured in eight right-handed healthy male volunteers using positron emission tomography during a two-ball-rotation task using the right hand, the same task using the left hand and two control tasks. In the two-ball-rotation tasks, subjects were required to rotate the same two iron balls either with the right or left hand. In the control task, they were required to hold two balls in each hand without movement. The primary motor area, premotor area and cerebellum were activated bilaterally with each unilateral hand movement. In contrast, the supplementary motor area proper was activated only by contralateral hand movements. In addition, we found a positive correlation between the rCBF to the premotor area and the degree of improvement in skill during motor task training. The results indicate that complex hand movements are organized bilaterally in the primary motor areas, premotor areas and cerebellum, that functional asymmetry in the motor cortices is not evident during complex finger movements, and that the premotor area may play an important role in motor skill learning.     

The supplementary motor area modulates interhemispheric interactions during movement preparation

The execution of coordinated hand movements requires complex interactions between premotor and primary motor areas in the two hemispheres. The supplementary motor area (SMA) is involved in movement preparation and bimanual coordination. How the SMA controls bimanual coordination remains unclear, although there is evidence suggesting that the SMA could modulate interhemispheric interactions. With a delayed‐response task, we investigated interhemispheric interactions underlying normal movement preparation and the role of the SMA in these interactions during the delay period of unimanual or bimanual hand movements. We used functional MRI and transcranial magnetic stimulation in 22 healthy volunteers (HVs), and then in two models of SMA dysfunction: (a) in the same group of HVs after transient disruption of the right SMA proper by continuous transcranial magnetic theta‐burst stimulation; (b) in a group of 22 patients with congenital mirror movements (CMM), whose inability to produce asymmetric hand movements is associated with SMA dysfunction. In HVs, interhemispheric connectivity during the delay period was modulated according to whether or not hand coordination was required for the forthcoming movement. In HVs following SMA disruption and in CMM patients, interhemispheric connectivity was modified during the delay period and the interhemispheric inhibition was decreased. Using two models of SMA dysfunction, we showed that the SMA modulates interhemispheric interactions during movement preparation. This unveils a new role for the SMA and highlights its importance in coordinated movement preparation.     

Simultaneous movements of upper and lower limbs are coordinated by motor representations that are shared by both limbs: a PET study

The purpose of this study was to examine the cerebral control of simultaneous movements of the upper and lower limbs. We examined two hypotheses on how the brain coordinates movement: (i) by the involvement of motor representations shared by both limbs; or (ii) by the engagement of specific neural populations. We used positron emission tomography to measure the relative cerebral blood flow in healthy subjects performing isolated cyclic flexion-extension movements of the wrist and ankle (i.e. movements of wrist or ankle alone), and simultaneous movements of the wrist and ankle (a rest condition was also included). The simultaneous movements were performed in the same directions (iso-directional) and in opposite directions (antidirectional). There was no difference in the brain activity between these two patterns of coordination. In several motor-related areas (e.g. the contralateral ventral premotor area, the dorsal premotor area, the supplementary motor area, the parietal operculum and the posterior parietal cortex), the representation of the isolated wrist movement overlapped with the representation of the isolated ankle movement. Importantly, the simultaneous movements activated the same set of motor-related regions that were active during the isolated movements. In the contralateral ventral premotor cortex, dorsal premotor cortex and parietal operculum, there was less activity during the simultaneous movements than for the sum of the activity for the two isolated movements (interaction analysis). Indeed, in the ventral premotor cortex and parietal operculum, the activity was practically identical regardless whether only the wrist, only the ankle, or both the wrist and the ankle were moved. Taken together, these findings suggest that interlimb coordination is mediated by motor representations shared by both limbs, rather than being mediated by specific additional neural populations.     

Left parietal activation related to planning,executing and suppressing praxis hand movements

ObjectiveWe sought to investigate the activity of bilateral parietal and premotor areas during a Go/No Go paradigm involving praxis movements of the dominant hand.MethodsA sentence was presented which instructed subjects on what movement to make (S1; for example, “Show me how to use a hammer.”). After an 8-s delay, “Go” or “No Go” (S2) was presented. If Go, they were instructed to make the movement described in the S1 instruction sentence as quickly as possible, and continuously until the “Rest” cue was presented 3 s later. If No Go, subjects were to simply relax until the next instruction sentence. Event-related potentials (ERP) and event-related desynchronization (ERD) in the beta band (18–22 Hz) were evaluated for three time bins: after S1, after S2, and from −2.5 to −1.5 s before the S2 period.ResultsBilateral premotor ERP was greater than bilateral parietal ERP after the S2 Go compared with the No Go. Additionally, left premotor ERP was greater than that from the right premotor area. There was predominant left parietal ERD immediately after S1 for both Go and No Go, which was sustained for the duration of the interval between S1 and S2. For both S2 stimuli, predominant left parietal ERD was again seen when compared to that from the left premotor or right parietal area. However, the left parietal ERD was greater for Go than No Go.ConclusionThe results suggest a dominant role in the left parietal cortex for planning, executing, and suppressing praxis movements. The ERP and ERD show different patterns of activation and may reflect distinct neural movement-related activities.SignificanceThe data can guide further studies to determine the neurophysiological changes occurring in apraxia patients and help explain the unique error profiles seen in patients with left parietal damage.     

Recording of movement-related potentials from the human cortex

A patient with intractable epilepsy secondary to a brain tumor was evaluated with a chronically implanted array of 64 stainless-steel subdural electrodes covering the perirolandic area. Cortical potentials associated with voluntary, self-paced middle-finger extension were recorded simultaneously from subdural and scalp electrodes using a computer-assisted method for averaging movement-related potential (MRP) in relation to electromyographic (EMG) onset. A high-amplitude negative potential, Bereitschaftspotential/negative slope (BP/NS'), preceding the onset of the EMG activity by more than 1 sec was recorded in an extremely localized fashion exclusively from electrodes placed in the precentral hand motor area as well as in the more medial part of the somatosensory hand area. These results suggest that the hand motor and sensory areas have an essential participation in the generation of MRPs and, therefore, also in the preparation of voluntary finger movements.     

Spectral analysis of EEG during self-paced movements: differences between untreated schizophrenics and normal controls.

Thirteen untreated schizophrenic patients, among them nine who had never been treated, were compared with a corresponding number of matched normal controls with regard to changes of the spectral composition of the electroencephalogram (EEG) accompanying voluntary movements. Triggered by self-paced movements of the right fingers (fast fist closure), the spectral composition of three epochs was analyzed: (1) rest (2,5-1,5 sec before movement), (2) movement preparation (last sec before movement onset), and (3) movement execution (1st sec following movement onset). For frequencies above 6 Hz, marked differences between schizophrenics and controls were evident, in particular over the parietal electrodes. Whereas patients exhibited a clear decrease of power density during movement as compared to rest, controls showed only a small decrease (left and mid parietal) or virtually none (only right parietal). Consequently there were significant differences over the right parietal area (P4) between patients and controls in the theta, alpha- and beta-bands with regard to the mean power density and center frequencies of these bands. Also at parietal positions, schizophrenics lacked the enhancement of theta-power during the preparatory epoch that was characteristic for normal controls at all parietal positions. The results are discussed with regard to the well-known disturbances of voluntary motor behavior in schizophrenia.