Task-dependent effects of interhemispheric inhibition on motor control

Interhemispheric communication consists of a complex balance of facilitation and inhibition that is modulated in a task-dependent manner. However, it remains unclear how individual differences in interhemispheric interactions relate to motor performance. To assess interhemispheric inhibition, we utilized the ipsilateral silent period technique (iSP; evoked by suprathreshold transcranial magnetic stimulation), which elicits inhibition of volitional motor activity. Participants performed three force production tasks: (1) unimanual (right hand) constant force, (2) bimanual constant force, (bimanual simultaneous) and (3) bimanual with right hand constant force and left hand sine wave tracking (bimanual independent). We found that individuals with greater IHI capacity demonstrated reduced mirror EMG activity in the left hand during unimanual right hand contraction. However, these same individuals demonstrated the poorest performance during the bimanual independent force production task. We suggest that a high capacity for IHI from one motor cortex to another can effectively prevent “motor overflow” during unimanual tasks, but it can also limit interhemispheric cooperation during independently controlled bimanual tasks.     

Transcranial magnetic stimulation measures in attention-deficit/hyperactivity disorder

Children affected by attention-deficit/hyperactivity disorder demonstrate diminished intrahemispheric inhibition (short interval cortical inhibition), as measured by transcranial magnetic stimulation. This study determined whether interhemispheric inhibition (ipsilateral silent period latency) correlates with clinical behavioral rating and motor control deficits of affected children. In 114 right-handed children (aged 8-12 years; age/sex-matched; 50 affected, 64 controls), we performed comprehensive assessments of behavior, motor skills, and cognition. Transcranial magnetic stimulation reliably elicited ipsilateral silent periods in 54 children (23 affected); all were on average older than those with unobtainable measures. Mean ipsilateral silent period latency was 5 milliseconds longer in the affected group (P?=?0.007). Longer latencies correlated with more severe behavioral symptom scores (r?=?0.38, P = 0.007), particularly hyperactivity (r?= 0.39, P = 0.006), and with worse motor ratings on the Physical and Neurological Examination for Soft Signs (r?= 0.27, P = 0.05). Longer latency also correlated with short interval cortical inhibition (r?= 0.36, P = 0.008). Longer ipsilateral silent period latencies suggest interhemispheric inhibitory signaling is slower in affected children. The deficit in this inhibitory measure may underlie developmental, behavioral, and motor impairments in children with attention-deficit/hyperactivity disorder.     

Involvement of area MT in bimanual finger movements in left-handers: an fMRI study

The ease with which humans are able to perform symmetric movements of both hands has traditionally been attributed to the preference of the motor system to activate homologous muscles. Recently, we have shown in right-handers, however, that bimanual index finger adduction and abduction movements in incongruous hand orientations (one palm down/other up) preferentially engaged parietal perception-associated brain areas. Here, we used functional magnetic resonance imaging to investigate the influence of hand orientation in left-handers on cerebral activation during bimanual index finger movements. Performance in incongruous orientation of either hand yielded activations involving right and left motor cortex, supplementary motor area in right superior frontal gyrus (SMA and pre-SMA), bilateral premotor cortex, prefrontal cortex, bilateral somatosensory cortex and anterior parietal cortex along the intraparietal sulcus. In addition, the occipito-temporal cortex corresponding to human area MT (hMT) in either hemisphere was activated in relation to bimanual index finger movements in the incongruous hand orientation as compared with the same movements in the congruous hand orientation or with simply viewing the pacing stimuli. Comparison with the same movement condition in right-handed subjects from a former study support these hMT activations exclusively for left-handed subjects. These results suggest that left-handers use visual motion imagery in guiding incongruous bimanual finger movements.     

The importance of the dominant hemisphere in the organization of bimanual movements

The successful control of upper limb movements is an essential skill of the human motor system. Yet, the neural organization of bimanual actions remains an issue of debate. Their control can be directed from both hemispheres, or, coordinated motion might be organized from the dominant (left) hemisphere. In order to unravel the neural mechanisms of bimanual behavior, we analyzed the standard task-related and directed coherence between EEG signals picked up over the primary sensorimotor cortices in right-handed subjects during unimanual as well as bimanual in-phase (symmetrical) and anti-phase (asymmetrical) movements. The interhemispheric coherence in the beta frequency band (>13-30 Hz) was increased in both unimanual and bimanual patterns, compared to rest. During unimanual actions, the drive in the beta band from one primary sensorimotor cortex to the other was greater during movement of the contralateral as opposed to ipsilateral hand. In contrast, during bimanual actions, the drive from the dominant to the non-dominant primary sensorimotor cortex prevailed, unless task constraints induced by an external perturbation resulted in a substantial uncoupling of the hand movements, when interhemispheric coherence would also drop. Together, these results suggest that the contralateral hemisphere predominantly organizes unimanual movements, whereas coupled bimanual movements are mainly controlled from the dominant hemisphere. The close association between changes in interhemispheric coupling and behavioral performance indicates that synchronization of neural activity in the beta band is exploited for the control of goal-directed movement.     

An analysis of the naming deficit of left-handers

Left-handers have been found to have a naming deficit when confronted with briefly flashed words. Three alternative explanations of this deficit were tested: whether it was due to deviant interhemispheric cooperation, relatively diffuse neural organization, or left hemispheric dysfunction. In Experiment I, four words were presented for 190 ms, unilaterally (to a single hemisphere), or bilaterally (between the hemispheres). Although left-handers (N = 48) named significantly less than right-handers (N = 30), performance was parallel across hemispheric conditions. Experiment II required semantic categorization, but not naming. The performance of the left-handers (N = 27) was indistinguishable from that of right-handers (N = 27) both in terms of overall performance and interhemispheric collaboration. It is concluded that the linguistic deficit of left-handers is specific to oral naming and that it is not caused by deviant interhemispheric cooperation.     

Hemispheric asymmetries of cortico-cortical connections in human hand motor areas.

OBJECTIVE: To evaluate possible functional asymmetries of the motor cortex on the hand-dominant versus the non-dominant hemisphere. METHODS: We assessed the handedness of 15 consenting volunteers using the Edinburgh Inventory. They were divided in two groups: 9 right-handers and 6 left-handers. We used single- and paired-transcranial magnetic stimulation (TMS) to measure the relaxed and active motor threshold and the ipsilateral cortico-cortical inhibition and facilitation curve for both hand motor areas. We looked for hemispheric asymmetries of variables related to the side of stimulation (dominant versus non-dominant) and to handedness.RESULTS: We found no significant intra- or intergroup hemispheric asymmetry for the relaxed and active thresholds. Among the right-handers, the cortico-cortical inhibition and facilitation curve showed an increased amount of facilitation in the dominant as compared with the non-dominant hand area. No such changes were seen among the left-handers. Both the dominant and the non-dominant hand areas of the right-handers showed more inhibition and less facilitation on the cortico-cortical inhibition and facilitation curve than the corresponding areas of left-handers. CONCLUSION: In the right-handers, paired TMS studies showed a functional asymmetry of the motor cortex between the dominant and the non-dominant hand. The left-handers did not show this lateralization. Under TMS investigation their motor cortex function appeared different from that of right-handers.     

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.     

Intermanual coordination in relation to handedness, familial sinistrality and lateral preferences

Intermanual coordination assessed by alternating finger tapping and finger-tapping asymmetry were investigated in 105 healthy right- and 105 left-handers and related to handedness, familial sinistrality and lateral preferences (in hand-clasping, arm-folding and eyedness). Compared to right-handers, left-handers with less pronounced left-hand preferences (Subgroup B) showed higher values in intermanual coordination and lower values in finger-tapping asymmetry. Moreover, familial sinistrality and eyedness interacted with handedness effects. While in right-handers intermanual coordination was significantly higher in subjects with dominant left eye, in left-handers of the Subgroup B it was somewhat higher in those with dominant right eye. Higher values in intermanual coordination and reduced asymmetry in finger tapping may be associated with a greater bihemispheric control and better performance in fast bimanual movements.     

Motor control of the hands: the effect of familial sinistrality.

Left- and right-handed subjects, selected on the basis of degree of hand preference and for the presence or absence of familial sinistrality, responded to monaurally presented tonal stimuli (440 Hz note played on four different instruments) using their right and left hands on separate occasions. It was found that in both the strong left-handers and the inconsistent strong right-handers, motor control of the hands was related to familial sinistrality (FS). Specifically, strong left-handers and inconsistent strong right-handers with FS have a difference in the motor control of the hands in the left hemisphere, with a left hemisphere-left hand advantage. Strong left-handers and inconsistent strong right-handers with no FS have a difference in the motor control of the hands in the right hemisphere, with a right hemisphere-left hand advantage.     

Effects of eye dominance (left vs. right) and cannabis use on intermanual coordination and negative symptoms in schizophrenia patients

Based on the previous findings, it has been assumed that in schizophrenia patients, eye dominance and cannabis use will affect negative symptoms and intermanual coordination (IMC), an index of interhemispheric communication. But eye dominance, specifically the clinical findings for it, has been neglected in schizophrenia research. We therefore investigated its effects in 52 right-handed (36 right-eyed and 16 left-eyed) and 51 left-handed (35 left-eyed and 16 right-eyed) schizophrenia in-patients without and with drug use. Eye dominance affected IMC in all schizophrenia patients. When comparing right- and left-handers, we found that this result was only significant in the right-handed patients and in the smaller subgroup without drug use. In the right-handers, left eye dominance—like left-handedness—was associated with higher values in IMC and less pronounced manifestation of negative symptoms, right eye dominance was not. Thus, left-eyed right-handers may be more closely related to left-handers than to right-handers. In accordance with the results from the literature, we suggest that these findings are due to better interhemispheric connections and less impairment of white matter structures, especially in right-hemispheric regions. Moreover, cannabis use was related to higher scores in IMC and less pronounced negative symptoms, but only in the right-eyed and not in the left-eyed right-handers or in the left-handers. Hence, differences in eye dominance and handedness may be partially responsible for different results in interhemispheric connections among cannabis users. In conclusion, both eye dominance and use of cannabis should be taken into account when assessing clinical symptoms in schizophrenia patients.     

Modulation of interhemispheric interactions across symmetric and asymmetric bimanual force regulations

The corpus callosum is essential for neural communication between the left and right hemispheres. Although spatiotemporal coordination of bimanual movements is mediated by the activity of the transcallosal circuit, it remains to be addressed how transcallosal neural activity is involved in the dynamic control of bimanual force execution in human. To address this issue, we investigated transcallosal inhibition (TCI) elicited by single‐pulse transcranial magnetic stimulation (TMS) in association with the coordination condition of bimanual force regulation. During a visually‐guided bimanual force tracking task, both thumbs were abducted either in‐phase (symmetric condition) or 180° out‐of‐phase (asymmetric condition). TMS was applied to the left primary motor cortex to elicit the disturbance of ipsilateral left force tracking due to TCI. The tracking accuracy was equivalent between the two conditions, but the synchrony of the left and right tracking trajectories was higher in the symmetric condition than in the asymmetric condition. The magnitude of force disturbance and TCI were larger during the symmetric condition than during the asymmetric condition. Right unimanual force tracking influenced neither the force disturbance nor TCI during tonic left thumb abduction. Additionally, these TMS‐induced ipsilateral motor disturbances only appeared when the TMS intensity was strong enough to excite the transcallosal circuit, irrespective of whether the crossed corticospinal tract was activated. These findings support the hypotheses that interhemispheric interactions between the motor cortices play an important role in modulating bimanual force coordination tasks, and that TCI is finely tuned depending on the coordination condition of bimanual force regulation.     

Interhemispheric cooperation of left- and right-handers in mental calculation tasks

Relations between handedness and interhemispheric processing in cognitive tasks were examined. Thirty six right-handers and thirty left-handers (familial and nonfamilial left-handers) were asked to add two numbers which were presented tachistoscopically. Two numbers were displayed either to one visual field, or one to the left and one to the right visual field simultaneously. In Experiment 1, the numbers were displayed in Arabic numerals, and in Experiment 2 one of the numbers was displayed in Kanji and one in Arabic numerals. The results of Experiment 1 showed a bilateral advantage, however no subject group difference was shown in the performance of the three (left unilateral, right unilateral, and bilateral) presentation conditions. Though familial left-handers showed a weaker tendency to different patterns than right and non-familial left-handers, the results of Experiment 2 were largely similar to those of Experiment 1. These findings suggest that interhemispheric processing may not differ between left- and right-handers.     

Children with comorbid attention-deficit-hyperactivity disorder and tic disorder: evidence for additive inhibitory deficits within the motor system

For children with attention-deficit-hyperactivity disorder (ADHD) or tic disorder (TD), we recently reported deficient inhibitory mechanisms within the motor system by using transcranial magnetic stimulation. These deficits--stated as reduced intracortical inhibition in ADHD and shortened cortical silent period in TD--could be seen as neurophysiological correlates of motor hyperactivity and tics, respectively. To investigate neurophysiological aspects of comorbidity, we measured motor system excitability for the first time also in children with combined ADHD and TD. The findings of a reduced intracortical inhibition as well as a shortened cortical silent period in these comorbid children provide evidence for additive effects at the level of motor system excitability.     

Influence of handedness on peripheral auditory asymmetry

It is well established that in humans many differences between right- and left-handers, anatomical, physiological and functional, exist. Left- and mixed-handedness is associated with greater bihemispheric representation of cognitive functions than in right-handers. Several studies indicate a left–right asymmetry in the function of hearing pathways between cochlea and auditory cortex, and furthermore, that this asymmetry is associated with handedness. Our investigation focuses on the medial olivo-cochlear system, which has been demonstrated to be more effective in the right than left ear in right-handers. The aim of the study was to investigate this auditory efferent system asymmetry according to handedness, gender, eyedness, footedness and the presence of spontaneous otoacoustic emissions. The medial efferent system has been found to be more effective in the right than left ear in right-handers, while functioning symmetrically in left-handers. Furthermore, the olivo-cochlear system, assumed to be involved in basic language processing, shows an asymmetrical pattern of functioning influenced by handedness as well as by hemispheric language representation. Reverse medial efferent system asymmetry was observed in left-handers compared to that in right-handers, on condition that only left-handed males were considered, or that the left-handers were also left-eyed, or that spontaneous otoacoustic emissions were present in the left ear of the left-handers, or when only left-handers without mixed-handers were considered.     

Ipsilateral motor activation during unimanual and bimanual motor tasks.

OBJECTIVE: To test for the presence and possible asymmetry of ipsilateral motor activation during unimanual and bimanual motor tasks. METHODS: Twelve right-handed healthy subjects underwent motor evoked potential (MEP) measurement of one hand (target-hand) while the other hand (task-hand) performed different motor tasks. The target-hand was either at rest (first experiment) or performed a Perdue PegBoard task (second experiment). The task-hand was either at rest, performed a simultaneous pegboard task, or rotated a coin (second experiment). RESULTS: In the first experiment, the motor task resulted in significant increase in MEP area in the target-hand, regardless which hand was the task-hand, with a greater increase when the left hand was the task-hand. In the second experiment, ipsilateral motor activation was not present for either hand, however, when the right hand was the task-hand, performance of continuous coin rotation by the right hand resulted in a significant decrease in the MEP area of the left hand. CONCLUSIONS: Hemispheric asymmetry and task-dependence of ipsilateral motor cortex activation supports the postulate that motor activity may start bilaterally with subsequent interhemispheric inhibition. Furthermore, in right-handers, the left motor cortex is either more active in ipsilateral hand movements or exerts more effective inhibitory control over the right motor cortex than vice versa. SIGNIFICANCE: We suggest that hemispheric asymmetry in ipsilateral motor control is a factor in determining motor dominance in right-handed individuals.     

Subtle hemispheric asymmetry of motor cortical inhibitory tone.

OBJECTIVE: To test whether a novel paired transcranial magnetic stimulation (TMS) protocol (J Physiol 545.1 (2002) 153) detects hemispheric differences in motor cortical inhibition. METHODS: Nine right-handers and 8 left-handers participated. Focal paired TMS was applied to the hand area of the dominant (M1-D) or non-dominant motor cortex (M1-ND). Motor evoked potentials (MEP) were recorded from the relaxed contralateral abductor digiti minimi. The first (S1) and second pulse (S2) were separated by 1.5 or 2.1 ms. Nine stimulus intensities of S1 and S2 (i.e. 9x9 intensity conditions) ranging from 60 to 140% of resting motor threshold (RMT) were tested. The interaction between S1 and S2 was expressed by MEP(S1+S2)/(MEP(S1)+MEP(S2))*100%. Values below and above 100% indicate short-interval intracortical inhibition (SICI) and facilitation (SICF), respectively. RESULTS: In right-handers, RMT was lower, SICI was present with fewer intensity conditions and the magnitude of SICI was less in M1-D than M1-ND. No hemispheric asymmetry was found for SICF. Left-handers showed no hemispheric difference for any of these measures. CONCLUSIONS: Findings suggest that, in right-handers, M1-D is controlled by less inhibitory tone than M1-ND. This may put the M1-D to an advantage for processes that are associated with a reduction of SICI, such as voluntary activation and use-dependent plasticity.     

Handedness, laterality and the size-weight illusion

The goal of this study was to determine how handedness and lifting hand influence the way in which we lift objects and perceive their weights. To this end, we examined the fingertip forces and perceptual judgements of 30 left-handers and 30 right-handers during lifts of specially constructed ‘size-weight illusion’ (SWI) cubes with their left and right hands. All participants completed a series of lifts first with one hand and then the other, so we could additionally examine asymmetries in the retention and transfer of force information between the limbs. Right-handers experienced a larger illusion with their left hand than they did with their right hand, whereas left-handers showed no such asymmetry in their illusions. The perceptual illusion’s independence from the application of fingertip force was highlighted by an unexpected lack of asymmetry in terms of fingertip force scaling. Left- and right-handers showed no dominant hand advantage in this task – they were no more skilled at correcting their fingertip force errors with their preferred hand than they were with their non-preferred hand. In addition, although no asymmetries were observed with regard to the most efficient direction of intermanual transfer, the right-handed individuals transferred force information between the hands more effectively than the left-handers. Overall, these findings indicate that hand dominance does not affect the control of the fingertip forces, suggesting that existing models of cerebral laterality must be re-visited to consider kinetic (i.e., related to forces), as well as kinematic (i.e., related to movement) variables.     

Avowed, assessed, and familial handedness and differential hemispheric processing of brief sequential and non-sequential visual stimuli

Right-handers with no family history of left-handedness (RHFH-), right-handers with such history (RHFH+), and left-handers (LH) were tested on a lateralized letter masking task. Only the RHFH - group showed significant right visual field superiority on the masking task. The results would seem to reflect interhemispheric communication efficiency rather than which hemisphere is dominant for language expression.     

Age-dependent changes in physiological threshold asymmetries for the motor evoked potential and silent period following transcranial magnetic stimulation

OBJECTIVE: To study the effect of age on the physiological threshold asymmetries for the motor evoked potential (MEP) and silent period (SP) following transcranial magnetic stimulation. METHODS: We studied 63 right-handed subjects and 13 young left-handed subjects (19-39 years). The right-handers were classified into three age groups; 22 young (20-38 years), 20 middle-aged (40-58 years) and 21 old (61-82 years) subjects. We measured the MEP thresholds at rest and during voluntary contraction (VC), and the SP thresholds from the right and left abductor pollicis brevis (APB) muscles. We also measured the side to side differences of the F wave persistency and the F wave/M wave amplitude ratio from the same muscles. RESULTS: Among young subjects, all of the MEP and SP thresholds for the right APB were significantly lower than those for the left APB in the right-handers, and the reverse was true in the left-handers. The results in the middle-aged right-handers were similar to those in the young right-handers, but in the old right-handers, none of the thresholds were different between the two sides. We did not find any asymmetries of the F wave in the subjects of any age group. CONCLUSION: We speculate that the age-dependent threshold asymmetries are preferentially related to functional asymmetries at the cortical level.