Reduced corticomotor excitability with cyclic passive movement: a study using transcranial magnetic stimulation

Human voluntary movement involves the integration of kinaesthetic information with efferent motor activity during the planning and execution stages of movement. While much is known of the inhibitory and excitatory effects resulting from activation of specific kinaesthetic sensory receptors, in the present study we employed cyclic passive movement of the index finger in order to activate a range of kinaesthetic receptors in a manner that was intended to correspond to how these receptors might be active during a comparable voluntary movement. We intended to identify how this passive movement protocol might affect the excitability of the corticomotor pathway. During 1 Hz cyclic passive movement of the index finger there was an approximately 60% reduction in the amplitude of the motor evoked response from the first dorsal interosseous muscle. The results of the present study demonstrate that passive movement can have a profound effect on the excitability of the corticomotor pathway.     

Modulations of use-dependent excitability changes of human motor cortex (M1) by practice condition

Effects of repetitive index finger abductions on excitability changes in the human primary motor cortex (Ml) are assumed to be dependent on practice conditions of the task. To address how different effects occur dependent on various practice conditions, motor evoked potentials (MEPs) elicited from the first dorsal interosseous (FDI) muscle were investigated. Practice effects on the index finger abduction were examined for changes in excitability of first dorsal interosseous muscle under three forearm position changes (neutral vs prone) and two muscle contraction modes (isometric vs isotonic). Analysis showed that after practice MEP amplitude increased in the prone position but not in the neutral position and MEP increases in the isotonic contraction were larger than those in the isometric mode. These results suggest that use-dependent excitability changes are largely dependent on practice conditions because the amount of afferent input depends on the practice conditions.     

The Effect of Paired Muscle Stimulation on Preparation for Movement

Paired muscle stimulation is used clinically to facilitate the performance of motor tasks for individuals with motor dysfunction. However, the optimal temporal relationship between stimuli for enhancing movement remains unknown. We hypothesized that synchronous, muscle stimulation would increase the extent to which stimulated muscles are concurrently prepared for movement. We validated a measure of muscle-specific changes in corticomotor excitability prior to movement. We used this measure to examine the preparation of the first dorsal interosseous (FDI), abductor digiti minimi (ADM), abductor pollicis brevis (APB) muscles prior to voluntary muscle contractions before and after paired muscle stimulation at four interstimulus intervals (0, 5, 10, and 75 ms). Paired muscle stimulation increased premovement excitability in the stimulated FDI, but not in the ADM muscle. Interstimulus interval was not a significant factor in determining efficacy of the protocol. Paired stimulation, therefore, did not result in a functional association being formed between the stimulated muscles. Somatosensory potentials evoked by the muscle stimuli were small compared to those commonly elicited by stimulation of peripheral nerves, suggesting that the lack of functional association formation between muscles may be due to the small magnitude of afferent volleys from the stimulated muscles, particularly the ADM, reaching the cortex.     

Time and direction preparation of the long latency stretch reflex

This study investigated time and direction preparation of motor response to force load while intending to maintain the finger at the initial neutral position. Force load extending or flexing the index finger was given while healthy humans intended to maintain the index finger at the initial neutral position. Electromyographic activity was recorded from the first dorsal interosseous muscle. A precue with or without advanced information regarding the direction of the forthcoming force load was given 1000 ms before force load. Trials without the precue were inserted between the precued trials. A long latency stretch reflex was elicited by force load regardless of its direction, indicating that the long latency stretch reflex is elicited not only by muscle stretch afferents, but also by direction-insensitive sensations. Time preparation of motor response to either direction of force load enhanced the long latency stretch reflex, indicating that time preparation is not mediated by afferent discharge of muscle stretch. Direction preparation enhanced the long latency stretch reflex and increased corticospinal excitability 0–20 ms after force load when force load was given in the direction stretching the muscle. These enhancements must be induced by preset of the afferent pathway mediating segmental stretch reflex.     

Facilitation of corticospinal excitability during motor imagery of wrist movement with visual or quantitative inspection of EMG activity

The present study investigated facilitation of corticospinal excitability during motor imagery of wrist movement with visual or quantitative inspection of background electromyographic (EMG) activity. Ten healthy participants imagined wrist extension from a first-person perspective in response to a start cue. Transcranial magnetic stimulation was delivered to the motor cortex 2 sec. after the start cue. EMG signals were recorded from the extensor carpi radialis muscle. Trials with background EMG activity were discarded based on visual inspection. Both motor-evoked potential (MEP) and background EMG amplitudes increased during motor imagery. The amount of increase in MEP amplitude was positively correlated with the amount of increase in background EMG amplitude during motor imagery. The statistically significant increase in MEP amplitude during motor imagery disappeared when the effect of muscle activity was statistically eliminated or after trials with background EMG activity were discarded based on strict quantitative criteria. Facilitation of corticospinal excitability during motor imagery of wrist movement depends partially on muscle activity. Discarding background EMG activity during motor imagery based on visual inspection is not sufficient to equalize background EMG amplitude between resting and motor imagery. Discarding trials with background EMG activity through strict quantitative criteria is useful to equalize background EMG amplitude between at rest and during motor imagery.     

Impaired modulation of corticospinal excitability following subthreshold rTMS in focal hand dystonia

Previous studies have demonstrated that subthreshold 1 Hz repetitive transcranial magnetic stimulation (rTMS) causes a decrease in corticospinal excitability in neurologically normal subjects. The effects of subthreshold 1 Hz rTMS upon corticospinal excitability and intracortical inhibition in subjects with focal hand dystonia (FHD) is not yet clear. The purpose of this study was to examine the effects of low intensity 1 Hz rTMS upon these variables in control and FHD subjects. We recorded electromyographic (EMG) from the first dorsal interosseous (FDI) muscle of the dominant hands of seven control subjects, and seven affected hands of five FHD subjects. We used single and paired pulse TMS to examine motor evoked potential (MEP) amplitude, short interval intracortical inhibition (ICI) and silent period duration before, during and after 20 min of low intensity 1 Hz rTMS. MEP amplitude decreased significantly over the course of the rTMS in control subjects, but did not change in FHD subjects. Silent period duration was significantly longer in control subjects after rTMS, but there was no change in FHD subjects. There was no significant change in ICI after rTMS in either subject group, despite the rTMS intensity being set to preferentially activate intracortical inhibitory networks. This suggests that low intensity 1 Hz rTMS may have limited application in the normalisation of inhibitory function in FHD.     

Temporal aspects of passive movement-related corticomotor inhibition

We have previously shown that during rhythmic passive movement of the index finger, the amplitude of the motor evoke potential (MEP) of the first dorsal interosseous muscle (FDI) as the index finger moved through mid-range adduction, is significantly reduced compared to rest [Edwards, D. J., Thickbroom, G. W., Byrnes, M. L., Ghosh, S., & Mastaglia, F. L. (2002). Reduced corticomotor excitability with passive movement: A study using Transcranial Magnetic Stimulation. Human Movement Science 21, 533-540]. In the present study we have investigated the time-course of this phenomenon. We found that MEP amplitude was significantly reduced at the mid-range position in the first cycle of movement (50+/-6% of resting baseline values), and did not vary across subsequent cycles (10 cycles in 50 s), but that MEP amplitude returned to baseline values within 1s of cessation of movement. The results suggest that the pattern of afferent discharge set up by the kinematics of the movement acting at spinal or supraspinal levels underlies the inhibition observed, rather than an effect of central origin or a cumulative effect of ongoing cyclic movement.     

Attention focus modulates afferent input to motor cortex during skilled action

Psychomotor studies have identified a key role for attention in skill performance and acquisition. However, the neural mechanisms that underpin attention's role in motor control are not well understood. The current study investigated the differential effects of focus of attention upon short-latency afferent inhibition (SAI). SAI was chosen as it is positively correlated with the amount of sensory afference reaching the cortex. SAI is also sensitive to cholinergic influence, the same neurotransmitter involved in regulating attention, and is known to interact with other intracortical networks in the motor cortex. SAI in the first dorsal interosseous muscle was assessed while two separate groups produced the same physical sequential skill represented as a series of response key colors (external focus) or response fingers (internal focus). SAI was assessed at rest, immediately preceding, one element before or two elements before an index finger response. Compared to rest, both attention focus groups demonstrated a reduction in first dorsal interosseous SAI across the three sequence elements. However, the relative magnitude of SAI was greater under an internal focus of attention as an index finger response approached. This pattern indicates an attentional enhancement of somatosensory afference when attention is directed to a bodily dimension that counters the typical movement-related suppression of SAI. The current results support contemporary theories of attention's role in motor control, where an external focus of attention promotes a cortical state that maximizes effector coordination to maximize motor outcome.     

Rapid plastic changes of human primary motor cortex with repetitive motor practice and transcranial magnetic stimulation

Excitability changes of human primary motor cortex are assumed to be associated with motor learning processes. To examine motor behavioral and neural mechanisms in these processes, the adaptive motor learning processes of the index finger abduction were investigated using motor evoked potential (MEP) elicited from the first dorsal interosseous and extensor carpi radialis muscles. Practice effects were examined on changes of MEP amplitudes elicited from these muscles during motor imagery. Given general consensus that the MEP amplitude change during motor imagery is a useful parameter reflecting changes in excitability of the human primary motor cortex, the present results, that MEP amplitudes of both muscles increased with repeated practice by the index finger abduction and that magnitudes of MEP amplitudes of both muscles (motor learning curves) were clearly different, suggested that participation of the muscles performing the index finger abduction gradually changed with practice. Short-term plastic changes of human primary motor cortex occur with repetitive practice and such adaptive change in human primary motor cortex is expressed in human voluntary movement that becomes more automatic.     

Interindividual Variability in Use-Dependent Plasticity Following Visuomotor Learning: The Effect of Handedness and Muscle Trained

Motor learning has been linked with increases in corticospinal excitability (CSE). However, the robustness of this link is unclear. In this study, changes in CSE associated with learning a visuomotor tracking task were mapped using transcranial magnetic stimulation (TMS). TMS maps were obtained before and after training with the first dorsal interosseous (FDI) of the dominant and nondominant hand, and for a distal (FDI) and proximal (biceps brachii) muscle. Tracking performance improved following 20 min of visuomotor training, while map area was unaffected. Large individual differences were observed with 18%–36% of the participants revealing an increase in TMS map area. This result highlights the complex relationship between motor learning and use-dependent plasticity of the motor cortex.     

Effects of proprioceptive neuromuscular facilitation on the initiation of voluntary movement and motor evoked potentials in upper limb muscles

To better understand the mechanisms behind proprioceptive neuromuscular facilitation (PNF), an important method in motor rehabilitation, we investigated the effects of assuming a PNF posture relative to a neutral posture on the initiation of voluntary movement (Experiment 1) and the excitability of the motor cortex (Experiment 2) using a wrist extension task. The initiation of voluntary wrist movement was operationalized in terms of the electromyographic reaction time (EMG-RT), and the excitability of the motor cortex in terms of motor evoked potentials (MEPs). Compared to the neutral position, we found that (1) the facilitation position changed the muscle discharge order enhancing the movement efficiency of the joint, (2) the facilitation position led to a reduction in EMG-RT, the magnitude of which depended on the proximity of the muscle to the movement joint, and (3) MEP amplitude increased and MEP latency decreased in the facilitation position as a function of the proximity of the muscle to the joint. These findings corroborate the presumed effects of PNF and provide insights into the neurophysiological mechanisms underlying the PNF method.     

Difference in Cortical Relay Time Between Intrinsic Muscles of Dominant and Nondominant Hands

The authors aimed to calculate and compare cortical relay time (CRT) between intrinsic hand muscles and between homonymous muscles of dominant and nondominant hands. The participants comprised 22 healthy volunteers. The CRT for long-latency reflexes (LLRs) was calculated by subtracting the peak latency of somatosensory evoked potentials of component N20 and the onset latency of motor evoked potentials from the onset latency of LLRs. CRT was significantly shorter for the first dorsal interosseous muscle than for the abductor pollicis brevis muscle, regardless of hand dominance. CRT for the abductor pollicis brevis muscle was significantly shorter in the dominant hand than in the nondominant hand. Evaluation of CRT for intrinsic muscles might be beneficial in the understanding of individuated finger functions.     

Sex comparisons of the bilateral deficit in proximal and distal upper body limb muscles

Bilateral deficit (BLD) describes a phenomenon that the force produced during maximal simultaneous bilateral contraction is lower than the sum of those produced unilaterally. The aim of this study was to examine the potential sex-related differences in BLD in upper body proximal and distal limb muscles. Ten men and eight women performed single-joint maximal contractions with their elbow flexors and index finger abductors at separate laboratory visits, during which the maximal isometric voluntary contractions (MVICs) were performed unilaterally and bilaterally with a randomized order in the designated muscle group. Surface electromyographic (EMG) signals were recorded from the prime movers of the designated muscle groups (biceps brachii and first dorsal interosseous) during the maximal contractions. Both men and women demonstrated BLD in their elbow flexors (deficit: men = −11.0 ± 6.3%; women = −10.2 ± 5.0%). Accompanied by this force deficit was the reduced EMG amplitude from the dominant biceps brachii (collapsed across sex: p = 0.045). For the index finger abductors, only men (deficit = −13.7 ± 6.1%), but not women showed BLD. Our results suggested that the BLD in the proximal muscle group is likely induced by the decreased maximal muscle activity from the dominant prime mover. The absence of BLD in women’s index finger muscle is largely due to the inter-subject variability possibly related to the sex hormone flux and unique levels of interhemispheric inhibition.     

Premovement posture and focal movement velocity affects on postural responses accompanying rapid arm movement

Coordination of intentional upper limb movement concurrent with supporting postural activity was investigated in adult males under varying task conditions. Seven subjects performed a 60 deg rapid elbow flexion (focal movement) to a target in movement times of 170, 195, or 220 ms while standing. Measurement of center of pressure via a force platform revealed that subjects adopted individual premovement postural preferences such that locus of center of pressure resided in one predominant quadrant of the foot. Each premovement postural preference was accompanied by one most common postural muscle onset sequence as indicated by bilateral EMG analysis of rectus femoris and biceps femoris. In addition, onset times for postural muscles exhibiting anticipatory postural activity occurred earlier relative to biceps branchii as focal movement velocity increased. The finding that each premovement postural condition was accompanied by one particular postural muscle onset sequence suggested that postural synergies were flexibly organized with respect to onset sequence.     

Movement related EMGs become more variable during learning of fast accurate movements

Human subjects performed simple flexion and extension movements about the elbow in a visual step-tracking paradigm. Movements were self-terminated. Subjects were instructed to increase movement velocity while maintaining end-point accuracy during practice. The effects of practice on the pattern and variability of EMG activity of the biceps and triceps muscles were studied. Initial movements were performed using reciprocal phasic activation of agonist and antagonist muscles as indicated by surface EMGs. With practice, increases in movement speed were associated with larger agonist and antagonist bursts and an earlier onset of the antagonist burst. Decreased duration of the premovement antagonist silence was also observed during practice. Decreases in variability of movements during practice were not accompanied by equivalent decreases in variability of the associated EMGs. Surprisingly, both agonist and antagonist EMGs were more variable in faster, practiced movements. The combined agonist-antagonist EMG variability depended on both movement speed and trajectory variability. Lower variability in movements in the presence of greater variability in the related EMGs occurred because of linked variations in agonist and antagonist muscle activities. Variations in the first agonist burst were often compensated for by associated variations in the antagonist and late agonist bursts. These linked variations maintained the limb trajectory relatively constant in spite of large variations in the first agonist burst. Modifications to impulse-variability models are therefore needed to explain compensations for variability in accelerative impulses (produced by the first agonist burst) by linked variations in impulses for deceleration (produced by the antagonist and late agonist bursts).     

Movement Related EMGs Become More Variable During Learning of Fast Accurate Movements

Human subjects performed simple flexion and extension movements about the elbow in a visual step-tracking paradigm. Movements were self-terminated. Subjects were instructed to increase movement velocity while maintaining end-point accuracy during practice. The effects of practice on the pattern and variability of EMG activity of the biceps and triceps muscles were studied. Initial movements were performed using reciprocal phasic activation of agonist and antagonist muscles as indicated by surface EMGs. With practice, increases in movement speed were associated with larger agonist and antagonist bursts and an earlier onset of the antagonist burst. Decreased duration of the premovement antagonist silence was also observed during practice.

Decreases in variability of movements during practice were not accompanied by equivalent decreases in variability of the associated EMGs. Surprisingly, both agonist and antagonist EMGs were more variable in faster, practiced movements. The combined agonist-antagonist EMG variability depended on both movement speed and trajectory variability. Lower variability in movements in the presence of greater variability in the related EMGs occurred because of linked variations in agonist and antagonist muscle activities. Variations in the first agonist burst were often compensated for by associated variations in the antagonist and late agonist bursts. These linked variations maintained the limb trajectory relatively constant in spite of large variations in the first agonist burst. Modifications to impulse-variability models are therefore needed to explain compensations for variability in accelerative impulses (produced by the first agonist burst) by linked variations in impulses for deceleration (produced by the antagonist and late agonist bursts).     

Musical groove modulates motor cortex excitability: A TMS investigation

Groove is often described as a musical quality that can induce movement in a listener. This study examines the effects of listening to groove music on corticospinal excitability. Musicians and non-musicians listened to high-groove music, low-groove music, and spectrally matched noise, while receiving single-pulse transcranial magnetic stimulation (TMS) over the primary motor cortex either on-beat or off-beat. We examined changes in the amplitude of the motor-evoked potentials (MEPs), recorded from hand and arm muscles, as an index of activity within the motor system. Musicians and non-musicians rated groove similarly. MEP results showed that high-groove music modulated corticospinal excitability, whereas no difference occurred between low-groove music and noise. More specifically, musicians’ MEPs were larger with high-groove than low-groove music, and this effect was especially pronounced for on-beat compared to off-beat pulses. These results indicate that high-groove music increasingly engages the motor system, and the temporal modulation of corticospinal excitability with the beat could stem from tight auditory–motor links in musicians. Conversely, non-musicians’ MEPs were smaller for high-groove than low-groove music, and there was no effect of on- versus off-beat pulses, potentially stemming from suppression of overt movement. In sum, high-groove music engages the motor system, and previous training modulates how listening to music with a strong groove activates the motor system.     

Relationships between movement initiation times and movement-related cortical potentials in Parkinson's disease

Movement-related cortical potentials recorded from the scalp reveal increasing cortical activity occurring prior to voluntary movement. Studies of set-related cortical activity recorded from single neurones within premotor and supplementary motor areas in monkeys suggest that such premovement activity may act to prime activity of appropriate motor units in readiness to move, thereby facilitating the movement response. Such a role of early stage premovement activity in movement-related cortical potentials was investigated by examining the relationship between premovement cortical activity and movement initiation or reaction times. Parkinson's disease and control subjects performed a simple button-pressing reaction time task and individual movement-related potentials were averaged for responses with short compared with long reaction times. For Parkinson's disease subjects but not for the control subjects, early stage premovement cortical activity was significantly increased in amplitude for faster reaction times, indicating that there is indeed a relationship between premovement cortical activity amplitude and movement initiation or reaction times. In support of studies of set-related cortical activity in monkeys, it is therefore suggested that early stage premovement activity reflects the priming of appropriate motor units of primary motor cortex, thereby reducing movement initiation or reaction times.PsycINFO classification: 2330; 2520; 2530     

Vibration-Induced Kinesthetic Illusions and Corticospinal Excitability Changes

The authors' aim was to investigate the changes of corticospinal excitability during kinesthetic illusions induced by tendon vibration. Motor-evoked potentials in response to transcranial magnetic stimulation were recorded from the vibrated flexor carpi radialis and its antagonist, extensor carpi radialis. The illusions were evoked under vision conditions without feedback for the position of the wrist (open or closed eyes). In these two conditions motor-evoked potential changes during vibration in the antagonist were not identical. This discrepancy may be a result of 2 simultaneously acting, different and opposite influences and the balance between them depends on visual conditions. Thus, the illusion was accompanied by the facilitation of corticospinal excitability in both vibrated muscle and its antagonist.     

Functional lateralization of the human premotor cortex during sequential movements

A neurological truism is that each side of the brain controls movements on the opposite side of the body. Yet some left hemisphere brain lesions cause bilateral impairment of complex motor function and/or ideomotor apraxia. We report that the left dorsal premotor cortex of normal right-handed people plays a fundamental role in sequential movement of both right and left hands. Subjects performed sequential finger movements during functional magnetic resonance imaging of the motor cortices. In right-handed subjects, the volume of activated dorsal premotor cortex showed a left hemispheric predominance during hand movements. We suggest that the observed left premotor dominance contributes to the lateralization found in lesion studies.