Linda M. Harrison

A neurophysiological study of mirror movements in adults and children.

The mechanism underlying mirrored activity/movements in normal individuals is unknown. To investigate this, we studied 11 adults and 39 children who performed sequential finger–thumb opposition or repetitive index finger abduction. Surface electromyographic (EMG) activity recorded from the left and right first dorsal interosseous muscles (1DI) during unilateral sequential finger–thumb opposition (voluntarily activated muscle, 1DIvol) showed mirrored EMG activity (homologous muscle of the opposite hand, 1DImm) that decreased with increasing age. The time of onset of involuntary compared with voluntary EMG activity was variable but could start at the same time. A significant increase in E2 (transcortical component) size of the cutaneomuscular reflex recorded from the 1DImm indicated increased excitability of the motor cortex ipsilateral to the 1DIvol during active index finger abduction compared with the 1DIvol relaxed. Transcranial magnetic stimulation, using the Bistim technique, indicated that the transcallosal inhibitory pathway in children may not operate in the same way as in the adult. Cross‐correlation analysis did not detect shared synaptic input to motoneuron pools innervating homologous left and right hand muscles. We conclude that the mirrored movements/activity observed in healthy adults and children are produced by simultaneous activation of crossed corticospinal pathways originating from both left and right motor cortices. Ann Neurol 1999;45:583–594

Plasticity of central motor pathways in children with hemiplegic cerebral palsy

To obtain neurophysiologic evidence for a reorganization of central motor pathways in children who had suffered a cerebral lesion at birth, we performed cross-correlation analyses of multiunit EMG recordings obtained from children with hemiplegic cerebral palsy and marked mirror movements. We found that the motoneuron pools of homologous left and right hand muscles received common synaptic input from abnormally branched presynaptic axons. The results of electromagnetic brain stimulation, cutaneomuscular, and tendon reflex testing suggested that these common inputs are provided by abnormally branched corticospinal tract fibers whose origin is the undamaged motor cortex.

Evidence for bilateral innervation of certain homologous motoneurone pools in man.

1. Surface EMG recordings were made from left and right homologous muscle pairs in healthy adults. During each recording session subjects were requested to maintain a weak isometric contraction of both the left and right muscle. 2. Cross‐correlation analysis of the two multiunit EMG recordings from each pair of muscles was performed. Central peaks of short duration (mean durations, 11.3‐13.0 ms) were seen in correlograms constructed from multiunit EMG recordings obtained from left and right diaphragm, rectus abdominis and masseter muscles. No central peaks were seen in correlograms constructed from the multiunit EMG recordings from left and right upper limb muscles. 3. To investigate descending pathways to the homologous muscle pairs, the dominant motor cortex was stimulated using a focal magnetic brain stimulator whilst recording from homologous muscle pairs. 4. Following magnetic stimulation of the dominant motor cortex, a response was recorded from both right and left diaphragm, rectus abdominis and masseter muscles. In contrast, when recording from homologous upper limb muscles, a response was only seen contralateral to the side of stimulation. 5. The finding of short duration central peaks in the cross‐correlograms constructed from multiunit recordings from left and right diaphragm, rectus abdominis and masseter, suggests that muscles such as these, that are normally co‐activated, share a common drive. The mechanism is discussed and it is argued that the time course of the central correlogram peaks is consistent with the hypothesis that they could be produced by a common drive that arises from activity in last‐order branched presynaptic fibres although presynaptic synchronization of last‐order inputs is also likely to be involved. 6. The results of the magnetic stimulation experiments suggest that this common drive may involve the corticospinal tract. 7. We saw no evidence for a common drive to left and right homologous muscle pairs that may be voluntarily co‐activated but often act independently.

Task‐dependent changes in the size of response to magnetic brain stimulation in human first dorsal interosseous muscle.

1. Electromyographic responses have been recorded from human first dorsal interosseous muscle (FDI) in response to magnetic and transcutaneous electrical stimulation of the brain. 2. Following magnetic but not electrical stimulation of the brain, the recorded EMG response was larger when FDI was active during voluntary isometric index finger abduction than during a power grip. 3. In the same experiment, cutaneous reflex responses have been recorded from FDI following electrical stimulation of the digital nerves. The long‐latency excitatory component at about 60 ms (E2) was larger when recorded during voluntary finger abduction than during a power grip. This difference in size of E2 with task bore no simple relationship to the difference in size with task of the motor response to magnetic brain stimulation. 4. The results are discussed in relation to the presumed site of action of magnetic and electrical brain stimulation. It is concluded that the results may best be interpreted by assuming a higher level of cortical activity during a voluntary index finger abduction than during a grip and that this could in part explain the task‐dependent changes in the long‐latency response to cutaneous stimulation.

Task‐dependent changes in cutaneous reflexes recorded from various muscles controlling finger movement in man.

1. Cutaneous reflex responses have been recorded from muscles involved in the control of finger movement following electrical stimulation of the digital nerves of the fingers in man. 2. Recordings have been made while subjects performed various manual tasks. 3. Reflexes recorded while subjects performed a relatively isolated finger movement consisted of an initial short‐latency increase in muscle electrical activity, followed by a decrease, followed by a prominent longer‐latency increase. The long‐latency excitatory component was smaller or absent during those grips used in the present study. 4. The short‐latency excitatory (E1) and inhibitory (I1) components of the cutaneomuscular reflex response are mediated via spinal pathways. The second longer‐latency excitatory component (E2) is of supraspinal origin, requiring the integrity of the dorsal columns, sensorimotor cortex and corticospinal tract (Jenner & Stephens, 1982). The results of the present study suggest that one or more of these supraspinal pathways is more active when a finger is used in a relatively isolated manner than when the same finger participates in any of the gripping manoeuvres used in the present experiments.

Changes in EMG coherence between long and short thumb abductor muscles during human development

In adults, motoneurone pools of synergistic muscles that act around a common joint share a common presynaptic drive. Common drive can be revealed by both time domain and frequency domain analysis of EMG signals. Analysis in the frequency domain reveals significant coherence in the range 1–45 Hz, with maximal coherence in low (1–12 Hz) and high (16–32 Hz) ranges. The high‐frequency range depends on cortical drive to motoneurones and is coherent with cortical oscillations at ∼20 Hz frequencies. It is of interest to know whether oscillatory drive to human motoneurone pools changes with development. In the present study we examined age‐related changes in coherence between rectified surface EMG signals recorded from the short and long thumb abductor muscles during steady isometric contraction obtained while subjects abducted the thumb against a manipulandum. We analysed EMG data from 36 subjects aged between 4 and 14 years, and 11 adult subjects aged between 22 and 59 years. Using the techniques of pooled coherence analysis and the χ2 difference of coherence test we demonstrate that between the ages of 7 and 9 years, and 12 and 14 years, there are marked increases in the prevalence and magnitude of coherence at frequencies between 11 and 45 Hz. The data from subjects aged 12–14 years were similar to those obtained from adult controls. The most significant differences between younger children and the older age groups were detected at frequencies close to 20 Hz. We believe that these are the first reported results demonstrating significant late maturational changes in the ∼20 Hz common oscillatory drive to human motoneurone pools.

Organization of inputs to motoneurone pools in man.

1. Surface EMGs were recorded from pairs of muscles involved in movements of the wrist and/or digits in the upper limb and from pairs of intrinsic foot muscles in the lower limb during voluntary isometric contractions. 2. EMGs were also recorded from lower limb and trunk muscles during three different tasks: lying, standing and balancing. 3. To investigate if the co‐contraction of muscles was due to the presence of a common drive to each of the two motoneurone pools, cross‐correlation analysis of the two multiunit EMG signals was used. 4. Evidence for a common drive was seen between pairs of muscles that share a common joint or joint complex (such as the metacarpophalangeal joints); no evidence was found for a common drive to co‐contracting muscles that did not share a common joint. 5. When considering analogous hand and foot muscle pairs, the degree of synchrony was significantly greater for lower limb pairs. 6. Where a common drive was detected with lower limb muscle pairs, the degree of synchrony was significantly larger during balancing than during either lying or standing. 7. The origin of the common drive is discussed. It is concluded that activity in both last‐order branched presynaptic fibers and presynaptic synchronization is involved.

Cutaneomuscular reflexes recorded from the lower limb in man during different tasks.

1. Cutaneomuscular reflexes have been recorded in ten adult subjects from extensor digitorum brevis (EDB), tibialis anterior (TA), soleus (Sol), quadriceps femoris (Quad) and erector spinae (ES) following electrical stimulation of the digital nerves of the second toe. 2. Recordings were made while subjects were instructed to activate voluntarily the relevant muscles and also when these muscles were active posturally. 3. Reflex responses could comprise three components: an initial increase in EMG (E1), followed by a decrease (I1), followed by a second increase (E2). E1 and I1 were confined to muscles acting at the ankle and in the foot. E2 was most pronounced in EDB but also found in TA, Sol, Quad (1 subject) and ES. No responses were recorded contralateral to the stimulus. 4. E2 was significantly larger when the reflex was recorded during voluntary contraction of the muscle, rather than when the muscle was active posturally. 5. E1 and I1 components are mediated via spinal pathways. E2 requires the integrity of the dorsal columns, sensorimotor cortex and corticospinal tract (Jenner & Stephens, 1982; Rowlandson & Stephens, 1985b). The present study suggests that one or more of these supraspinal pathways is more active during voluntary contraction of lower limb muscles than when these muscles are active posturally.

Cross-correlation analysis of motor unit activity recorded from two separate thumb muscles during development in man.

1. Multi‐unit surface EMG signals were recorded from the short and long thumb abductor muscles of seventy‐five children aged from 4 to 15 years and from nine adults during simultaneous abduction and extension of the left and right thumb. Ability to perform independent finger movements was investigated by timing a series of sequential finger‐to‐thumb oppositions. 2. Cross‐correlograms were constructed from the discharges of motor units recorded from the long and short abductor muscles acting on the same thumb. In the majority of subjects, short duration central peaks were present indicating the presence of a common drive to the motoneurone pools innervating these two muscles. Except for those subjects aged 4 and 5 years, the size of these central correlogram peaks did not differ significantly between the dominant and non‐dominant hands. 3. The prevalence of central cross‐correlogram peaks in different subjects increased from the age of 4 years to 15 years. The size of the central cross‐correlogram peak increased with age up to 10 years but did not alter significantly after this age. The duration of the central peak steadily decreased over the age range of 4 to 15 years. 4. Multilinear regression analysis of data recorded from children revealed that there was a positive, but weak, correlation between the size of the cross‐correlogram peak and the rate of performance of sequential finger movements after having controlled for age.

Physiological tremor in human subjects with X-linked Kallmann's syndrome and mirror movements

1 Human physiological tremor consists of mechanical‐reflex and neurogenic components. The origin of the neurogenic component, classically detected in the frequency range 7‐12 Hz, has been much debated. We have studied six subjects with X‐linked Kallmanns syndrome (XKS) and mirror movements. In these subjects unilateral magnetic brain stimulation results in abnormal bilateral EMG responses. Furthermore, abnormal sharing of central nervous inputs between the left and right motoneurone pools results in both abnormal motor unit synchronisation between left and right EMGs and abnormal sharing of long but not short‐latency cutaneomuscular reflexes. XKS subjects with mirror movements thus provide a model for studying the central origin of physiological tremor. 2 During sustained co‐extension of the left and right index fingers, simultaneous finger tremor and extensor indicis (EI) EMGs were recorded and cross‐correlated. The tremor and EMG signals were also subjected to time and frequency domain analysis. 3 Results of frequency domain analysis between ipsilateral finger tremor and EI EMG were similar for both control and XKS subjects. However, in contrast to the controls, short‐term synchronisation of left and right EI motor unit activity and significant coherence between left and right EMG, left and right tremor, left EMG and right tremor and right EMG and left tremor were found in XKS subjects. The frequency range (6‐40 Hz) and coherence values between left and right were similar to ipsilateral coherence values of rectified EMG and tremor. 4 These data provide strong evidence to support the hypothesis that the neurogenic component of physiological tremor is supraspinal in origin and ranges from 6 to 40 Hz.