J A Stephens

The frequency content of common synaptic inputs to motoneurones studied during voluntary isometric contraction in man.

1. The discharges of pairs of individual motor units were recorded from intrinsic hand muscles in man. Single motor unit recordings were obtained either when both members of the motor unit pair were within first dorsal interosseous muscle (1DI:1DI recordings) or where one motor unit was within 1DI and the other in second dorsal interosseous muscle (1DI:2DI recordings). The pairs of motor unit spike trains were cross‐correlated in the time domain and the results compared to those of coherence analysis performed on the same spike train data. Central peaks were present in the cross‐intensity functions, indicating the presence of common synaptic input to the motoneurone pair. Coherence analysis of these data indicated significant association between motor unit firing in the frequency ranges 1‐12 and 16‐32 Hz. 2. Analysis of sequential non‐overlapping segments of data recorded from individual motor unit pairs, demonstrated that both the central cross‐intensity peak and coherence in the frequency bands 1‐12 and 16‐32 Hz were consistent features throughout a long recording. In these sequential recordings, the size of the central cross‐intensity peak and the maximal value of coherence in the frequency band 16‐32 Hz covaried from segment to segment. Analysis of the entire population of motor unit pairs confirmed a positive relationship between the magnitude of peak coherence and the size of the central cross‐intensity peak. 3. Voluntary sinusoidal co‐modulation of the firing rates of pairs of individual motor units recorded from within 1DI was found to produce significant values of coherence corresponding to the frequency of the common modulation. However, firing rate co‐modulation was not found to affect either the size of the central cross‐intensity peak or the maximum value of coherence in the frequency band 16‐32 Hz. 4. Pairs of single motor units were recorded from within 1DI and biceps brachii muscles of healthy subjects. The number and size of the central cross‐intensity peaks and coherence peaks detected were compared for the two muscles. The incidence and size of central cross‐intensity peaks and the incidence and magnitude of 16‐32 Hz coherence peaks were both found to be greater for 1DI recordings when compared to biceps brachii recordings. 5. Single motor unit recordings were made from the intrinsic hand muscles of a patient with severe peripheral deafferentation. Time‐ and frequency‐domain analysis of these recordings revealed cross‐intensity peaks and frequency bands of coherence similar to those seen in healthy subjects.(ABSTRACT TRUNCATED AT 400 WORDS)

Cutaneous reflex responses and their central nervous pathways studied in man

1. Cutaneous reflex responses have been recorded in human first dorsal interosseous and extensor digitorum brevis muscles following electrical stimulation of the digital nerves of the index finger and second toe respectively.

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.

Mirror movements studied in a patient with Klippel-Feil syndrome.

1. Electromyographic (EMG) recordings have been made from upper limb muscles in a patient with well‐defined congenital mirror movements occurring in association with Klippel‐Feil syndrome and the results compared to those obtained in normal control subjects. 2. In the patient, liminal percutaneous electrical or magnetic brain stimulation applied over either hemisphere elicited bilateral and symmetrical short‐latency muscle responses in relaxed intrinsic hand muscles. In the normal subjects unilateral brain stimulation only elicited contralateral muscle responses. 3. F response and H reflex studies for the patients ulnar‐supplied intrinsic hand muscles were normal. No crossed responses were recorded in the homologous muscles of the contralateral hand. 4. Scalp‐recorded somatosensory‐evoked responses following ulnar or median nerve stimulation were of normal latency and distribution in the patient. 5. In the patient, cross‐correlation analysis of on‐going single and multiunit needle EMGs recorded between muscles of left and right hands revealed a central peak in the cross‐correlogram. No cross‐correlogram peaks were found between left‐ and right‐hand muscles in normal subjects. The magnitude and time course of the central peaks in the cross‐correlograms constructed between the firing of motor units on opposite sides of the body in the patient were similar to those found in cross‐correlograms constructed between the firing of motor units from muscles on the same side of the body in the patient and in normal subjects. 6. The magnitude of cross‐correlogram peaks detected within a muscle and those detected between left and right homologous muscles showed a gradient in which the largest peaks were found in the intrinsic hand and forearm extensor muscles. The smallest peaks were observed in the forearm flexor muscles. No peaks were detected between left and right biceps brachii muscles. In intrinsic hand muscles, the size of the cross‐correlogram peak detected between the EMGs of homologous muscle pairs was greater than that found for non‐homologous muscle pairs. 7. Cutaneous reflex responses were recorded from first dorsal interosseous muscle following unilateral electrical stimulation of the digital nerves of the index finger. In the patient, this produced an early excitatory (E1) response on the stimulated side. Later excitatory (E2 and E3) responses, of approximately equal size and latency, were distributed bilaterally. In the normal subjects, reflex responses were confined to the stimulated side.(ABSTRACT TRUNCATED AT 400 WORDS)

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.

Central nervous pathways underlying synchronization of human motor unit firing studied during voluntary contractions.

1. Motor unit firing has been studied during weak voluntary isometric contractions with pairs of needle electrodes in normal human subjects. 2. Pre‐ and post‐stimulus time histograms of the firing time of firing of one event unit before and after the time of firing of another reference (stimulus) unit showed a clear central peak, indicative of synchronization. 3. Synchronization was seen in all the muscles studied. The mean strength of synchronization, expressed as the number of concomitant discharges of the two units as a proportion of the number of stimulus unit discharges, was 0.095 extra event unit spikes/reference unit spike (range 0.042‐0.28) for first dorsal interosseous muscle, 0.016 extra event unit spikes per reference unit spike (range 0‐0.043) for medial gastrocnemius and 0.056 extra event unit spikes per reference unit spike range 0.016‐0.079) for tibialis anterior. 4. The mean duration of synchronization was 11.3 ms (range 5.0‐21.0 ms) for first dorsal interosseous, 10.3 ms (range 3.5‐21.7 ms) for medial gastrocnemious and 13.5 ms (range 3.0‐25.0) for tibialis anterior. 5. Seven patients with radiographically and clinically identified central strokes were studied while they made weak voluntary isometric contractions. The duration of synchronization was significantly prolonged compared to that found in normal subjects. In these stroke patients the mean duration of synchronization on the affected side was longer than that seen in the normal subjects, and in first dorsal interosseous muscle was 35.4 ms (range 12.0‐65.0 ms), in medial gastrocnemius was 21.3 ms (range 4.0‐43.0 ms) and in tibialis anterior was 28.8 ms (range 14.0‐49.0 ms). 6. The mean strength of synchronization of motor unit discharge was found to be greater in the stroke patients than that seen in the normal subjects for first dorsal interosseous muscle (0.161 extra event unit spikes per reference unit spike, range 0.017‐0.391) and for medial gastrocnemius (0.030 extra event unit spikes per reference unit spike) but only significantly so when pooled data was compared. There was no difference in the strength of motor unit synchronization in tibialis anterior between stroke patients and normal subjects. 7. Broad duration synchronization among first dorsal interosseous motor units was also found in a patient with a rostral cervical spine lesion (total duration range 43‐46 ms; n = 2), but not in a patient with a caudal (thoracic) spinal lesion.(ABSTRACT TRUNCATED AT 400 WORDS)

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.

A review of recent applications of cross-correlation methodologies to human motor unit recording

This article reviews some recent applications of time and frequency domain cross-correlation techniques to human motor unit recording. These techniques may be used to examine the pre-synaptic mechanisms involved in control of motoneuron activity during on-going motor tasks in man without the need for imposed and artificial perturbations of the system. In this review we examine, through several examples, areas in which insights have been gained into the basic neurophysiological processes that bring about motoneuron firing in man and illustrate how these processes are affected by central nervous system pathology. We will demonstrate that synchronization and coherence may be revealed between human motor unit discharges and give examples that support the hypothesis that these phenomena are generated by activity in a focused common corticospinal input to spinal motoneurons. Disruption of central motor pathways due to diseases of the nervous system leads to pathophysiological alterations in the activity of these pre-synaptic motoneuron inputs that can be revealed by cross-correlation analysis of motor unit discharges. The significance of these studies and outstanding questions in this field are discussed.