The use of transcranial magnetic stimulation for monitoring descending spinal cord motor function.

This report describes our initial clinical experience using transcranial magnetic stimulation for monitoring spinal cord motor function during surgical procedures. Motor evoked potentials were elicited using a cap shaped coil placed on the scalp of 27 patients while recording peripheral motor responses (compound muscle action potentials--CMAPs) from the upper (N = 1) or lower limbs (N = 26). Wherever possible, cortical somatosensory responses (SEPs) were also monitored by electrically stimulating the left and right posterior tibial nerve (N = 25) or the median nerve (N = 1). The judicious choice of anesthetic regimens resulted in successfully obtaining motor evoked responses (MEPs) in 21 of 27 patients and SEPs in 26 of 27 patients. Single pulse TMS resulted in peripheral muscle responses having large variability, whereas, the variability of SEPs was much less. Criteria based on response variability for assessing clinically significant changes in both MEPs and SEPs resulted in two false negative predictions for SEPs and none for MEPs when evaluating postoperative motor function. We recommend monitoring both sensory and motor pathways during procedures where placing the spinal cord at risk of damage.     

Modality-related scalp responses after electrical stimulation of cutaneous and muscular upper limb afferents in humans

To elucidate whether the selective electrical stimulation of muscle as well as cutaneous afferents evokes modality-specific responses in somatosensory evoked potentials (SEPs) recorded on the scalp of humans, we compared scalp SEPs to electrical stimuli applied to the median nerve and to the abductor pollicis brevis (APB) motor point. In three subjects, we also recorded SEPs after stimulation of the distal phalanx of the thumb, which selectively involved cutaneous afferents. Motor point and median nerve SEPs showed the same scalp distribution; moreover, very similar dipole models, showing the same dipolar time courses, explained well the SEPs after both types of stimulation. Since the non-natural stimulation of muscle afferents evokes responses also in areas specifically devoted to cutaneous input processing, it is conceivable that, in physiological conditions, muscle afferents are differentially gated in somatosensory cortex. The frontocentral N30 response was absent after purely cutaneous stimulation; by contrast, it was relatively more represented in motor point rather than in mixed nerve SEPs. These data suggest that the N30 response is specifically evoked by proprioceptive inputs.     

High voltage electrical stimulation of the proximal hypoglossal nerve in normal subjects.

OBJECTIVES: It is often difficult to stimulate the proximal hypoglossal nerve by magnetic occipital stimulation, even in normal subjects. Therefore, we tested an improved method of stimulating the proximal hypoglossal nerve, using high voltage electrical stimulation. METHODS: The proximal hypoglossal nerve was activated by high voltage electrical stimulation using surface electrodes over the occipital skull. The compound muscle action potential (CMAP) was recorded from the lingual muscles using surface electrodes in 10 normal subjects. CMAP and F waves produced by distal hypoglossal nerve stimulation and motor evoked potentials produced by transcranial magnetic stimulation were also recorded. RESULTS: When the anode electrode was placed at the mastoid process and the cathode below the inion, the unilateral proximal hypoglossal nerve was readily stimulated supramaximally in all the subjects. The CMAP latency was the same as that obtained with magnetic occipital stimulation. The central motor conduction time (CMCT) calculated from the proximal CMAP was 4.1+/-0.4 ms in the contralateral corticobulbar tract and 4.4+/-0.4 ms in the ipsilateral. The CMCT calculated from the minimal F wave latency was 3.3+/-0.2 ms. CONCLUSIONS: The high voltage electrical stimulation is a useful method for stimulating the proximal hypoglossal nerve to estimate the CMCT of the corticobulbar tract.     

Brain excitability and long latency muscular arm responses: non-invasive evaluation in healthy and parkinsonian subjects.

Thirty healthy and 35 volunteers affected by Parkinson's disease (PD) were examined. Long latency responses (LLRs) and short latency somatosensory evoked potentials (SEPs) after median nerve stimulation were respectively recorded from forearm flexor muscles, and from 19 scalp electrodes, during relaxation (condition 1), light and maximal muscle contraction (conditions 2 and 3). Linear interpolation of SEPs was performed to produce isopotential colour maps. Latencies and amplitudes of the V1-V2 component in LLR, as well as of parietal, central and frontal scalp SEPs were analysed in the 3 experimental conditions. Highly significant inverse correlation matched the frontal SEP to the LLR V2 component amplitudes, both in healthy and in PD subjects. However, the V2 component--which in the former group was reliably identifiable only in condition 3--was presented in conditions 1 and 2 in a high percentage of PD subjects who also showed an abnormally reduced frontal SEP during complete relaxation. Excitability changes of brain motor areas induced by a sensory input were tested as follows: the motor cortex was transcranially stimulated (TCS) by magnetic pulses with an intensity 10% below (A) or above (B) the threshold for twitch elicitation during complete relaxation of forearm muscles; TCS was randomly preceded (range 14-32 msec) by a shock to the median or ulnar nerve at the elbow with identical characteristics as for LLR elicitation. An initial epoch of 'inhibition' followed by a peak of 'facilitation' of the amplitude of motor responses to TCS was observed when conditioning stimuli to the median nerve preceded TCS by 14-20 and by 24-32 msec, respectively. Contrary to normals, conditioning stimulation of the median nerve did not significantly influence the excitability threshold to TCS in those parkinsonians with depressed frontal N30.     

Neuromuscular consequences of prolonged hunger strike: an electrophysiological study.

OBJECTIVES: The purpose of this study was to determine the electrophysiological consequences of neuromuscular and central nervous system involvement in a group of patients presented with the neurological complications of a long-term hunger strike (HS). METHODS: Motor and sensory nerve conduction (NCV), F wave, somatosensory evoked potential (SEP) and motor evoked potential (MEP) studies were performed in 12 male and 3 female patients (mean age: 29.4) following HS. RESULTS: All patients whose weight loss was 11-31 (mean: 22.8) kg after 69-day HS, had neurological findings consistent with Wernicke's encephalopathy or Wernicke-Korsakoff syndrome. Abnormally prolonged latency and/or low amplitude sensory nerve action potentials were found in 7 patients. The amplitudes of compound muscle action potentials were significantly reduced in ulnar, median and tibial motor NCV studies as compared to the controls. F waves elicited by median nerve stimulation at wrist and muscle responses evoked by cervical and lumbar magnetic stimulation had significantly prolonged latencies. MEPs recorded from the lower extremities showed a slight prolongation in central conduction times. The cortical response latencies were prolonged in tibial SEPs. CONCLUSIONS: The most prominent finding in this patient group was the low amplitude of CMAPs elicited in motor NCV studies which was concluded to be resulted from the reversible muscular changes. The other electrophysiological findings suggested that peripheral nerves and long central nervous system pathways were also mildly involved.     

Unmasking of presynaptic and postsynaptic high-frequency oscillations in epidural cervical somatosensory evoked potentials during voluntary movement.

OBJECTIVE: To investigate the effect of the voluntary movement on the amplitude of the somatosensory evoked potentials (SEPs) recorded by an epidural electrode at level of the cervical spinal cord (CSC). METHODS: Fourteen patients underwent an epidural electrode implant at CSC level for pain relief. After the median nerve stimulation, SEPs were recorded from the epidural electrode and from 4 surface electrodes (in frontal and parietal regions contralateral to the stimulated side, over the 6th cervical vertebra, and on the Erb's point). SEPs were recorded at rest and during a voluntary flexo-extension movement of the stimulated wrist. Beyond the low-frequency SEPs, also the high-frequency oscillations (HFOs) were analysed. RESULTS: The epidural electrode contacts recorded a triphasic potential (P1-N1-P2), whose negative peak showed the same latency as the cervical N13 response. The epidural potential amplitude was significantly decreased during the voluntary movement, as compared to the rest. Two main HFOs were identifiable: (1) the 1200 Hz HFO which was significantly lower in amplitude during movement than at rest, and (2) the 500 Hz HFO which was not modified by the voluntary movement. CONCLUSIONS: The low-frequency cervical SEP component is subtended by HFOs probably generated by: (1) postsynaptic potentials in the dorsal horn neurones (1200 Hz), and (2) presynaptic ascending somatosensory inputs (500 Hz). SIGNIFICANCE: Our findings show that the voluntary movement may affect the somatosensory input processing also at CSC level.     

Nerve conduction during Wallerian degeneration in the baboon

Conduction in the lateral popliteal nerve of the baboon was studied during the course of Wallerian degeneration. Six nerves were examined. In each case the muscle response to nerve stimulation and the ascending nerve action potential were recorded daily until the nerve became inexcitable. The muscle response to nerve stimulation disappeared after four to five days, but ascending nerve action potentials could be recorded for a further two to three days. There was no change in maximal motor conduction velocity or in distal latency until the muscle response to nerve stimulation was severely reduced in amplitude. At this stage there was a consistent increase in distal latency, sometimes associated with a mild reduction in maximal motor velocity in the leg. There was no change in the velocity of ascending nerve action potentials. Histological studies confirmed the presence of degeneration in the terminal parts of the intramuscular nerve fibres at a time when the proximal parts of the same fibres were relatively normal.     

Source generators of the early somatosensory evoked potentials to tibial nerve stimulation: an intracerebral and scalp recording study.

OBJECTIVE: To investigate the location of the cerebral generators of the early scalp somatosensory evoked potentials (SEPs) after tibial nerve stimulation. METHODS: Tibial nerve SEPs were recorded in 15 patients, suffering from Parkinson's disease, who underwent implantation of intracerebral (IC) electrodes in the subthalamic nucleus, in the globus pallidum or in the thalamic ventralis intermediate nucleus. SEPs were recorded both from the scalp surface and from the IC leads. RESULTS: The lemniscal P30 response was recorded by all the electrodes. The IC waveforms included a negative N40IC response, followed by a positive (P50IC) and a negative (N60IC) potential. The N40IC, the P50IC and the N60IC potentials did not differ in latency from the P40, the N50 and the P60 responses recorded by the Cz electrode. In 6 patients, in which SEPs were recorded also during the voluntary movement of the stimulated foot (active gating), an amplitude reduction of the SEP components following the P30 potential was observed during movement at the vertex and in the IC traces. Instead, in the contralateral temporal traces the SEP components (N40temp and P50temp) were not modified by active gating, and in the ipsilateral parietal traces only the positive potentials at about 60ms of latency was decreased. CONCLUSIONS: Two differently oriented generators are active in the contralateral hemisphere at both 40 and 50ms of latency after tibial nerve stimulation. One source is oriented perpendicularly to the mesial hemispheric surface and generates the potentials recorded by the contralateral temporal and the ipsilateral parietal leads; the other dipolar source is radial to the hemispheric convexity, and generates the potentials at the vertex and those recorded by the IC electrodes.     

Estimation of facial central motor delay by electrical stimulation of the motor cortex of the dog.

Central delay time (CD) has been estimated for activation of limb muscles by electrical or transcranial magnetic coil (TMC) stimulation of motor cortex and ventral root outflow. In the present study, we used surface electrical stimulation of the motor cortex of the right hemisphere to produce evoked compound muscle action potentials (CMAP) from the contralateral orbicularis oris (o.r.), and orbicularis oculi (o.c.), in dogs. Monopolar electrical stimulation of the facial nerve at the cerebello-pontine (CP) angle yielded CMAP activation of ipsilateral facial muscles. These latencies when subtracted from those obtained by direct cortical stimulation established CD for activation of the seventh cranial nerve. Preliminary data with single pulse magnetic stimulation at high outputs (greater than 80%) revealed CMAP with onset latencies similar to the direct facial nerve stimulation at the CP angle by electrical means.     

Latencies of peripheral nerve and cerebral evoked responses to air-puff and electrical stimuli

This study examined the latency relationship between mechanically and electrically elicited sensory nerve action potentials (SNAPs) and the somatosensory-evoked potentials (SEPs) they produce. Brief air-puff and electrical stimuli were applied to the tip of the index finger in separate trials and SNAPs from the median nerve at the wrist and SEPs from the scalp were recorded for each stimulus presentation. Air-puff evoked SNAPs were polyphasic, usually consisting of 2 to 4 separate waves, unlike triphasic activity elicited by electrical stimulation. The SEPs produced by these 2 distinct forms of inputs, however, were similar in morphology. The latencies of the initial components of SNAPs and SEPs were longer for air-puff stimulation. The conduction time, however, of the fastest afferent volleys from the wrist to cortex was not significantly different for air-puff (20.52 +/- 1.06 ms, mean +/- SD) and electrical stimulation (20.17 +/- 0.66 ms). It is therefore concluded that the latency delays for air-puff evoked SNAPs and SEPs are due solely to a transduction time at the skin receptors and not due to differences in conduction velocities as suggested in the previous literature.     

Neurophysiological testing in anorectal disorders

The neurophysiological techniques currently available to evaluate anorectal disorders include concentric needle electromyography (EMG) of the external anal sphincter, anal nerve terminal motor latency (TML) measurement in response to transrectal electrical stimulation or sacral magnetic stimulation, motor evoked potentials (MEPs) of the anal sphincter to transcranial magnetic cortical stimulation, cortical recording of somatosensory evoked potentials (SEPs) to anal nerve stimulation, quantification of electrical or thermal sensory thresholds (QSTs) within the anal canal, sacral anal reflex (SAR) latency measurement in response to pudendal nerve or perianal stimulation, and perianal recording of sympathetic skin responses (SSRs). In most cases, a comprehensive approach using several tests is helpful for diagnosis: needle EMG signs of sphincter denervation or prolonged TML give evidence for anal motor nerve lesion; SEP/QST or SSR abnormalities can suggest sensory or autonomic neuropathy; and in the absence of peripheral nerve disorder, MEPs, SEPs, SSRs, and SARs can assist in demonstrating and localizing spinal or supraspinal disease. Such techniques are complementary to other methods of investigation, such as pelvic floor imaging and anorectal manometry, to establish the diagnosis and guide therapeutic management of neurogenic anorectal disorders.     

Short-latency cortical potentials evoked by tactile air-jet stimulation of body and face in man

Natural cutaneous stimulation was performed in 10 healthy volunteers by means of a brief, localized air jet directed to the glabrous skin of the face, finger or toe. Neurograms (from finger stimulation) and somatosensory evoked potentials (SEPs) were recorded and, in the case of finger and toe stimulation, compared with the SEPs obtained by low intensity electrical stimulation. Comparing the latencies at wrist and elbow of the respective neurograms, it appears that a 2 msec period accounts for skin indentation and build-up of the generator potential in the receptors activated by the air jet. A slightly lower conduction velocity was obtained on natural than on electrical stimulation, and the cortical SEPs accordingly had a longer latency. In spite of the much smaller amplitude of the air-jet evoked neurograms, the amplitudes of the SEPs from finger and toe were similar to the amplitudes of the SEPs on electrical stimulation of the same regions. Natural stimulation in the regions innervated by the 3 branches of the trigeminal nerve (tongue included) yielded consistent SEPs, comparable with those reported in the literature to electrical stimulation. These potentials were distinguishable from the electrical activity due to the blink reflex, which invariably takes place on air-jet stimulation of the first trigeminal branch.     

Antidromic corticospinal tract potential of the brain.

OBJECTIVE: To describe a novel potential component (antidromic corticospinal tract potential, ACSP) of the brain after translaminar spinal stimulation of a relaxed patient during scoliosis surgery. To study the origin of this component and to compare its source to known sources of the somatosensory evoked potentials (SEPs). METHODS: We studied 17 consecutive patients during posterior scoliosis surgery. SEPs and ACSPs were elicited by translaminar spinal stimulation at the Th 2 and L 1 levels. ACSPs and SEPs were recorded on the scalp midline. Neurogenic motor evoked potentials (NMEPs) were recorded on the popliteal spaces. Preoperative tibial SEPs were also recorded. RESULTS: ACSP was distinctly separated from the corresponding spinally evoked cortical SEP that showed longer latency than the ACSP. ACSPs decreased and disappeared when stimulation was moved to the caudal direction in the conus region while SEP persisted. In addition, the hemispheric origin of ACSP was confirmed with multichannel midline recordings of the scalp and neck. Thus there was no confusion to the response of nucleus gracilis, corresponding the P 31 response of the tibial nerve SEP. CONCLUSIONS: The origin of ACSP seemed to be in the rostral part of the corticospinal tract. ACSP diminished in the conus region when stimulation was moved caudally and it disappeared when the stimulus was given to the root level. This proves that ACSP is not a response of the somatosensory tract, instead ACSP represents antidromic response of the pyramidal tract. ACSP can be used in monitoring of the motor tracts during scoliosis surgery together with NMEPs.     

Magnetoneurography of evoked compound action currents in human cervical nerve roots.

OBJECTIVE: A measurement protocol for magnetoneurography (MNG) is established which allows the non-invasive localization and tracing of evoked compound action currents propagating along cervical nerve roots in man. METHODS: Inside a magnetically shielded room either both median or both ulnar nerves of healthy subjects were conventionally electrostimulated in alternation. Evoked magnetic responses were recorded using a multichannel SQUID-detector with a planar measuring area centered over the neck. Simultaneously, electric surface potentials were recorded using cervical bipolar electrode montages. RESULTS: Upon median (ulnar) nerve stimulation somatosensory evoked magnetic fields up to 20 fT (10 fT) amplitude were detected propagating over the cervical transforaminal root entry zone, with corresponding electrical surface potentials of 1.5 microV (0.5 microV). Furthermore, the signal-to-noise ratio of the spatiotemporal magnetic field mappings in median nerve stimulation experiments allowed dipolar source reconstructions and tracing of the propagation of the compound action currents along nerve root fibers. CONCLUSION: Magnetoneurography allows tracing of the propagation of evoked compound action currents along cervical roots in healthy subjects with millisecond temporal and high spatial resolution. Thus, MNG offers a sensitivity appropriate to serve as a clinical diagnostic tool for localizing focal neuropathies of cervical nerve roots.     

Modulation of cortical excitability during action observation: a transcranial magnetic stimulation study

Paired-pulse transcranial magnetic stimulation (TMS) was used to examine changes in cortical excitability during action observation. We stimulated the left primary motor cortex (M1) of eight healthy volunteers during rest, observation of handwriting and observation of arm movements. Motor evoked potentials (MEP) were recorded from the first dorsal intereosseous (FDI) and biceps (BIC) muscles. Our results showed that action observation induced a facilitation of the MEP amplitude evoked by the single test stimulus and reduced intracortical inhibition and facilitation at 3 ms and 12 ms interstimulus intervals (ISIs), respectively, during paired-pulse stimulation. These changes were specific for the muscle involved in the observed action. Our study presents further evidence that motor excitability is significantly modified when the subject observes an action performed by another individual.     

Motor evoked potentials (MEPs) in lacunar syndromes.

Motor evoked potentials (MEPs) evoked in the biceps, thenar and tibialis anterior muscles by electrical stimulation of the scalp and of the spinal regions were recorded in 32 patients with focal deficits due to minor cerebral ischemia of the lacunar type and in a control group. Somatosensory evoked potentials (SEPs) to median nerve stimulation were also recorded. The central motor conduction times (CMCTs) and the threshold intensities for eliciting MEPs in the relaxed muscles were significantly increased on the affected side. Central motor conduction, for at least one muscle, was altered in 18 patients. MEP abnormalities were related to pyramidal signs (though they could be observed also in a patient without any motor impairment) and occurred independently of a specific clinical picture or a radiologically confirmed lacunar lesion. SEPs were less frequently altered than MEPs.     

Spatial dispersion of magnetic stimulation in peripheral nerves

To assess the longitudinal dispersion of the stimulus induced by the magnetic coil, collision experiments were performed in seven normal ulnar nerves. A supramaximal electrical stimulus S1 was delivered at the wrist, and followed by a supramaximal stimulus S2 in the upper arm, which was either electrical (electrical collision studies), or magnetic (magnetic collision studies). The interstimulus interval was varied by 0.2 msec increments from the time of complete cancellation of the S2 evoked motor response onwards, to include the entire span of recovery of that compound motor action potential. Collision curves were obtained for both magnetic and electrical stimuli by plotting the amplitude of the motor response elicited by S2 as a function of the interstimulus interval. In all seven normal ulnar nerves, comparison of the collision curves showed that the S2 evoked motor response is restored significantly more slowly when magnetic stimulation is used. This finding is best explained by longitudinal dispersion of the stimulus induced by the magnetic coil relative to conventional electrical stimulation, the large fibers being stimulated further away from the coil than the small ones. This interpretation is confirmed by the findings obtained with the same method in two cases of ulnar neuropathy, and by comparison of different intensities of magnetic stimulation.     

Epidurally recorded cervical spinal activity evoked by electrical and mechanical stimulation in pain patients

Spinal SEPs to electrical and mechanical stimulation of the upper limb of the non-painful side in 7 pain patients were recorded from the cervical epidural space. In response to electrical stimulation of the median nerve, the longitudinal distribution of the spinal postsynaptic negativity (N13) along the cord had a distinct level of maximal amplitude at the C5 vertebral body. When recorded at increasing distances cranial or caudal to this level, the latency of N13 was successively prolonged, in agreement with a spread-out near-field generator in the dorsal horn. Similar patterns of distribution and levels of maximal amplitude were demonstrated for the N13 wave evoked by electrical stimulation of the ulnar and thumb nerves as well as by mechanical stimulation of the thumb ball. The amplitude ratios of the N13 waves evoked by electrical stimulation of the median nerve and the thumb nerves, and by mechanical stimulation of the thumb ball were 3.9 to 1.4 to 1. The slow positive wave (P18), which has been assumed to represent recurrent presynaptic activity, had a somewhat different distribution, with a lower maximal amplitude and a less marked falling off in amplitude along the cord, as compared to the N13 component. The initial presynaptic positivity (P10) appeared with an almost constant amplitude along the cord. Tactile stimuli produced responses with considerably longer latency and duration than those obtained with electrical stimulation. There seemed to be a non-linear relationship between the amplitude of the response and the depth of skin indentation. The presented data contribute a more detailed picture of epidurally recorded spinal SEPs than previous studies. They will serve as a reference for further analysis of SEPs evoked by stimulation of the affected side in pain patients, to explore whether the painful state is associated with altered SEPs before or after therapeutic intervention.     

Decreased sensory cortical excitability after 1 Hz rTMS over the ipsilateral primary motor cortex.

OBJECTIVES: To study changes in the excitability of the sensory cortex by repetitive transcranial magnetic stimulation (rTMS) in humans. METHODS: Somatosensory evoked potentials (SEPs) and antidromic sensory nerve action potentials (SNAPs) were elicited by right median nerve stimulation at the wrist before and after low frequency (1 Hz) rTMS over the left motor cortex, lateral premotor cortex, sensory cortex, and also after sham stimulation. The intensity of rTMS was fixed at 1.1 times the active motor threshold at the hand area of motor cortex. RESULTS: N20 peak (N20p)-P25 and P25-N33 amplitudes were suppressed after rTMS over the motor cortex, whereas the N20 onset (N20o)-N20p and SNAP amplitudes were not affected. They recovered to the baseline about 100 min after the rTMS. rTMS over the premotor cortex or sensory cortex or sham stimulation had no suppressive effect on SEPs. CONCLUSIONS: The reduction of N20p-P25 and P25-N33 components without any changes of N20o-N20p amplitude suggests that the suppression occurs in the sensory cortex. rTMS (1 Hz) of the motor cortex induces a long-lasting suppression of the ipsilateral sensory cortex even at an intensity as low as 1.1 times the active motor threshold, probably via cortico-cortical pathways between motor and sensory cortex.     

Selective attention effects on somatosensory evoked potentials

Short and long latency somatosensory evoked potentials (SEPs) to median nerve stimulation were recorded over the contralateral hemisphere. Simultaneously, signals evoked by the same stimulus were monitored at Erb's point. Recordings were made during three conditions which were presented in a different random order to each of the subjects tested. During the control condition the subjects were instructed to attend to and count the number of electrical pulses delivered to the median nerve of their right hand. During the two task conditions, in addition to the pulses, the subjects received stimulation on the dorsal surface of one of their hands. This consisted in drawing circles lightly for the duration of SEP recording using a cotton swab (Q-tip). During the trial, the Q-tip was momentarily withdrawn 15 to 20 times and the subject's task was to ignore the pulses, attend to this cutaneous stimulation and count the number of times the cutaneous stimulation was interrupted. SEPs to the pulse were significantly greater in amplitude when cutaneous stimulation was delivered to the same hand as the pulse (the right hand) than when it was delivered to the left hand. This effect was confined to the long-latency SEPs and did not appear in either the Erb's point response or the short latency SEPs. These data indicate that selective attention to peripheral stimulation is a relatively late process mediated by cortical mechanisms and argue against the notion of early suppression of irrelevant stimulus channels in subcortical centers or in the periphery.(ABSTRACT TRUNCATED AT 250 WORDS)