Effect of spinal cord ischemia on compound muscle action potentials and spinal evoked potentials following spinal cord stimulation in the dog

We recorded the compound muscle action potentials (CMAP) from the soleus muscle and spinal evoked potentials (SpEP) from the caudal spinal cord after stimulation of the rostral spinal cord via epidural electrodes in 18 dogs. We examined the changes of CMAP and SpEP after the cord was made ischemic by clamping the aorta at different levels. Clamping the abdominal aorta below the artery of Adamkiewicz (five dogs) did not change either CMAP or SpEP significantly. When the thoracic aorta was clamped above the radicular and Adamkiewicz arteries (10 dogs), CMAP disappeared entirely within 5-10 min of occlusion, but SpEP showed only minimal latency prolongation limited to the late peaks in seven of 10 dogs. In the remaining three dogs, both CMAP and SpEP disappeared within 30 min of occlusion but with the more rapid deterioration of CMAP than of SpEP. Progressive ligation of lumbar arteries (three dogs) from caudal to rostral levels did not change CMAP until ligation of Adamkiewicz artery. Then CMAP disappeared, but SpEP remained unchanged. These findings suggest that CMAP and SpEP are mediated through different pathways and that CMAP reflect anterior cord function. The described electrophysiologic technique would be useful to monitor spinal cord motor function during surgery of the spine, spinal cord, or thoracoabdominal aorta.     

An experimental study on conductive spinal cord action potentials evoked by direct stimulation of the spinal cord--pathway and source of conductive action potentials in the spinal cord

The following experiments were carried out in adult cats to clarify the pathway and origin of the conductive spinal cord action potential evoked by dorsal epidural stimulation. (1) Comparison with the potential by surface stimulation of the spinal cord: Since waveforms, conduction velocity, and the relationships between the stimulation site and the change in threshold level were equal to those of surface stimulation, epidural stimulation and direct surface stimulation apparently induced the potential deriving from the same origin. (2) Recording of single fiber action potential: The mean conduction velocity of the dorsal column fiber was approximately 50 m/sec and that of the dorsolateral funiculus fiber was about 80 m/sec. 15-20% of potential N1 and 80-85% of potentials N2 and N3 were composed by the dorsal column fibers, whereas 80-85% of N1 and 15-20% of N2 and N3 were composed by the dorsolateral funiculus fibers.     

The effect of anesthetic agents on descending spinal cord evoked potential and the compound muscle action potentials elicited by stimulation at the cerebral motor cortex and the spinal cord]

Recently, intraoperative monitoring of the motor tract by descending spinal cord motor evoked potentials (MEP) and compound muscle action potentials (CMAP) has been applied in clinical testing. Since several reports have mentioned the vulnerability of these potentials to anesthetic agents, experimental studies were carried out on the relationship between these potentials and anesthesia using 41 adult cats. The effects of anesthesia on changes in amplitude of the direct wave (D wave) and indirect wave (I wave) of the MEP and CMAPs were investigated. These potentials were generated by stimulation of the spinal cord and the motor cortex, respectively. Enflurane (2%), halothane (1%) and isoflurane (1.5%) with pure oxygen decreased the amplitude of the I wave to less than 50% of the control level. The CMAP after stimulation of the spinal cord was degraded to less than 30%, and the CMAP after cortical stimulation vanished completely. Only the D wave was stable against inhalational anesthetic agents. Sixty-seven percent nitrous oxide with the above concentrations of these inhalational anesthetic agents decreased the amplitude of the I wave to less than 30% and the CMAP evoked by spinal cord stimulation vanished. The effect of modified NLA (diazepam and pentazocine) on these potentials was weaker than that of the inhalational anesthetic agents.     

Monitoring of motor action potentials after stimulation of the spinal cord

We recorded motor action potentials in cats, using surface electrodes placed over the soleus muscle. The action potentials were generated by stimulating the spinal cord with electrodes in the epidural space at the level of the fifth or sixth thoracic vertebra. This also was done in humans, using the same methods of stimulating and recording, but the intensity of the stimulus was adjusted to produce little or no twitch of the paraspinal muscles. In the animal experiment, the motor action potential was abolished after transection of the pyramidal tract and was progressively attenuated with effective doses of a curare-like agent. We also tested the effect of distraction, using the same technique as is used in Harrington instrumentation, and found that the amount of distraction that caused reduction of the amplitude of the motor action potential of more than 50 per cent, when sustained for longer than seven minutes, caused permanent paraplegia in two cats. The evaluation of spinal evoked potentials that were obtained from epidural electrodes placed caudad to the level of distraction, and of motor action potentials that were recorded over the soleus muscle, following the same stimulus, showed a similar pattern of reduction after distraction in five of seven cats. The other two cats had irreversible reduction of motor action potential associated with unchanged spinal evoked potential, and both cats became paraplegic.(ABSTRACT TRUNCATED AT 250 WORDS)     

Change of muscle motor-evoked potentials after motor cortex stimulation caused by acute spinal cord injury in cats

The validity of the evoked compound muscle action potential (ECMAP) as an index of spinal cord injury has not been established in neurophysiologic monitoring of motor function, although evoked spinal cord potential (ESCP) has been. In the current study, nine cats were used. After craniotomy, electric stimuli were applied to the motor area. Four cats were given stimulation of various numbers and frequencies, and the other five cats underwent graded compression of the spinal cord, and then ECMAPs and ESCPs were recorded. Three cats were awakened and their motor functions were assessed 3 weeks later. The amplitude of the ESCP never decreased to 60% or less of the control value, even when ECMAPs disappeared. No motor dysfunction was present 3 weeks after the experiment. ECMAP is clinically useful, providing information on impairments of the spinal cord that otherwise would remain undetected.     

Dissociation of muscle action potentials and spinal somatosensory evoked potentials after ischemic damage of spinal cord

In patients undergoing spinal fusion and Cotrel-Dubousset instrumentation we recorded compound muscle action potentials (CMAP) from the lower limb and spinal somatosensory evoked potentials (SSEP) from the caudal epidural space after direct stimulation of rostral spinal cord via epidural electrodes. In three of 30 patients tested, the derotation maneuver altered CMAP but not SSEP. In ten dogs, we observed similar dissociation with decrease or disappearance of CMAP amplitude and unchanged SSEP after ligation of the thoracoabdominal aorta or intercostal arteries at each level. In contrast, both CMAP and SSEP were unchanged by clamping the artery at the lumbar level. This is likely due to the lack of collateral vascular flow at the thoracic cord level, the anterior cord in particular, which is mainly supplied by a single large radicular artery (Adamkiewicz artery). These findings support that the CMAP and SSEP are mediated through two independent pathways located in the anterior and posterior spinal cord, respectively. We postulate that the dissociate alteration of CMAP and SSEP by derotation maneuver is due to greater vulnerability of the anterior cord or motor tract to ischemia caused by the displacement of anterior spinal or radiculomedullary artery. Therefore, the patients requiring major derotation procedure would benefit from CMAP monitoring, which provides more sensitive measure of anterior cord function that the conventional SSEP monitoring.     

Subdural air limits the elicitation of compound muscle action potentials by high-frequency transcranial electrical stimulation

High-frequency transcranial electrical stimulation was performed in 8 patients undergoing surgery in the sitting position. Following the opening of the dura of the posterior fossa changes in compound muscle action potentials were observed. These changes were not attributable to surgical manoeuvres at the brain stem or spinal cord, or to anaesthetic changes. In all these cases intraoperative fluoroscopy of the skull revealed a subdural air collection underneath the stimulation electrodes. Such a subdural air collection, not infrequent in patients operated on in the sitting position, limits the application of high-frequency transcranial electrical stimulation as a monitoring technique. It remains unclear if this effect is due to the increasing distance between scalp and cortex and the insulating effect of subdural air, or due to displacement of the motor cortex. The practical importance of this report is derived from the increasing application of intraoperative motor pathway monitoring.     

Spinal cord evoked injury potentials in patients with acute spinal cord injury

Six patients were examined in the acute stage of spinal cord injury, between 11 h and 12 days posttrauma. Quadripolar epidural electrodes were positioned either percutaneously using a Tuohy needle or directly into the epidural space during surgical intervention. These electrodes were combined with a common reference to obtain monopolar recordings of spinal cord evoked potentials resulting from either median nerve stimulation at the wrist or tibial nerve stimulation at the popliteal fossa. Spinal cord evoked injury potentials (SCEIPs), stationary potentials with positive polarity on the distal aspect of the lesion and negative polarity on the proximal aspect, were recorded in all cases. The average amplitude (n = 3) of the SCEIP resulting from tibial nerve stimulation as measured across the lesion was 13.5 microV with an average duration of 12.7 msec. For median nerve stimulation, the average amplitude (n = 3) of the SCEIP was 16.3 microV with an average duration of 6.7 msec. There was a change in polarity in all cases over a distance of less than 6 mm, the distance between the electrode contacts on the epidural electrode. In one case, recordings were performed initially at 11 h and repeated at 21 days posttrauma. In the latter recording, the SCEIP was still present but was five times smaller in amplitude. Coincidentally, the patient also showed clinical signs of improvement in sensory and motor spinal cord function. This study demonstrates the feasibility of recording the SCEIP in patients with acute spinal cord injury, describes the features of these SCEIPs, discusses their origins, and explores the utility of recording the SCEIP as an aid in determining the severity of the injury as well as a means of monitoring changes in spinal cord function.     

Modification of spasticity by transcutaneous spinal cord stimulation in individuals with incomplete spinal cord injury

Context/objective

To examine the effects of transcutaneous spinal cord stimulation (tSCS) on lower-limb spasticity.

Design

Interventional pilot study to produce preliminary data.

Setting

Department of Physical Medicine and Rehabilitation, Wilhelminenspital, Vienna, Austria.

Participants

Three subjects with chronic motor-incomplete spinal cord injury (SCI) who could walk ≥10 m.

Interventions

Two interconnected stimulating skin electrodes (Ø 5 cm) were placed paraspinally at the T11/T12 vertebral levels, and two rectangular electrodes (8 × 13 cm) on the abdomen for the reference. Biphasic 2 ms-width pulses were delivered at 50 Hz for 30 minutes at intensities producing paraesthesias but no motor responses in the lower limbs.

Outcome measures

The Wartenberg pendulum test and neurological recordings of surface-electromyography (EMG) were used to assess effects on exaggerated reflex excitability. Non-functional co-activation during volitional movement was evaluated. The timed 10-m walk test provided measures of clinical function.

Results

The index of spasticity derived from the pendulum test changed from 0.8 ± 0.4 pre- to 0.9 ± 0.3 post-stimulation, with an improvement in the subject with the lowest pre-stimulation index. Exaggerated reflex responsiveness was decreased after tSCS across all subjects, with the most profound effect on passive lower-limb movement (pre- to post-tSCS EMG ratio: 0.2 ± 0.1), as was non-functional co-activation during voluntary movement. Gait speed values increased in two subjects by 39%.

Conclusion

These preliminary results suggest that tSCS, similar to epidurally delivered stimulation, may be used for spasticity control, without negatively impacting residual motor control in incomplete SCI. Further study in a larger population is warranted.     

Quadriceps muscle deoxygenation during functional electrical stimulation in adults with spinal cord injury

STUDY DESIGN: Cross-sectional study comparing healthy subjects with age and gender matched subjects with spinal cord injury (SCI, injury levels from C5 to T12). OBJECTIVES: To compare the acute cardiorespiratory responses and muscle oxygenation trends during functional electrical stimulation (FES) cycle exercise and recovery in the SCI and healthy subjects exercising on a mechanical cycle ergometer. SETTING: Seven volunteers in each group participated in one exercise test at the Rick Hansen Center, University of Alberta, Edmonton, Canada. METHODS: Both groups completed a stagewise incremental test to voluntary fatigue followed by 2 min each of active and passive recovery. Cardiorespiratory responses were continuously monitored using an automated metabolic cart and a wireless heart rate monitor. Tissue absorbency, an index of muscle oxygenation, was monitored non-invasively from the vastus lateralis using near infrared spectroscopy. RESULTS: The healthy subjects showed significant (P<0.05) increases in the oxygen uptake (VO2), heart rate (HR) and ventilation rate (VE) from rest to maximal exercise. The SCI subjects showed a twofold increase in VO2 (P>0.05), a threefold increase in VE (P<0.05) and a 5 beats/min increase in HR (P>0.05) from the resting value. The SCI subjects demonstrated a lesser degree (P<0.05) of muscle deoxygenation than the healthy subjects during the transition from rest to exercise. Regression analysis indicated that the rate of decline in muscle deoxygenation with respect to the VO2 was significantly (P<0.05) faster in the SCI subjects compared to healthy subjects. CONCLUSIONS: FES exercise in SCI subjects elicits: (a) modest increases in the cardiorespiratory responses when compared to resting levels; (b) lower degree of muscle deoxygenation during maximal exercise, and (c) faster changes in muscle deoxygenation with respect to the VO2 during exercise when compared to healthy subjects.     

Studies on motor action potentials following transcranial stimulation and somatosensory evoked potentials including absolute refractory time in experimental spinal cord injury

The motor action potential (MAP) following transcranial stimulation and absolute refractory time (ART) in somatosensory evoked potential (SSEP) were investigated after experimental spinal cord injuries in rabbits. The thoracic cords were injured at the level of the 11th vertebrae by Allen's method. The paralysis after the trauma was classified into 4 groups depend on its severity; severe, mild, transient and non palsy group. A single transcranial stimulation evoked the double MAPs (MAP1 and MAP2) which were characteristic for the palsy groups. The amplitude of the MAP1 was greater than MAP2 in the transient palsy group, while that of the MAP1 was lower than MAP2 in both severe and mild palsy groups. The amplitude of the MAP was significantly reduced in all injured animals. There was no correlation between the amplitude or latency of the SSEP and the severity of the palsy. However, the ART of the SSEP was considerably prolonged in all injured animals regardless of the severity of the palsy.     

Comparison of spinal cord evoked potentials and peripheral nerve evoked potentials by electric stimulation of the spinal cord under acute spinal cord compression in cats

STUDY DESIGN: Spinal cord evoked potentials and peripheral nerve evoked potentials after spinal cord stimulation were recorded under acute spinal cord compression in 19 cats. OBJECTIVES: To investigate the effects of acute compression upon grey matter and white matter by comparing both potentials. METHODS: We compared peripheral nerve evoked potentials, recorded at the biceps brachii branch of the musculocutaneous nerve, with descending spinal cord evoked potentials, recorded from the lumbar spinal cord, by stimulation to the C2 level, under compression of the C6 segment. RESULTS: The amplitude of both potentials decreased with increased compression. The second wave of peripheral nerve evoked potentials, which are motor fibre action potentials, decreased sooner than those of the spinal cord evoked potentials. CONCLUSION: These findings indicate that peripheral nerve evoked potentials are sensitive to acute damage of the segmented compression. This suggests that grey matter is more vulnerable to compression than white matter.     

Surface electrical stimulation of skeletal muscle after spinal cord injury.

STUDY DESIGN: Survey. OBJECTIVE: Examine muscle contractile activity during electrical stimulation (ES) after spinal cord injury (SCI). SETTING: General community of Athens, Georgia, USA. METHODS: Eight clinically complete SCI adults (C6 to T12) 4+/-1 (mean+/-SE) years post injury and eight able-bodied adults were studied. Surface ES was applied to the left m. quadriceps femoris for three sets of 10, 1 s isometric actions (50 Hz trains, 400 micros biphasic pulses, 50 micros phase delay, 1 s: 1 s duty cycle) with 90 s of rest between sets. Current was set to evoke isometric torque that was (1) sufficient to elicit knee extension with 2.3 kg attached to the ankle (low level ES), and (2) intended to equal 30% (mid level ES) or 60% of maximal voluntary torque of able-bodied adults (high level ES, able-bodied only). The absolute and relative cross-sectional area (CSA) of m. quadriceps femoris that was stimulated as reflected by contrast shift in magnetic resonance images and torque were measured. RESULTS: Six+/-2, 20+/-2 and 38+/-4% of the average CSA of m. quadriceps was stimulated during low, mid and high level ES, respectively, for able-bodied. Corresponding values for SCI for low and mid level ES were greater (61+/-12 and 92+/-7%, P = 0.0002). Torque was related to the CSA (cm2) of stimulated muscle (Nm = 3.53 x stimulated CSA+13, r2 = 0.68, P = 0.0010), thus ES of a greater per cent of m. quadriceps femoris in SCI was attributed to their smaller muscle (24+/-3 vs 73+/-5 cm2, P = 0.0001). The decline in torque ranged from 9+/-l to 15+/-4% within and over sets for low, mid or high level ES in able-bodied. SCI showed greater (P = 0.0001) fatigue (19+/-3 to 47+/-6%). CONCLUSION: The territory of muscle activation by surface electrical stimulation varies among SCI patients. Given sufficient current, a large portion of the muscle of interest can be stimulated. The resulting torque is modest, however, compared to that attainable in able-bodied individuals due to the small size and limited fatigue resistance of skeletal muscle years after spinal cord injury.     

Neuroprotective effect of epidural electrical stimulation against ischemic spinal cord injury in rats: electrical preconditioning

BACKGROUND: Electroconvulsion therapy is likely to serve as an effective preconditioning stimulus for inducing tolerance to ischemic brain injury. The current study examines whether electrical stimuli on the spinal cord is also capable of inducing tolerance to ischemic spinal cord injury by transient aortic occlusion. METHODS: Spinal cord ischemia was induced by occlusion of the descending thoracic aorta in combination with maintaining systemic hypotension (40 mmHg) during the procedure. Animals implanted with epidural electrodes were divided into four groups according to electrical stimulation and sham. Two groups consisted of rapid preconditioning (RE group, n = 8) and sham procedure (RC group, n = 8) 30 min before 9 min of spinal cord ischemia. In the two groups that underwent delayed preconditioning, rats were exposed to 9 min of aortic occlusion 24 h after either pretreatment with epidural electrical stimulation (DE group, n = 8) or sham (DC group, n = 8). In addition, rats were exposed to 6-11 min of spinal cord ischemia at 30 min or 24 h after epidural electrical stimulation or sham stimulation. The group P50 represents the duration of spinal cord ischemia associated with 50% probability of resultant paraplegia. RESULTS: Pretreatment with electrical stimulation in the DE group but not the RE group protected the spinal cord against ischemia, and this stimulation prolonged the P50 by approximately 15.0% in the DE group compared with the DC group. CONCLUSIONS: Although the optimal setting for this electrical preconditioning should be determined in future studies, the results suggest that epidural electrical stimulation will be a useful approach to provide spinal protection against ischemia.