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Neurophysiological Evidence of Spared Upper Motor Neurons After Spinal Cord Injury

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Neurophysiological Evidence of Spared Upper Motor Neurons After Spinal Cord Injury Paraplegia (1996) 34, 39-45 © 1996 International Medical Society of Paraplegia All rights reserved 0031-1758/96 $12.00 Neurophysiological evidence of spared upper motor neurons after spinal cord injury l 3 2 1 1 SS Haghighi , DH York , L Spollen , JJ Oro and MA Perez-Espejo 1 Division of Neurosurgery and 2 Department of Pathology, University of Missouri-Columbia, and 3 Department of Neurosciences at St. fohn's Mercy Hospital, Columbia, Missouri, USA Fourteen cats were subjected to a moderate (100 gm-cm; n = 7) or a severe (600 gm-cm; n = 7) spinal cord injury at the C4-C5 level using a weight drop technique. Somatosensory evoked potentials (SSEPs) were recorded after stimulation of the median nerve in the forearm. The SSEPs were measured in each animal before and after the injury. Motor evoked potentials (MEPs) were recorded from forearm extensor muscles after transcranial magnetic stimulation of the motor cortex. The SSEPs and The MEPs were measured in each animal before and after the injury under ketamine-based anesthesia. After the moderate injury (n = 7), 83% of the animals (6/7) maintained the SSEPs and 100% (7/7) maintained the MEPs. Postoperatively, only one animal who lost the SSEPs post-injury became tctraplegic. The remainder were neurologically intact. In the severely injured animals (n = 7), 5/7 of animals lost SSEPs and subsequently became tetraplegic. The MEPS were maintained in 3/5 (60%) of these tetraplegic animals. Two of seven animals (40%) in this group did not lose SSEPs or MEPs and recovered with no clinical deficit. Our data show a good correlation between the presence of SSEPs and functional recovery in the injured groups. The presence of MEPs in 3/5 (60%) of the tetraplegic animals may imply the existence of functionally active motor fibers after severe spinal trauma. Keywords: muscle action potential; spinal cord injury; transcranial magnetic stimulation Introduction The application of somatosensory evoked potentials evoked potentials (MEPs) can be obtained by (SSEPs) for both clinical and experimental use has stimulating neuronal tissue in motor cortex, spinal been an important factor in assessing spinal cord injury roots and peripheral nerves. Responses can be (SCI) for the last two decades.1 -3 SSEPs are based on recorded with electromyographic or evoked potential the principle that when a sensory nerve in the equipment.4,11,12,25,26 The combination of MEPs with periphery is stimulated, evoked electrical activity can SSEPs studies would provide a comprehensive be recorded from the somatosensory cortex4. The technique for the noninvasive investigation of spinal SSEPs have been shown to be useful for evaluating cord function.17,19,22 Prolonged latencies of the MEPs, spinal cord conduction with high degree of correlation attributable to slowed central conduction and reduced between potential neurological recovery following SCI response amplitude, are typically present in central and evoked activities.4-6 However, a few reported demyelinating disease,15 motor neuron disease,27 spinal cases have noted the failure of SSEP monitoring to cord compression,22,23 and after SCI.17,22-24 alert the surgeon to impending damage to the spinal MEP findings usually correspond to the clinical motor pathways.7,8 status of patients, inasmuch as MEPs cannot be The technique of transcranial electrical and evoked in patients with clinically complete paraly­ magnetic stimulation of the motor cortex has sis.17,24 In patients with incomplete spinal cord injury, provided a unique opportunity to study the corticosp­ MEPs show prolongation of latency and reduction in inal connections in human subjects.9-13 Cortical the response amplitude.15,19,21,23,24 However, several stimulation has been widely employed for clinical clinical studies have demonstrated EMG responses, research studies.14-19 These methods provide valuable distal to the injurls site, in patients with clinically information on the state of the motor tracts in several complete paralysis. 8-31 These responses were obtain­ neurological disorders.2o-24 A further potential appli­ able when neurological reinforcement was em­ cation is the study of SCI. Magnetically induced motor ployed.18,28 These findings indicate the existence of structurally functional motor pathways that have been spared injury. The existence of spared axons after SCI with Correspondence: SS Haghighi clinically complete paralysis is documented through Spared upper motor neurons in spinal cord after injury -- SS Haghighi et a/ 40 extensive neuropathological evidence. It has been base was 20 to 30 msec and cutoff filters were set at shown that in most post mortem specimens the 3000 and 10 Hz for muscle recording and 500 to 10 Hz necrosis was most severe in the central gray area and for the SSEPs. The ground lead was attached to a 2 posterior white column.3 •33 Accordingly, some mid-thoracic spinous process between the stimulating authors categorize lesions as 'discomplete' where and the recording electrodes. clinically the patients exhibit complete paralysis, but The left forearm was stimulated using transdermally neurophysiologically they possess residual suprasfinal placed needle electrodes in the footpad. Repetitive influence over motoneurons distal to the injury? (2.81 Hz) rectangular pulses of 0.2 msec duration, 2 -5 We investigated the immediate neurophysiological, volts intensity, and no delay (Models S88, and SIU neuropathological, and functional outcome occurring 8T, stimulator and isolation unit, Grass Instrument, after SCI utilizing the weight drop method in cats. We Quincy, Massachusetts) were used to generate the correlated the presence or absence of MEPs and cortical responses. On average, 250 responses were SSEPs with neurological outcome and histopathologi­ recorded and averaged and displayed on the monitor. cal findings. In addition, the excitability of the spared To record the muscle action potential from forearm upper motoneurons after severely injuring the spinal extensor muscle, single shock magnetic stimulation cord was documented using magnetic stimulation. (MES-I0, Cadwell laboratories, Kennewick, Washing­ ton) was used. Magnetic stimulation was delivered Materials and methods through an eight-shaped coil, each loop 5 cm in diameter. The coil was placed tangentially to the A total of 14 cats weighing from 3 to 5 kg were used scalp on the right side with the handle pointing for the experiment. Animals were premedicated with posteriorly. The magnetic stimulator was operated at atropine (0.04 mgjkg) and anesthetized with an 100% of the stimulator's output. At this stimulus intramuscular injection of Ketalar plus Acepromazine intensity, the shortest latency responses were achieved. maleate (35 mgjkg). Additional doses of the anesthetic The C-5 root latency was obtained after bipolar were given if needed. After tracheostomy and electrical stimulation of the ventral root at 1 Hz. intubation, animals were ventilated in room air Intensity was adjusted until evoked muscle response (Model 665, Animal ventilator, Harvard Apparatus, reached the shortest onset latency with maximal peak South Natick, Massachusetts). The volume and rate of amplitude. Central motor conduction time (CMCT) the ventilator was adjusted to obtain an end-tidal CO2 was calculated by subtracting the C-5 latency from the of 3.5 to 4% using a digital CO2 monitor (Datex, cortical motor latency. Instrumentarium, Oy, Finland). A polyethylene cathe­ A weight drop model of spinal cord injury was ter was inserted in the right femoral vein for infusion utilized. The trauma device consisted of a perforated of fluids. The right femoral artery was exposed and aluminium tube containing a cylindrical stainless steel cannulated for arterial blood pressure monitoring. weight of 20 g and a lightweight acrylic platform with Body temperature was monitored with a rectal a circular impact surface 0.5 cm in diameter. It was thermometer and maintained at the range 36.5- mounted on a micromanipulator, and the acrylic 38SC using a heating blanket (Model RK-200, impactor was centered on the dorsal midline at the Aquamatic K thermia, Bellville, Ohio) and a heating C-5 level. The SSEPs and muscle action potentials lamp, as needed. Continuous readings of the arterial were recorded before the injury and after injury every blood pressure and the electrocardiogram were hour up to four hours post-injury. The neurological recorded (Tektronix, Beaverton, Oregon). outcome was assessed immediately after the 4th hour Animals were transferred to a Kopf stereotactic post-injury when animals were fully recovered from spinal unit (David Kopf Instruments, Tujunga, anesthesia. Tetraplegia was confirmed by demonstrat­ California). The vertebral column was immobilized ing muscle flaccidity distal to the injury level and lack by using a clamp attached to the T -4 spinous process of any movements in all four extremities. The animals and pelvic pins which were attached firmly to the iliac were placed into two groups. The first group (n = 7) crest bilaterally. A three-level laminectomy was was subjected to a severe injury (600 gm-cm). The performed at C4-C6 levels. The dura mater was left second group (n = 7) was moderately traumatized intact. (100 gm-cm). Somatosensory evoked potentials (SSEPs) were Euthanasia was performed with an intravenous recorded using standard EEG needle electrodes placed overdose of sodium pentobarbital (35 mgjkg; LV.) transdermally over the vertex (active electrode) and the after 5 h post-injury. In each animal, the spinal cord upper nasal region (reference electrode). To record the was transacted above and below the traumatized area forearm extensor muscle action potential, two needle and fixed in 10% buffered formalin. The spinal electrodes were inserted into the muscle on the left segments inclusive of the lesion were removed side. Impedance of the recording electrode was kept (approximately 1 cm length) and kept in formalin below 5 KOhms. An evoked potential system (Model until tissue preparation. Histological evaluation was 8400, Cadwell Laboratories, Kennewick, Washington) performed on two moderately injured and two severely was utilized for generation of stimulus and amplifica­ injured animals.
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