Evoked potentials induced by transcranial stimulation in dogs
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1 Iowa State University From the SelectedWorks of Bonnie Hay-Kraus November, 1990 Evoked potentials induced by transcranial stimulation in dogs Karl H. Kraus, University of Missouri Dennis O'Brien, University of Missouri Eric R. Pope, University of Missouri Bonnie Hay Kraus, University of Missouri Available at: 7/
2 This material has been provided by the publisher for your convenience. It may not be further reproduced in any manner, including (but not limited to) reprinting, photocopying, electronic storage or transmission, or uploading onto the Internet. It may not be redistributed, amended, or overprinted. Reproduction of this material without permission of the publisher violates federal law and is punishable under Title 17 of the United States Code (Copyright Act) and various international treaties. Reprints or permission to reprint may be ordered by contacting Evoked potentials induced by transcranial stimulation in dogs Karl H. Kraus, DVM, MS; Dennis O'Brien, DVM, PhD; Eric R. Pope, DVM, MS; Bonnie Hay Kraus, DVM SUMMARY Evoked potentials were induced by transcranial stimulation and recovered from the spinal cord, and the radial and sciatic nerves in six dogs. Stimulation was accomplished with an anode placed on the skin over the area of the motor cortex. Evoked potentials were recovered from the thoracic and lumbar spinal cord by electrodes placed transcutaneously in the ligamentum flavum. Evoked potentials were recovered from the radial and sciatic nerves by surgical exposure and electrodes placed in the perineurium. Signals from 100 repetitive stimuli were averaged and analyzed. Waveforms were analyzed for amplitude and latency. velocities were estimated from wave latencies and distance traveled. The technique allowed recovery of evoked potentials that had similar characteristics among all dogs. velocities of potentials recovered from the radial and sciatic nerves suggested stimulation of motor pathways; however, the exact origin and pathway of these waves is unknown. Somatosensory-evoked potentials have been widely used to monitor spinal cord function in experimental and in clinical settings. 1 There are inherent shortcomings in this technique because the path of the somatosensory-evoked potential, which is initiated by peripheral nerve stimulation, has been shown in cats to travel to the dorsal columns and dorsal spinocerebellar tracts. These pathways carry proprioceptive and fine tactile information. 2 Information from this portion of the spinal cord may not be indicative of the function or condition of the rest of the spinal cord, specifically the motor tracts. The dorsal columns and motor tracts have different blood supplies. Also, the grey matter of the spinal cord is more susceptible to ischemic 3-5 and acute impact trauma 6 than the white matter of the spinal cord. For these reasons, monitoring of motor pathways has been investigated in animals and human beings Stimulation of motor pathways results in propagated impulses down motor pathways resulting in synaptic transmission at the ventral grey horn of the spinal cord and transmission through peripheral nerves. Recording of the motor-evoked potential from the spinal Received for publication Nov 13, From the Department of Veterinary Medicine and Surgery, College of Veterinary Medicine, University of Missouri, Columbia, MO Dr. Kraus' present address is Tufts University, School of Veterinary Medicine, 200 Westboro Road, North Grafton, MA cord will give an indication of the status of the m otor pathways. Recording from peripheral nerves may indicate the functional status of cell bodies in the spinal cord grey matter. Evoked potentials recovered from the spinal cord and peripheral nerves have been reported from transcranial stimulation of the brain in human beings 10 and cats, 9 and by direct cortical stimulation in dogs.11 The purpose of the study reported here was to use trans cranial electrical stimulation to induce evoked potentials, and recover them from the spinal cord and peripheral nerves. Materials and Methods Experiments were performed on 6 adult mixed-breed dogs (18 to 28 kg). All dogs received humane care in compliance with the "Guide for the Care and Use of Laboratory Animals" published by the National Institutes of Health. 12 The dogs were given atropine sulfate (0.05 mg/ kg) sc and anesthesia was induced wit h thiopental sodium (10.0 mg/kg) administered IV. The dogs were intubated and anesthesia was maintained with 1 % isoflurane and 100% oxygen, and a continuous IV drip of oxymorphone (0.8 µg/kg/min). The femoral artery was cannulized with a 16-gauge 3.5-inch catheter to monitor arterial blood pressure and to obtain samples for blood gas analysis. The dogs were mechanically ventilated and muscle paralysis was induced and maintained with succinylcholine chloride administered as an IV drip (30.0 µg/kg/min). Lactated Ringer solution was administered at a total dosage of 20 ml/kg/hr. Femoral artery blood pressure, ECG, end-expiratory C0 2 and rectal temperature were monitored continuously. Body temperature was maintained with a thermostatically contrblled water blanket. Serial blood gas analysis was performed and blood ph was maintained between 7.25 and Arterial Pac 02 was maintained between 25 and 35 mm of Hg. A 4-channel electrophysiologic diagnosis systema was used for stimulation and recording of the intraoperative spinal cord signal (Fig 1). Evoked responses were generated by transcranial stimulation of the dog with the anode placed over the area of the central sulcus and the cathode placed at the nuchal crest of the calvarium. The anode consisted of a series of twelve 1.6-mm stainless steel pinsb arranged in a "bed-of-nails" pattern, which covered a 3 x 2-cm surface. The cathode was a single stainless steel pin, which penetrated to a depth of 2 cm. One hundred repetitive stimuli, using a square-wave Nicolet Instrument Corp, Fremont, Calif. b Richards Medical Co, Memphis, Tenn. Am J Vet Res, Vol 51, No. 11, November 1990
3 'LI, SIGNAL. RECORDER I AVEAAGER l i1 i'\.. -- :, ( ' V""'"'JV : 1 ' \/ ' ii I "---' Figure 1-Diagram indicating the positions of the stimulating, recording, and reference electrodes used for recording transcranially induced evoked potentials in dogs. ~ }\ 'I, llj i1)t ---~r ~v-~- ~--~ J - 1 ' i ~J : ; I - L... Figure 3-Evoked potentials initiated by transcranial stimulation and recorded from the spinal cord at the area of the fo urth and fift h thoracic vertebrae in 6 dogs. ~ i~ \ './ ' I lu ft II! [j_j (\ _.I r... r \ j ' - :I : :: I ll.j L Figure 2-Evoked potentials initiated by transcranial stimulation and recorded from the spinal cord at the area of the first and second thoracic vertebrae in 6 dogs. Positive polarity is up in this and subsequent figures. stimulus of 400 seconds at 4.8 Hz, were used. Stimulus intensity was increased until an increase in intensity did not result in an increase in amplitude of recovered signals. Stimulus intensity ranged from 22 to 32 ma be- Am J Vet Res, Vol 51, No. 11, November 1990 tween dogs and was kept constant throughout the experiment. Impedance between the stimulating anode and cathode was < 5,000 D. The evoked potentials were recovered simultaneously in 4 channels. Potentials were recovered from the cranial thoracic and caudal lumbar portions of the spinal cord, and from the radial and sciatic nerves. Spinal cord recordings were accomplished with 55-mm monopolar electromyographic needlesc placed in the ligamentum flavum between the first and second thoracic and fourth and fifth lumbar vertebrae. Reference electrodes were placed in adjacent muscle. The radial nerve was exposed at the elbow and the sciatic nerve was exposed 3 cm proximal to the stifle. Nerve signals were recorded by use of pairs of platinum EEG needle electrodestl placed 1 to 2 cm apart in the perineurium lengthwise along the nerve. Bandpass filtering for the spinal cord signal was 100 to 1,500 Hz and for the peripheral nerves was 10 to 1,500 Hz. Impedance for all electrodes was between 1,000 and 5,000 D. The response to the 100 repetitive stimuli were recorded for 30-ms band widths and averaged. After proper stimulus intensity was determined, a series of 6 averages were obtained and stored on computer disk for future retrieval and analysis. Amplitudes and ' TECA Corp, Pleasantville, NY. d Grass instrument Co, Quincy, Mass. 1733
4 :: l. ii :1 \Ji\N"'~.c - ~- " : :11~~. ' ~ :rr I L r\ 11 I\. ' \ J'i I. I i I lo! /JI!' 1 iv\/ f r ~ ~v-- -~>14W"M--~j\ '!'..'\.'\, Figure 4-Evoked potentials initiated by transcranial stimulation and recorded from the radial nerve at the level of the elbow in 6 dogs. Table 1-Waveform analysis of transcranially induced evoked potentials recovered from the first and second thoracic vertebrae Peak latency velocity Amplitude (ms) (m/s) (µ.v) Pl 4.35(0.42) 80.99(9.09) 17.87(5.51) Nl 6.26(0.92) 57.33(11.44) 6.23(3.76) P2 7.22(0.88) 49.16(7.56) 8.25(2.74) N (1.04) 32.28(4.34) 2.49(1.41) Data are expressed as mean(± SD). P =positive peak; N =negative peak. Table 2-Waveform analysis of transcranially induced evoked potentials recovered from the fourth and fifth lumbar vertebrae Pl Nl Peak latency (ms) 5.28(0.57) 6.70(0.75) velocity (m/s) (11.35) 93.31(6.49) Amplitude ( µ.v) 7.02(5.38) 3.50(3.04) latencies were determined directly from stored data and averaged between all 6 dogs. Standard deviations were calculated from these figures. The distances from the anode of the stimulation electrodes to the respective recording electrodes were measured along the estimated course of the spinal cord and nerves. These measurements served to calculate approximate conduction velocities ' Figure 5-Evoked potentials initiated by transcran ial stimulation and recorded from the sciatic nerve at the level of the stifl e in 6 dogs. Results Table 3-Waveform analysis of transcranially induced evoked potentials recovered from the radial nerve at the level of the elbow Latency (ms) velocity (m/s) P l (1.29) (4.34) Nl 6.40 (1.33) (2.67) P (1.27) (3.53) N (1.30) (3.40) P (1.38) (3.36) N (1.42) (3.48) P (1.47) (3.06) N (1.46) (3.34) Amplitude (µv) 3.34 (1.31) 2.22 (0.72) 1.22 (0.88) 1.67 (0.66) 0.99 (0.49) 1.33 (1.15) 0.96 (1. 04 ) 1.40 (1.25) The anesthetic regimen allowed consistent recovery of the evoked responses, including the peripheral nerve signals, in all dogs. In all channels, all 6 series of averages were shown to be consistent by superimposition of the recovered waveforms (Fig 2 to 5). The waveforms recovered from between the first and second thoracic vertebrae consisted of a large positive spike followed by a plateau or negative peak, then a second positive peak and a negative peak (Table 1). The waveforms recovered from between the fourth and fifth lumbar vertebrae generally consisted of a single pos- Am J Vet Res, Vol 51, No. 11, November 1990
5 Table 4-Waveform analysis of transcranially induced evoked potentials recovered from the sciatic nerve at the level of the stifle Peak latency velocity Amplitude (ms) (m/s) (µ.v) Pl (2.06) (7.95) 0.40 (0.18) Nl (2.06) (7.45) 0.34 (0.14) P (2.10) (7.18) 0.38 (0.20) N (2.11) (6.91) 0.65 (0.40) P (2.21) (6.72) 0.75 (0.33) N (2.18) (6.28) 0.53 (0.37) P (2.24) (6.01) 0.58 (0.42) N (2.24) (5. 70 ) 0.47 (0.29) P (2.30) (5.58) 0.24 (0.20) N (2.32) (5.39) 0.38 (0.25) itive and negative peaks. In 1 dog, the positive peak contained an additional deflection, and in 1 dog, the negative peak contained an additional deflection. The first positive peak and the first negative peak were analyzed (Table 2). The waveforms recovered from the radial nerve consisted of a strong positive wave followed by at least 3 positive waves. In 1 dog, a strong positive wave was also preceded by a weak biphasic wave. The first strong positive wave and 3 subsequent waves were analyzed (Table 3). The waveforms recovered from the sciatic nerve consisted of a series of several low-amplitude waves. One strong positive wave could be identified in all dogs. This wave, 2 preceding, and 2 following were analyzed (Table 4). Waves were numbered consecutively from the shortest to the longest latency. Discussion Transcranially stimulated-evoked potentials have been reported in human beings 10 and cats. 9 Some investigators 9 have suggested that transcranial stimulation of the cortex results in the production of waveforms that originate in the motor cortex and travel down corticospinal pathways and in the corticospinal tract in the spinal cord. Recent evidence 13 obtained from experiments in the rat has alternatively suggested that the waveforms generated from transcortical electrical stimulation arise from pathways outside the motor cortex, probably other descending motor pathways in the brain stem. Other descending motor pathways include the rubrospinal pathway originating from the rostral mesencephalon, and the medullary reticulospinal, pontine reticulospinal, and vestibulospinal pathways originating from the pontomedullary junction of the brain stem. It was our intention to stimulate motor fibers. The question of whether we stimulated motor fibers or antidromally stimulated sensory fibers remains unclear. The anode of the stimulator was placed over the motor cortex, but the cathode was positioned behind the skull. It is possible that the brain stem and even cranial cervical portions of the spinal cord were stimulated. Potentials could be carried antidromally down the spinal cord and peripheral nerves in the dorsal columns. The fibers of the dorsal columns are heavily myelinated and have conduction velocities of 100 to 120 m/s in dogs. The first peak latencies of the evoked potentials recorded over the spinal cord suggested a similar conduction time. Motor fibers of the spinal cord conduct at 9 to 63 m/s in the human being and cat, and, to our knowledge, have not been determined in the dog. An impulse carried to a peripheral nerve would make 1 or 2 synapses with delays of 0.5 ms each. Estimated conduction velocities of the evoked potential recovered from the radial and sciatic nerves suggest that the major peaks and those occurring thereafter are slow enough to be consistent with conduction through motor pathways. Slower sensory pathways, specifically the spinocerebellar and spinothalamic tracts, could not be conducted antidromally to peripheral nerves because they would have to conduct backward throu gh synapses in the spinal cord to do so. The technique of transcranially induced evoked potentials should be useful in evaluating the effects of ischemia and trauma to the spinal cord in the dog, and in intraoperative monitoring of clinical cases. Further studies are needed to determine the exact origin and pathways t hese potentials follow. References 1. Hollier LH. Protecting the brain and spinal cord. J Vase Surg 1987;5: Cohen AR, Young W, Ransohoff J. Intraspinal localization of the somatosensory evoked potential. Neurosurgery 1981;9: Tureen LL. Effect of experimental temporary vascular occlusion on the spinal cord: Correlation between structural and functional changes. Arch Neurol Psychiat 1936;35: Coles JG, Wilson GJ, Sima AF, et al. Intraoperative detection of spinal cord ischemia using somatosensory cortical evoked potentials during thoracic aortic occlusion. Ann Thorac Surg 1982;34: Coles JC, Ahmed NS, Mehta HU, et al. Role of free radical scavenger in protection of spinal cord during ischemia. Ann Thorac Surg 1986;41: Osterholm JL. The pathophysiology of spinal cord trauma. Springfield, Ill: Charles C Thomas Co, Publisher, Levy WJ. Spinal evoked potentials from the motor tract s. J Neurosurg 1983;58: Levy WJ, York DH. Evoked potentials from the motor tracts in humans. Neurosurgery 1983;12: Levy WJ, McCaffrey M, York DH, et al. Motor evoked potentials from transcranial stimulation of the motor cortex in cats. Neurosurgery 1984;15: Levy WJ, York DH, McCaffrey M, et al. Motor evoked potentials from transcranial stimulation of the motor cortex in humans. Neurosurgery 1984;15: Konrad PE, Tacker WA, Levy WJ, et al. Motor evoked potentials in the dog: effects of global ischemia on spinal cord and peripheral nerve signals. Neurosurgery 1987;20: Guide for the care and use of laboratory animals. National Institutes of Health, publication No , revised Zappulla RA, Hollis P, Ryder MA, et al. Noncortical origins of the spinal motor evoked potential in rats. Neurosurgery 1988;22: Mills KR, Murray NMF. Corticospinal tract conduction time in multiple sclerosis. Ann Neural 1985;18: Armstrong DM, Drew T. Discharges of pyramidal tract and other motor cortical neurones during locomotion in the cat. J Physiol 1984;346: Am J Yet Res, Vol 51, No. 11, November
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