Electrospinogram and spinal and cortical evoked potentials in experimental spinal cord trauma GLENN MORRISON, M.D., RONALD J. LORIC, PH.D., JERALD S. BRODKEV, M.D., ANDFRANK E. NULSEN, M.D. Division of Neurosurgery, Department of Surgery, Case Western Reserve University School of Medicine, University Hospitals of Cleveland, Cleveland, Ohio
~" Studies in 28 traumatized cats showed the following acute changes after spinal cord compression in the cord segment below the trauma: 1) increase in size of the spinal cord evoked potential; 2) increase in size of the electrospinogram; and 3) increase in frequency of the electrospinogram. KEvWoRDs 9 spinal cord 9 evoked potential 9 cortex 9 electrospinography 9 spinal cord c o m p r e s s i o n
LECTRICAL assessment of the functional integrity of the spinal cord is especially pertinent when the usual clinical methods are unavailable, for instance, intraoperatively and in the unconscious patient. The somatosensory cortical evoked potential (CEP) is useful in monitoring spinal cord function. However,the CEP is thought to be carried almost exclusively by the posterior columns in man and, therefore, theoretically, an anterior spinal cord lesion could go undetected by this technique. Bremer 1 first described the spontaneous electrical activity of the spinal cord. This electrospinogram (ESG) is thought to arise from segmental neurons and to be composed of a low-voltage background activity tonically maintained by afferent impulses from the periphery and larger sharp waves with amplitudes influenced by supraspinal centers and drugs. 2 When a peripheral nerve is stimulated, an evoked potential can be readily
E
J. Neurosurg. / Volume 43 / December, 1975
recorded from the spinal cord or dorsal root. This spinal evoked potential (SEP) is also modified by other spinal cord systems. The ESG and the SEP, in conjunction with the CEP, were studied in the setting of acute spinal cord trauma in the hope that they might provide early electrical indicators of spinal cord compromise more representative of the entire cord. M a t e r i a l s and M e t h o d s
Twenty-eight adult mongrel cats, weighing between 3 and 4 kg, were placed under halothane anesthesia with vascular (femoral artery and vein) and tracheal cannulation. They were paralyzed, respired, and suspended in a Kopf stereotaxic frame* with main-
*Stereotaxic frame made by David Kopf Instruments, 7324 Elmo Street, Tujunga, California 91042. 737
G. Morrison, R. J. Lorig, J. S. Brodkey and F. E. Nulsen
FIG. 1. The effect of rostral cord compression on the electrospinogram (ESG). Note that both amplitude (left) and frequency (right) were increased.
tenance of normothermia, normotension, and normal arterial blood gases. The left sciatic and superficial radial nerves were isolated, suspended on platinum/iridium stimulating electrodes and immersed in an agar-mineral oil mixture. Anterior and posterior steel screws were placed in the right calvaria, and stainless steel disc electrodes were placed epidurally on either side of the spinal cord in the L-5 region following a thoracolumbar laminectomy. The animals were maintained by either locally anesthetizing all pressure points and open wounds or by infusing pentobarbital (30 mg/kg) intravenously. The amplified ESG, filtered between 2 and 55 Hz, was recorded bipolarly from the epidural electrodes and displayed visually, recorded on a strip chart, and analyzed online by a PDP-11/20 computer for characterization and quantization. A root mean square value (RMS-amplitude) was calculated for a 10-second epoch. These data were converted to a spectral density (frequency spectrum) by fast Fourier transform analysis. This spectral density was integrated to give a frequency distribution of the wave form. The frequency distribution curves were analyzed with respect to the frequency at which 50% of the "energy" of the wave had been represented, and also, as a measure of analyzing the slope of the curves, the frequen738
cy band representing between 20% and 80% of the "energy" for a given 10-second epoch. The peripheral nerves were electrically stimulated by rectangular pulses at a frequency of 0.5 Hz (pulses/sec) at an amplitude of 2 to 4 volts and duration of 0.5 msec while recordings were made from either the epidural spinal or cranial electrodes. Forty such responses were averaged by the computer and displayed as the spinal evoked potential (SEP) or the cortical evoked potential (CEP). A weight was applied to the thoracic cord with a previously described apparatus 4 varying from 38 to 58 gm. The apparatus for compressing the cord consists of a hollow cylindrical aluminum rod, 30 cm in length with a 1 cm 2 baseplate which is anchored over the right and left articular facets. The baseplate has a central hole 7 mm in diameter through which a solid rod can be set on the dorsal surface of the cord. The top of the solid rod has a flat circular platform which holds any additional weight, and the rod itself weighs 18 gm. With this apparatus, weight can be gently applied extradurally to the cord. All electrical parameters were studied before, during, and after a given weight had been applied to the cord for a given period of time. Finally, the thoracic cord was transected and all recordings repeated. J. Neurosurg. / Volume 43 / December, 1975
Electrospinograms and evoked potentials in spinal trauma
FIG. 2. Graph showing the distribution of amplitude changes in ESG following cord compression in 20 animals.
FIG. 3. Graph showing typical changes in ESG frequency distribution before, during, and after cord compression above the recording site.
Results
As recorded epidurally, the amplified ESG is a 5- to 10-/~V (peak-to-peak) wave with a computer-calculated RMS-amplitude of 2 to 3/~V (Fig. 1). The components of the ESG as previously described 2 were appreciated. As the weight was applied to the thoracic cord the amplitude of the ESG was usually enhanced (Fig. 1). These changes were reversible to a certain extent with the cessation of cord compression but did not return to baseline. Figure 2 shows this initial amplitude change during compression in 20 experiments. The amplitude increased variably J. Neurosurg. / Volume 43 / December, 1975
FIG. 4. Graph showing the distribution of mean frequency increases in the ESG following rostral cord compression in 24 animals. from 18% to 230% of the control value with a mean increase of 91%. The ESG had a mean frequency of 7.5 Hz which shifted to 13 Hz with rostral cord compression and then reverted to 7 Hz when the weight was removed (Fig. 3). The frequency band representing between 20% and 80% of the energy for a given 10-second epoch shifted from 4 Hz and 13 Hz to 6 Hz and 19 Hz. The increase in mean frequency in 24 animals ranged from 0.5 Hz to 7 Hz with an average increase of 2.8 Hz (Fig. 4). The average increases at the 20% and 80% points of the integrated normalized energy concurrently shifted from 3 Hz and 12 Hz in the resting state to 5 Hz and 17 Hz after cord compression. In barbiturate-anesthetized animals, RMS values were initially smaller and frequencies slower; changes after trauma were similar but less marked. As a 48- to 58-gm weight was applied to the thoracic cord the CEP as obtained from leg stimulation would generally disappear within 5 to 10 minutes. Technical difficulties were obviated by noting the persistence of the CEP obtained by stimulating the ipsilateral foreleg. The computer-averaged SEP of 40 successive peripheral nerve stimuli recorded caudal to the compression was enhanced (Fig. 5). Following removal of the weight from the cord, the CEP would return and the SEP would diminish somewhat but would not generally reach the control level. In 25 experiments the response varied from no change 739
G. Morrison, R. J. Lorig, J. S. Brodkey and F. E. Nulsen
FIG. 5. Results of a typical experiment in which cord compression abolishes CEP but enhances SEP recorded below the spinal block. fold increase in the amplitude of the ESG 2 as corroborated by this study. Anesthetics have been noted to alter the ESG" and to affect the results of cord transection. An increase in the ESG under ether could not be perceived with barbiturate anesthesia? However, one of the same investigators later reported that cord transection increased the ESG in all preparations. 6 The frequency shift noted here was also seen by Visser, et al., 12 who transected cat spinal cords and reported that the lumbar intramedullary ESG shifted its frequency from 10 and 30 Hz to 30 and 70 Hz. The augmentation of the SEP after cord transection has been reported 2 and the same group has stimulated the brain stem of animals with intact spinal cords and noted Fl~. 6. Graph showing distribution of SEP very interesting variations in the SEP and augmentation following rostral cord compression amplitude of the ESG. 7 This fits well with the in 25 animals. effects noted with spinal cord trauma in the current experiments. It is postulated that when spinal cord trauma isolates the caudal part of the cord, the descending inhibitory in(two animals) to one animal with a 243% fluences on the ESG and the SEP are released amplitude increase. The mean increase was and thus the potentials are augmented. 60% (Fig. 6). Thus, significant changes do occur in the ESG and the SEP caudal to isolated spinal Discussion cord compression in the experimental situaRelatively few investigators have been in- tion. Graded spinal cord compression results volved in the characterization of the ESG and in an amplitude and a frequency increase in its clinical application. Most investigators the caudally recorded ESG and an increase in have used intramedullary ESG recordings to the SEP. ESG's have been recorded from characterize the wave and ascertain the humans by way of percutaneously placed effects of spinal cord manipulation. There has catheters within the cord 9 and epidurally,1~ been disagreement regarding the changes in and Cracco s has recorded an evoked potential the ESG following spinal cord transection. from the surface of the back. Whether these Some groups have reported that after spinal parameters prove valuable in the continuing cord transection the ESG did not change 12 or quest for better monitors of spinal cord funcwas diminished? Others have noted a several- tion intraoperatively remains to be seen. 740
J. Neurosurg. / Volume 43 / December, 1975
E|ectrospinograms and evoked potentials in spinal trauma Acknowledgments The authors gratefully acknowledge the technical assistance of Dennis M. Lorek and Walter F. Good.
References 1. Bremer E: (Spontaneous electrical activity of the spinal cord.) Arch lnt Physiol Biochim 51:51-84, 1941 (Fre) 2. Brust-Carmona H, Levitan H, Kasprzak H, et al: Spinal eleetrogram of the cat. I. Study of origin by degeneration and ischemia. Elec3.
4.
5. 6.
7.
troencephalogr Clin Neurophysiol 26:101-111, 1968 Cracco RQ: Spinal evoked response: peripheral nerve stimulation in man. Eiectroencephalogr Clin Neurophysiol 35:379-386, 1973 Croft T J, Brodkey JS, Nulsen FE: Reversible spinal cord trauma: a model for electrical monitoring of spinal cord function. J Neurosurg 36:402-406, 1972 Horsten GPM: (Spontaneous electrical activity of the mammalian spinal cord.) Arch In/ Physiol Biochim 55:304-306, 1948 (Fre) Kasprzak H, Gasteiger EL: Spinal electrogram of freely moving cat: supraspinal and segmental influences. Brain Res 22:207-220, 1970 Levitan H, Gasteiger EL, Kasprzak H, et al: Spinal eIectrogram of the cat. 2. Supraspinal influences, Eiectroencephalogr Clin Neurophysiol 26:111-118, 1968
J. Neurosurg. / Volume 43 / December, 1975
8. Mark VH, Gasteiger EL: Observations on the role of afferent and descending impulses on the spontaneous potentials of the spinal cord. 9. 10.
11. 12.
Electroencephalogr Clin Neurophysiol 5:251-258, 1953 Pool J: Electrospinogram: spinal cord action potentials recorded from a paraplegic patient. J Neurosurg 3:192-198, 1946 Shimoji K, Hagashi H, Kano T: Epidural recording of spinal electrogram in man. Electroencephalogr Clin Neurophysiol 30:236-239, 1971 ten Cate J: Spontaneous electrical activity of the spinal cord. Electroencephalogr Clln Neurophysiol 2:445-451, 1950 Visser P, ten Cate J, Bodes JTF: (Spinal cord electromyography after the transection of the spinal cord of a cat, dog, and rabbit.)$ Physiol (Paris) 50:557-560, 1972 (Fre)
This work was supported by N I H Grant GM 19599-02. Address for Dr. Morrison: Neurosurgical Associates, 4685 Ponce de Leon Boulevard, Coral Gables, Florida 33146. Address reprint requests to: Jerald S. Brodkey, M.D., 2065 Adelbert Road, Cleveland, Ohio 44106.
741
~" Studies in 28 traumatized cats showed the following acute changes after spinal cord compression in the cord segment below the trauma: 1) increase in size of the spinal cord evoked potential; 2) increase in size of the electrospinogram; and 3) increase in frequency of the electrospinogram. KEvWoRDs 9 spinal cord 9 evoked potential 9 cortex 9 electrospinography 9 spinal cord c o m p r e s s i o n
LECTRICAL assessment of the functional integrity of the spinal cord is especially pertinent when the usual clinical methods are unavailable, for instance, intraoperatively and in the unconscious patient. The somatosensory cortical evoked potential (CEP) is useful in monitoring spinal cord function. However,the CEP is thought to be carried almost exclusively by the posterior columns in man and, therefore, theoretically, an anterior spinal cord lesion could go undetected by this technique. Bremer 1 first described the spontaneous electrical activity of the spinal cord. This electrospinogram (ESG) is thought to arise from segmental neurons and to be composed of a low-voltage background activity tonically maintained by afferent impulses from the periphery and larger sharp waves with amplitudes influenced by supraspinal centers and drugs. 2 When a peripheral nerve is stimulated, an evoked potential can be readily
E
J. Neurosurg. / Volume 43 / December, 1975
recorded from the spinal cord or dorsal root. This spinal evoked potential (SEP) is also modified by other spinal cord systems. The ESG and the SEP, in conjunction with the CEP, were studied in the setting of acute spinal cord trauma in the hope that they might provide early electrical indicators of spinal cord compromise more representative of the entire cord. M a t e r i a l s and M e t h o d s
Twenty-eight adult mongrel cats, weighing between 3 and 4 kg, were placed under halothane anesthesia with vascular (femoral artery and vein) and tracheal cannulation. They were paralyzed, respired, and suspended in a Kopf stereotaxic frame* with main-
*Stereotaxic frame made by David Kopf Instruments, 7324 Elmo Street, Tujunga, California 91042. 737
G. Morrison, R. J. Lorig, J. S. Brodkey and F. E. Nulsen
FIG. 1. The effect of rostral cord compression on the electrospinogram (ESG). Note that both amplitude (left) and frequency (right) were increased.
tenance of normothermia, normotension, and normal arterial blood gases. The left sciatic and superficial radial nerves were isolated, suspended on platinum/iridium stimulating electrodes and immersed in an agar-mineral oil mixture. Anterior and posterior steel screws were placed in the right calvaria, and stainless steel disc electrodes were placed epidurally on either side of the spinal cord in the L-5 region following a thoracolumbar laminectomy. The animals were maintained by either locally anesthetizing all pressure points and open wounds or by infusing pentobarbital (30 mg/kg) intravenously. The amplified ESG, filtered between 2 and 55 Hz, was recorded bipolarly from the epidural electrodes and displayed visually, recorded on a strip chart, and analyzed online by a PDP-11/20 computer for characterization and quantization. A root mean square value (RMS-amplitude) was calculated for a 10-second epoch. These data were converted to a spectral density (frequency spectrum) by fast Fourier transform analysis. This spectral density was integrated to give a frequency distribution of the wave form. The frequency distribution curves were analyzed with respect to the frequency at which 50% of the "energy" of the wave had been represented, and also, as a measure of analyzing the slope of the curves, the frequen738
cy band representing between 20% and 80% of the "energy" for a given 10-second epoch. The peripheral nerves were electrically stimulated by rectangular pulses at a frequency of 0.5 Hz (pulses/sec) at an amplitude of 2 to 4 volts and duration of 0.5 msec while recordings were made from either the epidural spinal or cranial electrodes. Forty such responses were averaged by the computer and displayed as the spinal evoked potential (SEP) or the cortical evoked potential (CEP). A weight was applied to the thoracic cord with a previously described apparatus 4 varying from 38 to 58 gm. The apparatus for compressing the cord consists of a hollow cylindrical aluminum rod, 30 cm in length with a 1 cm 2 baseplate which is anchored over the right and left articular facets. The baseplate has a central hole 7 mm in diameter through which a solid rod can be set on the dorsal surface of the cord. The top of the solid rod has a flat circular platform which holds any additional weight, and the rod itself weighs 18 gm. With this apparatus, weight can be gently applied extradurally to the cord. All electrical parameters were studied before, during, and after a given weight had been applied to the cord for a given period of time. Finally, the thoracic cord was transected and all recordings repeated. J. Neurosurg. / Volume 43 / December, 1975
Electrospinograms and evoked potentials in spinal trauma
FIG. 2. Graph showing the distribution of amplitude changes in ESG following cord compression in 20 animals.
FIG. 3. Graph showing typical changes in ESG frequency distribution before, during, and after cord compression above the recording site.
Results
As recorded epidurally, the amplified ESG is a 5- to 10-/~V (peak-to-peak) wave with a computer-calculated RMS-amplitude of 2 to 3/~V (Fig. 1). The components of the ESG as previously described 2 were appreciated. As the weight was applied to the thoracic cord the amplitude of the ESG was usually enhanced (Fig. 1). These changes were reversible to a certain extent with the cessation of cord compression but did not return to baseline. Figure 2 shows this initial amplitude change during compression in 20 experiments. The amplitude increased variably J. Neurosurg. / Volume 43 / December, 1975
FIG. 4. Graph showing the distribution of mean frequency increases in the ESG following rostral cord compression in 24 animals. from 18% to 230% of the control value with a mean increase of 91%. The ESG had a mean frequency of 7.5 Hz which shifted to 13 Hz with rostral cord compression and then reverted to 7 Hz when the weight was removed (Fig. 3). The frequency band representing between 20% and 80% of the energy for a given 10-second epoch shifted from 4 Hz and 13 Hz to 6 Hz and 19 Hz. The increase in mean frequency in 24 animals ranged from 0.5 Hz to 7 Hz with an average increase of 2.8 Hz (Fig. 4). The average increases at the 20% and 80% points of the integrated normalized energy concurrently shifted from 3 Hz and 12 Hz in the resting state to 5 Hz and 17 Hz after cord compression. In barbiturate-anesthetized animals, RMS values were initially smaller and frequencies slower; changes after trauma were similar but less marked. As a 48- to 58-gm weight was applied to the thoracic cord the CEP as obtained from leg stimulation would generally disappear within 5 to 10 minutes. Technical difficulties were obviated by noting the persistence of the CEP obtained by stimulating the ipsilateral foreleg. The computer-averaged SEP of 40 successive peripheral nerve stimuli recorded caudal to the compression was enhanced (Fig. 5). Following removal of the weight from the cord, the CEP would return and the SEP would diminish somewhat but would not generally reach the control level. In 25 experiments the response varied from no change 739
G. Morrison, R. J. Lorig, J. S. Brodkey and F. E. Nulsen
FIG. 5. Results of a typical experiment in which cord compression abolishes CEP but enhances SEP recorded below the spinal block. fold increase in the amplitude of the ESG 2 as corroborated by this study. Anesthetics have been noted to alter the ESG" and to affect the results of cord transection. An increase in the ESG under ether could not be perceived with barbiturate anesthesia? However, one of the same investigators later reported that cord transection increased the ESG in all preparations. 6 The frequency shift noted here was also seen by Visser, et al., 12 who transected cat spinal cords and reported that the lumbar intramedullary ESG shifted its frequency from 10 and 30 Hz to 30 and 70 Hz. The augmentation of the SEP after cord transection has been reported 2 and the same group has stimulated the brain stem of animals with intact spinal cords and noted Fl~. 6. Graph showing distribution of SEP very interesting variations in the SEP and augmentation following rostral cord compression amplitude of the ESG. 7 This fits well with the in 25 animals. effects noted with spinal cord trauma in the current experiments. It is postulated that when spinal cord trauma isolates the caudal part of the cord, the descending inhibitory in(two animals) to one animal with a 243% fluences on the ESG and the SEP are released amplitude increase. The mean increase was and thus the potentials are augmented. 60% (Fig. 6). Thus, significant changes do occur in the ESG and the SEP caudal to isolated spinal Discussion cord compression in the experimental situaRelatively few investigators have been in- tion. Graded spinal cord compression results volved in the characterization of the ESG and in an amplitude and a frequency increase in its clinical application. Most investigators the caudally recorded ESG and an increase in have used intramedullary ESG recordings to the SEP. ESG's have been recorded from characterize the wave and ascertain the humans by way of percutaneously placed effects of spinal cord manipulation. There has catheters within the cord 9 and epidurally,1~ been disagreement regarding the changes in and Cracco s has recorded an evoked potential the ESG following spinal cord transection. from the surface of the back. Whether these Some groups have reported that after spinal parameters prove valuable in the continuing cord transection the ESG did not change 12 or quest for better monitors of spinal cord funcwas diminished? Others have noted a several- tion intraoperatively remains to be seen. 740
J. Neurosurg. / Volume 43 / December, 1975
E|ectrospinograms and evoked potentials in spinal trauma Acknowledgments The authors gratefully acknowledge the technical assistance of Dennis M. Lorek and Walter F. Good.
References 1. Bremer E: (Spontaneous electrical activity of the spinal cord.) Arch lnt Physiol Biochim 51:51-84, 1941 (Fre) 2. Brust-Carmona H, Levitan H, Kasprzak H, et al: Spinal eleetrogram of the cat. I. Study of origin by degeneration and ischemia. Elec3.
4.
5. 6.
7.
troencephalogr Clin Neurophysiol 26:101-111, 1968 Cracco RQ: Spinal evoked response: peripheral nerve stimulation in man. Eiectroencephalogr Clin Neurophysiol 35:379-386, 1973 Croft T J, Brodkey JS, Nulsen FE: Reversible spinal cord trauma: a model for electrical monitoring of spinal cord function. J Neurosurg 36:402-406, 1972 Horsten GPM: (Spontaneous electrical activity of the mammalian spinal cord.) Arch In/ Physiol Biochim 55:304-306, 1948 (Fre) Kasprzak H, Gasteiger EL: Spinal electrogram of freely moving cat: supraspinal and segmental influences. Brain Res 22:207-220, 1970 Levitan H, Gasteiger EL, Kasprzak H, et al: Spinal eIectrogram of the cat. 2. Supraspinal influences, Eiectroencephalogr Clin Neurophysiol 26:111-118, 1968
J. Neurosurg. / Volume 43 / December, 1975
8. Mark VH, Gasteiger EL: Observations on the role of afferent and descending impulses on the spontaneous potentials of the spinal cord. 9. 10.
11. 12.
Electroencephalogr Clin Neurophysiol 5:251-258, 1953 Pool J: Electrospinogram: spinal cord action potentials recorded from a paraplegic patient. J Neurosurg 3:192-198, 1946 Shimoji K, Hagashi H, Kano T: Epidural recording of spinal electrogram in man. Electroencephalogr Clin Neurophysiol 30:236-239, 1971 ten Cate J: Spontaneous electrical activity of the spinal cord. Electroencephalogr Clln Neurophysiol 2:445-451, 1950 Visser P, ten Cate J, Bodes JTF: (Spinal cord electromyography after the transection of the spinal cord of a cat, dog, and rabbit.)$ Physiol (Paris) 50:557-560, 1972 (Fre)
This work was supported by N I H Grant GM 19599-02. Address for Dr. Morrison: Neurosurgical Associates, 4685 Ponce de Leon Boulevard, Coral Gables, Florida 33146. Address reprint requests to: Jerald S. Brodkey, M.D., 2065 Adelbert Road, Cleveland, Ohio 44106.
741
