Anesth Analg 2002;94:907-912
© 2002 International Anesthesia Research Society
TECHNOLOGY, COMPUTING, AND SIMULATION
Motor-Evoked Potential Facilitation During Progressive Cortical Suppression by Propofol
Kai-Michael Scheufler, MD, and
Josef Zentner, MD, PhD
Department of Neurosurgery, University of Freiburg, Freiburg, Germany
Address correspondence and reprint requests to Kai-Michael Scheufler, MD, Abt. Allgemeine Neurochirurgie, Universitätsklinikum Freiburg, Breisacher Str. 64, D-79106 Freiburg, Germany. Address e-mail to scheufle{at}nz11.ukl.uni-freiburg.de
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Abstract
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We characterized the effects of various stimulation patterns on motor-evoked potentials (MEPs) elicited by repetitive transcranial magnetoelectric stimulation at different levels of cortical suppression by propofol. In 20 patients undergoing lumbar disk surgery, propofol target plasma concentrations (PTPCs) were increased incrementally by target plasma-level controlled infusion during the induction of anesthesia. MEPs were recorded from the muscles of the upper extremities after single, double, and quadruple magnetoelectric stimulation at 500, 200, and 100 Hz. The mean PTPC during loss of responsiveness to verbal instructions (CP50) was 3 µg/mL (CP95, 5 µg/mL). At PTPCs <3 µg/mL, maximal MEP amplitudes were elicited by quadruple stimulation at 100 Hz. At PTPCs 
3 µg/mL, four pulses at 200 Hz yielded peak MEP amplitudes. Therefore, quadruple magnetoelectric stimulation at 100 Hz yields peak myogenic responses in awake patients. With progressive cortical suppression resulting from PTPCs beyond 3 µg/mL, the most effective stimulation frequency shifts to 200 Hz. This may be explained by a differential dose-dependent action of propofol on GABAergic cortical interneurons, corresponding to the clinically observed state of vigilance. Recording of spinal cord evoked potentials will aid in further elucidation of the modulatory effects of general anesthesia on intracortical facilitation.
IMPLICATIONS: We investigated the effect of different transcranial magnetoelectric stimulation paradigms on motor-evoked potentials during different levels of cortical suppression by propofol. The most effective stimulation frequency seems to change from 100 to 200 Hz during progressive propofol dose escalation, possibly because of specific interaction with cortical interneurons.
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Introduction
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Numerous investigations have examined mechanisms of facilitation and inhibition of motor-evoked potentials (MEPs) in humans (1–4). Various theories have been established regarding the physiology of facilitation and inhibition of myogenic responses after electric or magnetoelectric stimulation of the motor cortex (4–9). Facilitation may be dependent on both cortical and spinal mechanisms. Corticocortical facilitative phenomena have been observed during repetitive electric and magnetoelectric stimulation at several discrete interstimulus intervals (ISIs) from 1 to 20 ms. Reciprocally, corticocortical inhibition (mediated by GABAergic inhibitory interneurons) also results from a range of distinct stimulation frequencies (2–4,6,10,11). The theoretical mechanisms of MEP facilitation after electrical stimulation during general anesthesia have been described in clinical investigations (7). Temporal and spatial summation of excitatory postsynaptic potentials at the spinal 
-motoneuron after repetitive electric stimulation of the motor cortex may enhance myogenic responses, with the most effective stimulation frequencies observed within the range of 200–500 Hz with multiple stimuli (7). This has led to the implementation of high-frequency repetitive electric stimulation for intraoperative monitoring of myogenic MEP under general anesthesia with various anesthetic protocols (12).
Although perioperative evaluation of MEP after magnetoelectric cortical stimulation (tcMMEP) is progressively being integrated into electrophysiologic monitoring of neurosurgical patients, the main goal has been to improve the assessment of different components of the motor system and to enhance both sensitivity and specificity of intraoperative changes. However, reliable interpretation of myogenic potentials elicited by intraoperative electric or magnetoelectric stimulation of the motor cortex remains cumbersome, chiefly because of the effects of general anesthesia. Therefore, numerous studies have addressed the differential effects of various anesthetics on MEP (13–17). However, the specific effect of anesthesia on the mechanisms of cortical and spinal facilitation has not been investigated in detail. In our study, we investigate facilitative phenomena after repetitive high-frequency train magnetoelectric stimulation of the motor cortex during progressive suppression of cortical activity by propofol, a 
-aminobutyric acid (GABA)-A agonist (18), administered in incremental doses by target plasma-level controlled infusion (TCI). GABA is the major inhibitory neurotransmitter in the mammalian central nervous system (19).
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Methods
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Twenty patients (10 men and 10 women) undergoing lumbar disk surgery were recruited for the study after written, informed consent was obtained. The study protocol was performed according to the declaration of Helsinki and was approved by our IRB. Preexisting motor deficits revealed by neurological and electrophysiological assessment (electromyographic studies and preoperative tcMMEP of the target muscles) precluded admission to the study protocol. Earplugs were inserted during stimulation under baseline conditions and in the awake patients to avoid transient threshold (T) shifts induced by the acoustic stimulus associated with the discharge of the stimulation coil. The mean age of our patient population was 39 ± 8 yr (mean ± SD; range, 28–49 yr). All patients received 1 mg of flunitrazepam orally at least 12 h before surgery to prevent significant effects on MEP during this study. No further sedatives or other centrally acting drugs were given before the induction of anesthesia. The patients were positioned supine on the operating table, with an IV line for the administration of fluids; IV anesthetics were placed on the arm contralateral to the MEP recording site. Mean arterial blood pressure was maintained >70 mm Hg, and hemoglobin oxygen saturation (>97%) and rectal temperature (37°C) were continuously assessed and held constant. Surface electromyographic recordings were made from the abductor pollicis brevis, abductor digiti minimi, and forearm flexor muscles by using Ag/AgCl cup electrodes in a belly-tendon montage. Electrode impedances <20 k
were accepted (mean electrode impedances <5 k). Standard electrophysiological equipment (SpiritTM evoked potential system; Nicolet Biomedical, Madison, WI) was used to record MEP. The high-pass filter was set to 30 Hz, and the low pass filter was set to 3 kHz. The notch filter was deactivated. The stimulating device (Magstim Quadropulse 500TM; Inomed, Teningen, Germany), capable of delivering up to four consecutive stimuli (pulses), each with a magnetic field pulse duration of 
500 µs, delivered at frequencies ranging from 10 Hz to 1 kHz and a maximal magnetic field strength of 2.5 tesla (corresponding induced tissue current 15 mA/cm2), was connected to the Spirit evoked potential system and was used as an external triggering device. We used a double-cone, highly focal coil (Magstim, Whitland, UK) placed perpendicular to the assumed line of the central sulcus. The coil position most suitable for activation of the target muscles was adjusted to yield consistent maximal MEP amplitudes at T stimulation intensity. In 60% of patients, the right motor cortex was stimulated, whereas stimulation of the left motor cortex was conducted in the remaining 40%. The coil was held in position by a specially designed clamp attached to the operating table. Resting MEPs were recorded without prior voluntary contraction of the target muscles.
An open three-compartment pharmacokinetic model (20) for propofol has been incorporated into a TCI system (DiprifusorTM; Zeneca Pharmaceuticals, Cheshire, UK), which calculates and maintains an appropriate propofol target plasma concentration (PTPC) with respect to individual patient characteristics and the desired level of surgical anesthesia. The TCI system continuously calculates the concentration of the drug within each of the three compartments, maintaining a constant PTPC independent of the duration of infusion. In each patient, PTPC was incrementally increased in steps of 1 µg/mL until complete suppression of evoked myogenic activity at all three recording sites was achieved. All patients received supplemental oxygen by mask beyond an anesthetic PTPC of 3 µg/mL. In a subgroup of patients (all men) who received peak PTPCs of up to 7 µg/mL to induce complete suppression of MEP, assisted mask ventilation was performed to maintain adequate oxygenation. Upon maximal suppression of MEP, patients received alfentanil (40 µg/kg), atropine sulfate (0.5 mg), and cisatracurium (0.4 mg/kg) before endotracheal intubation was performed.
The investigational protocol consisted of the following eight steps, beginning with the determination of the individual resting motor T under baseline conditions in each patient.
- Step 1. Determination of T, defined as the stimulator’s fractional output (Of, in percentage of 2.5 tesla) producing a myogenic potential of 50 µV after the application of a single-pulse stimulation (SPS) in at least 5 of 10 successive recordings.
- Step 2. Application of an SPS at T + 10% Of.
- Step 3. Application of an SPS at T + 20% Of.
- Step 4. Application of an SPS at T + 30% Of.
- Step 5. Double-pulse stimulation (DPS; 500 Hz) at T + 30% Of.
- Step 6. Quadruple-pulse stimulation (QPS; 500 Hz) at T + 30% Of.
- Step 7. QPS (200 Hz) at T + 30% Of.
- Step 8. QPS (100 Hz) at T + 30% Of.
Steps 2–8 were performed in random order, both under baseline conditions and after reaching each of the preset PTPCs (1, 2, 3. . .n µg/mL) to exclude systematic influences on MEP characteristics caused by the possible conditioning effects of repetitive stimulation. Ten minutes was allowed for equilibration after each step increase in PTPC. Four consecutive MEP recordings (separated by 20 s) were averaged during each stimulation paradigm (Steps 2–8) to ensure consistency of the results. For statistical analysis, a grand average including data from all muscle groups was calculated. MEPs were independently reviewed by two single-blinded investigators, with amplitudes measured from peak to peak as well as from peak to baseline. Latencies were defined as the interval between the first stimulation artifact and the onset of the MEP.
Data are expressed as mean ± SD or as median and range in those instances with substantial deviation from normal distribution of data. Two-sample significance of data that departed from a normal distribution was tested with the Mann-Whitney U-test. Simple regression analysis or Pearson’s correlation was used to relate continuous variables to one another. Analysis of variance (Kruskal-Wallis test) was used to describe differences in distribution among the various groups. Statistical significance was assumed for P < 0.05. All statistical analyses were performed with Statistica 5.0 (StatSoft, Hamburg, Germany).
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Results
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The T stimulus intensity to evoke reproducible tcMMEPs at each of the three recording sites in four consecutive recordings was 48.8% ± 11.7% (range, 20%–60%) of maximal stimulator output (maximal stimulator output, 2 tesla). No significant differences with respect to T stimulus intensity were found with respect to age or sex or between the left and right hemisphere (P > 0.63). MEP amplitudes and latencies recorded from the three muscle groups did not differ significantly throughout the whole study (P > 0.3; Fig. 1). No associations were found between changes in MEP amplitudes and latencies or phase numbers (Table 1). An average PTPC of 3 ± 1 µg/mL (range, 2–4 µg/mL) induced loss of responsiveness to verbal instructions in 50% of patients (CP50), whereas 5 ± 1 µg/mL (range, 4–7 µg/mL) induced loss of responsiveness in 95% of patients (CP95) and, in combination with 40 µg/kg alfentanil, tolerance to endotracheal intubation.
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Figure 1. Scatterplots of motor-evoked potential (MEP) amplitudes (µV) from three different muscle groups (thenar, hypothenar, and forearm flexors). Average MEP amplitudes from four consecutive recordings are plotted. MEP amplitudes from all three muscle groups are closely correlated (Spearman’s rank correlation coefficient [r] 0.8). The slope of the linear regression curve and the multiple correlation coefficient (R2) are specified in the graph.
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In general, a dose-dependent suppression of MEP amplitudes with increasing PTPC was noted (Fig. 2). As expected, MEP elicited by low-stimulation intensities near T (T + 10% and T + 20%) were obtained in awake patients only (PTPC 
3 µg/mL). Beyond the apparent CP50 of 3 µg/mL, stimulation intensities had to be increased to supra-T levels (minimum, T + 30%) to elicit MEP with SPS (Fig. 2).
At PTPCs ranging from 0 to 3 µg/mL, MEP amplitudes were directly related to stimulus intensity after SPS (Fig. 2, Table 2). Baseline MEP amplitudes at T were approximately doubled at T + 10% and quadrupled at T + 30% (Fig. 2). MEP latencies (23.9 ± 3.5 ms) were not affected by either the stimulation paradigm or PTPC throughout the whole study protocol.
The effect of different stimulation frequencies and pulse numbers on MEP amplitude was compared with the results obtained after SPS with a fixed stimulation intensity of T + 30%. No significant facilitative effects (i.e., increases in MEP amplitude) resulted from DPS at 500 Hz as compared with SPS (Fig. 2). MEPs recorded from forearm flexors were preserved up to peak a PTPC of 6 µg/mL; however, consistently lower MEP amplitudes (P < 0.05) were observed after DPS as compared with SPS (both at T + 30%) at PTPCs 5 µg/mL. With PTPCs ranging from 0 to 3 µg/mL, QPS at 100, 200, and 500 Hz yielded significantly larger MEPs than SPS and DPS (P < 0.05). At PTPCs of 0, 1, and 2 µg/mL, peak MEP amplitudes were recorded after QPS at 100 Hz (Figs. 2 and 3, Table 2). However, beyond a PTPC of 3 µg/mL, repetitive stimulation with four pulses at 200 Hz consistently produced maximal MEP amplitudes and the most reliable (i.e., reproducible) myogenic responses at all recording sites (Fig. 2, Table 2). This transition of the most effective stimulation frequency with regard to MEP amplitude from 100 to 200 Hz (P < 0.05) was associated with CP50 at PTPCs 3 µg/mL (Fig. 2, Table 2).
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Figure 3. Representative recordings from forearm flexors after double-pulse stimulation (DPS) and quadruple-pulse stimulation (QPS) at 100, 200, and 500 Hz (propofol target plasma concentration, 1 µg/mL). Stimulation artifacts are signified by arrows. The baseline is truncated, thus including only the latest stimulation artifacts in each recording. Motor-evoked potential (MEP) morphology (especially phase number) was significantly altered during QPS at 100 and 200 Hz as compared with single-pulse stimulation and DPS, whereas MEP latencies remained unchanged by stimulus number and frequency. T = threshold.
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Discussion
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An open, three-compartment pharmacokinetic model for propofol (20) has been incorporated into a TCI system (Diprifusor), allowing the clinician to achieve and maintain defined target blood concentrations. This should add to both ease and confidence in interpreting MEP during intraoperative monitoring, especially during separation of potential changes originating from a primary neurological lesion or surgical manipulation, respectively. Although there is no single blood concentration of an anesthetic that will result in satisfactory anesthesia for all patients and all surgical conditions (21), our study was designed to evaluate the effects of different stimulus intensities, pulse numbers, and stimulation frequencies on MEPs during transcranial magnetoelectric stimulation at different clinically relevant PTPCs. Constant physiological conditions were provided in all patients, minimizing influences from temperature, blood pressure, or different levels of apprehension. Experience from previous investigations (7,12) has shown that no confounding effects caused by the premedication used in this study (1 mg of flunitrazepam 12 hours before commencing with the investigation) are to be expected.
Propofol primarily augments inhibitory GABAergic intracortical circuits. Therefore, significant influences on the generation of I-waves involved in the activation of cortical motoneurons by magnetoelectric stimulation would be expected, rather than D-waves resulting from direct depolarization at the axonal hillock of motoneurons by electric stimulation. In addition, this study aimed to elucidate the neurophysiological effects attributable to the transition from consciousness to progressive levels of sedation induced by propofol. For these reasons, magnetoelectric stimulation, rather than electric stimulation, was used.
An average PTPC of 3 µg/mL produced loss of responsiveness to verbal instructions in 50% of our patients (CP50), whereas CP95 (and tolerance to endotracheal intubation after the additional administration of 40 µg/kg alfentanil) was attained at 5 µg/mL. This is in agreement with both the literature and the average values of our general neurosurgical patient population.
MEP amplitudes, but not latencies, were influenced by PTPC as well as by stimulation intensity and frequency. At PTPCs <3 µg/mL, maximal MEP amplitudes were elicited by train-of-four magnetic stimuli delivered at 100 Hz. Beyond PTPCs of 3 µg/mL, the most effective stimulation frequency shifted toward 200 Hz. The number of MEP phases was closely related to stimulation frequency. Decreasing the stimulation frequency resulted in progressive MEP polyphasia in the awake patient, whereas oligophasic MEPs were observed after both SPS and high-frequency repetitive stimulation at 500 Hz during significant cortical suppression (PTPC 5 µg/mL).
These results indicate a differential modification of cortical excitability during incremental suppression by a GABA agonist (propofol). In the absence of significant cortical suppression, MEP facilitation involving excitatory interneuronal circuits seems most effective at an ISI of 10 ms. However, progressive cortical suppression shifts the most effective stimulation pattern producing peak myogenic responses from 100 to 200 Hz. These findings differ from those reported by a previous study (9), which concluded that the stimulation frequency yielding peak myogenic responses after paired magnetoelectric stimulation remains unaffected by the administration of GABA agonists, such as ethanol, lorazepam, or vigabatrin. However, a different stimulation paradigm was used in that study, which used a first supra-T and a second sub-T stimulus. Furthermore, only ISIs ranging from 1 to 5 ms (producing peak myogenic responses at 1.2, 2.3–3, and 4.1—4.5 ms) were investigated (9), whereas earlier findings indicated a marked inhibitory effect of ethanol on intracortical facilitation during paired magnetic stimulation at ISIs of 8–12 ms (22,23). In addition, the individual drug concentrations were much smaller than in our study and therefore presumably were not sufficient to evoke a comparable amount of intracortical inhibition. The sequential shift of the most effective stimulation frequency during progressive cortical suppression has not been described. This finding may be explained by progressive suppression of I-waves. Because neocortical inhibitory interneurons synapse on pyramidal cells proximal to excitatory inputs, they may effectively block activation of corticospinal neurons by inhibitory control of arriving I-waves (24).
Analysis of spinal cord MEPs after electric stimulation of the motor cortex in a primate model has shown gradual stepwise T increases with respect to eliciting D-waves and the subsequent five to seven I-wave discharges during anesthesia (termed I1 to In in the order of appearance; see Ref. 25). Furthermore, I-waves are gradually suppressed by general anesthesia in reverse order, i.e., starting with the latest I-wave components (In) toward the early discharges. However, the exact mechanism by which propofol interacts with the cortical interneuronal system to suppress I-wave-mediated activation of corticospinal neurons after magnetoelectric stimulation remains to be elucidated in detail.
MEPs evoked by repetitive transcranial magnetoelectric stimulation result from the activation of a complex intracortical circuitry, which may be inhibited or facilitated by a range of discrete stimulus frequencies between 1000 and 100 Hz. The electrophysiological correlate of intracortical activation by a magnetoelectric stimulus resembles I-waves, presumably originating from synchronized discharge of cortical motoneurons. In turn, I-wave production by motoneurons is primarily controlled by GABA-related interneuronal circuits. Inhibitory synapses are less numerous and strategically better located than excitatory synapses, indicating that inhibition may be more efficient and therefore less energy consuming. These findings favor the assumption of a baseline inhibitory control of the central motor circuitry. During the induction of anesthesia with GABAergic substances, this baseline intracortical inhibition is augmented in a dose-dependent manner. Moreover, the most effective stimulation frequency maintaining peak MEP amplitudes after magnetoelectric stimulation progressively shifts from 100 Hz toward a frequency range of 200–500 Hz. This phenomenon may be explained by the suppression of I-waves and, therefore, intracortical facilitation.
The results of this study underscore the importance of using suitable stimulation paradigms for both perioperative and intraoperative monitoring of MEPs. Additional studies, including spinal recordings of D- and I-waves at different stimulation frequencies and different levels of anesthesia, are required to further elucidate the physiological mechanisms of cortical and spinal facilitation during magnetoelectric stimulation of the motor cortex.
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Acknowledgments
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Supported by Grants Ze 267/3-1 and Ze 267/3-2 from the Deutsche Forschungsgemeinschaft.
We thank Winfried Blumrich, MD, Department of Anesthesiology at the University Clinic of Freiburg, for providing expert help during preparation of the study protocol.
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References
|
|---|
-
Abbruzzese G, Buccolieri A, Marchese R, et al. Intracortical inhibition and facilitation are abnormal in Huntington’s disease: a paired magnetic stimulation study. Neurosci Lett 1997; 228: 87–90.[ISI][Medline]
-
Valls-Sole J, Pascual-Leone A, Wassermann EM, Hallett M. Human motor evoked responses to paired transcranial magnetic stimuli. Electroencephalogr Clin Neurophysiol 1992; 85: 355–64.[ISI][Medline]
-
Ziemann U, Rothwell JC, Ridding MC. Interaction between intracortical inhibition and facilitation in human motor cortex. J Physiol 1996; 496: 873–81.[ISI][Medline]
-
Ziemann U, Rothwell JC. I-waves in motor cortex. J Clin Neurophysiol 2000; 17: 397–405.[ISI][Medline]
-
Amassian VE, Stewart M, Quirk GJ, Rosenthal JL. Physiological basis of motor effects of a transient stimulus to cerebral cortex. Neurosurgery 1987; 20: 74–93.[ISI][Medline]
-
Pascual-Leone A, Tormos JM, Keenan J, et al. Study and modulation of human cortical excitability with transcranial magnetic stimulation. Electroencephalogr Clin Neurophysiol 1998; 15: 333–43.
-
Pechstein U, Cedzich C, Nadstawek J, Schramm J. Transcranial high-frequency repetitive electric stimulation for recording myogenic motor evoked potentials with the patient under general anesthesia. Neurosurgery 1996; 39: 335–43.[ISI][Medline]
-
Stokic DS, McKay WB, Scott L, et al. Intracortical inhibition of lower limb motor-evoked potentials after paired transcranial magnetic stimulation. Exp Brain Res 1997; 117: 437–43.[ISI][Medline]
-
Ziemann U, Tergau F, Wassermann EM, et al. Demonstration of facilitatory I-wave interaction in the human motor cortex by paired transcranial magnetic stimulation. J Physiol 1998; 511: 181–90.[Abstract/Free Full Text]
-
Chen R, Classen J, Gerloff C, et al. Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology 1997; 48: 1398–403.[Abstract]
-
Wassermann EM, Wedegaertrner FR, Ziemann U, et al. Crossed reduction of human motor cortex excitability by 1-Hz transcranial magnetic stimulation. Neurosci Lett 1998; 250: 141–4.[ISI][Medline]
-
Pechstein U, Nadstawek J, Zentner J, Schramm J. Isoflurane plus nitrous oxide versus propofol for recording of motor evoked potentials after high frequency repetitive electric stimulation. Electroencephalogr Clin Neurophysiol 1998; 108: 175–81.[Medline]
-
Jennum P, Winkel H, Fuglsang-Frederiksen A. Repetitive magnetic stimulation and motor evoked potentials. Electroecephalogr Clin Neurophysiol 1995; 97: 96–101.
-
Kalkman CJ, Drummond JC, Ribberink AA. Effects of propofol, etomidate, midazolam and fentanyl on motor evoked responses to transcranial electric or magnetic stimulation in humans. Anesthesiology 1992; 76: 502–9.[ISI][Medline]
-
Lee WY, Hou WY, Yang LH, Lin SW. Intraoperative monitoring of motor function by magnetic motor evoked potentials. Neurosurgery 1995; 36: 493–500.[ISI][Medline]
-
Taniguchi M, Nadstawek J, Langenbach U, et al. Effect of four anesthetic agents on motor evoked potentials elicited by magnetic transcranial stimulation. Neurosurgery 1993; 33: 407–15.[ISI][Medline]
-
Zentner J, Albrecht T, Heuser D. Influence of halothane, enflurane and isoflurane on motor evoked potentials. Neurosurgery 1992; 31: 298–305.[ISI][Medline]
-
Antkowiak B. Different actions of general anesthetics on the firing patterns of neocortical neurons mediated by the GABA(A) receptor. Anesthesiology 1999; 91: 500–11.[ISI][Medline]
-
McCormick DA. GABA as an inhibitory neurotransmitter in human cerebral cortex. J Neurophysiol 1989; 62: 1018–27.[Abstract/Free Full Text]
-
Coetzee JF, Glen JB, Wium CA, Boshoff L. Pharmacokinetic model selection for target controlled infusions of propofol. Anesthesiology 1995; 82: 1328–45.[ISI][Medline]
-
Adam HK, Kay B, Douglas EJ. Blood disoprofol levels in anaesthetised patients: correlation of concentrations after single or repeated doses with hypnotic activity. Anaesthesia 1982; 37: 536–40.[ISI][Medline]
-
Ziemann U, Lonnecker S, Paulus W. Enhancement of human motor cortex by ethanol: a transcranial magnetic stimulation study. Brain 1995; 118: 1437–46.[Abstract/Free Full Text]
-
Inghilleri M, Berardelli A, Marchetti P, Manfredi M. Effects of diazepam, baclofen and thiopental on the silent period evoked by transcranial magnetic stimulation in humans. Exp Brain Res 1996; 109: 467–72.[ISI][Medline]
-
DeFelipe J, Hendry SH, Jones EG. Visualization of chandelier cell axons by parvalbumin immunoreactivity in monkey cerebral cortex. Proc Natl Acad Sci U S A 1989; 86: 2093–7.[Abstract/Free Full Text]
-
Ghaly RF, Stone JL, Lee J, et al. Monitoring spinal cord motor and somatosensory evoked potentials in anesthetized primates. Neurol Res 1999; 21: 359–67.[ISI][Medline]
Accepted for publication December 14, 2001.
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Abstract
Introduction
