Mapping the brainstem: floor of the fourth ventricle

Intraoperative Monitoring of Neural Function Handbook of Clinical Neurophysiology, Vol. 8 M.R. Nuwer (Ed.) # 2008 Elsevier B.V. All rights reserved

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CHAPTER 23

Mapping the brainstem: floor of the fourth ventricle Jaime R. Lo´pez* Department of Neurology and Neurological Sciences, Stanford University School of Medicine, Stanford, CA 94305, USA

23.1. Introduction Surgical treatment of brainstem lesions carries a substantial risk of postoperative morbidity because of the risk of injuring the tightly packed cranial nerve nuclei (CNN) and neural tracts within the rhomboid fossa and brainstem (Lang et al., 1991). Historically, neurosurgeons considered this area to be a “no man’s land” with most lesions being inoperable (Baker, 1965; Katsuta et al., 1993). However, with the study by Lassiter et al. (1971), surgical treatment of intraaxial brainstem lesions has been considered a realistic option. In addition, continued improvement of technical imaging and microsurgical techniques has allowed for increased success in the treatment of brainstem lesions (Heffez et al., 1990). The improvement in magnetic resonance imaging (MRI) now allows better definition of the pathological anatomy within the brainstem and in many cases is also useful in helping to predict the pathology of the lesion (Heffez et al., 1990). Furthermore, the increased use of intraoperative neurophysiologic monitoring (IOM) with somatosensory evoked potentials (SEPs), brainstem auditory evoked potentials (BAEPs), and motor evoked potentials (MEPs) has helped to reduce postoperative neurologic deficits (Strauss et al., 1994; Steinberg et al., 2000). Unfortunately, these conventional neurophysiologic techniques are of limited use when attempting to surgically resect intra-axial brainstem lesions because they cannot be used to identify and map functional structures on the brainstem surface. This is of great importance because neurologic deficits can occur from mechanical and/or vascular injury to neural pathways and nuclei during surgical *

Correspondence to: Jaime R. Lo´pez, M.D., Intraoperative Neurophysiologic Monitoring Program, Department of Neurology and Neurological Sciences, and Neurosurgery, Stanford University School of Medicine, Room A343, 300 Pasteur Dr., Stanford, CA 94305, USA. Tel.: þ1-650-723-1975; fax: þ1-650-725-5095. E-mail: [email protected] (J.R. Lo´pez).

dissection of surface structures prior to the resection of intrinsic brainstem lesions (Strauss et al., 1994). Thus, it is critical to be able to identify surface brainstem structures since the majority of intrinsic brainstem lesions are approached through the fourth ventricle. Anatomical landmarks may not be discernible because they may be distorted by disease. Therefore, the use of neurophysiologic techniques to assist in identifying neural structures, allowing the surgeons to avoid these structures during surgery, has been advocated (Eisner et al., 1995).

23.2. Floor of the fourth ventricle anatomical landmarks It is imperative to have an understanding of the anatomy of the rhomboid fossa in order to properly plan the neurophysiologic techniques to use for mapping and monitoring of the brainstem. Anatomical landmarks of this area have been reported by Lang et al. (1991). They found that the striae medullares could not be considered an anatomical landmark because of its highly variable location on the surface. In addition, in 14% of their sample, no stria was seen. They also found that the broadest area of the rhomboid fossa is more frequently not the midpoint of its length. This is important because the facial colliculus is normally located above the striae. However, if the striae are not present, then visual identification of the facial colliculus becomes very difficult (Strauss et al., 1994). It is of critical importance to identify the facial colliculus because injury to this region may cause not only facial nerve dysfunction but also disturbance of the abducens nucleus, eye movements, and vestibular function because of the different neural pathways located in this area (Lang et al., 1991). The abducens nucleus and the medial longitudinal fasciculus (MLF) are in close proximity to the facial colliculus. The parapontine reticular formation (PPRF) is ventral and medial to the facial colliculus while the vestibular nuclei are lateral (Strauss et al., 1994). The

BRAINSTEM AND AUDITORY EVOKED POTENTIALS

ability to precisely identify functional neural structures is further complicated by the distortion and displacement produced by intrinsic brainstem space occupying lesions (Strauss et al., 1994; Eisner et al., 1995; Morota et al., 1996). Therefore, the need for a method to identify functional structures on the surface of the rhomboid fossa is vital. Such a technique, using electrical stimulation of brainstem surface structures, was first mentioned by Fahlbusch and Strauss in 1991 (Lang et al., 1991; Katsuta et al., 1993). Subsequently, similar techniques have been described by other authors (Rusyniak et al., 1992; Katsuta et al., 1993; Strauss et al., 1993; Eisner et al., 1995; Morota et al., 1995, 1996; Chang et al., 1999). 23.3. Assessment of brainstem function Routine, conventional neurophysiologic monitoring of brainstem function typically requires the use of BAEPs, SEPs, and MEPs. The combined multimodality use of SEPs and MEPs allows for monitoring of a larger brainstem territory. However, the combined use of these conventional modalities provides electrophysiologic coverage of only 20% of the brainstem cross-sectional area between the pontomedullary and pontomesencephalic junctions at any given level (Lang et al., 1991; Strauss et al., 1994). In addition, these conventional techniques are not useful in identifying surface structures prior to dissection. However, using techniques similar to those used for stimulation of peripheral nerve fibers, brainstem structures can be safely and reliably activated; thus, allowing for identification of the neural structures (Katsuta et al., 1993). 23.4. Brainstem stimulation The purpose of electrical stimulation of brainstem structures is to identify cranial motor nuclei and their motor tracts. The nucleus of most interest is the facial colliculus, not only because it lies above important neural structures as mentioned previously, but also because it lies only 0.25 mm beneath the ependyma. The hypoglossal nucleus is also reported to be situated 0.5–2.6 mm deep from the surface (Strauss et al., 1994). Both of these nuclei lend themselves to direct electrical stimulation and can be readily obtained at relatively low stimulation intensities.

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the several methods described. Strauss et al. (1993) used both monopolar and bipolar as well as constant current and constant voltage stimulation. Stimulation intensities varied between 0.1 and 2 mA and 0.1 and 1 V. Stimulation duration was between 50 and 400 ms. Single rectangular stimuli with levels up to 10 Hz were used. When using monopolar stimulation, a handheld probe which was insulated, except at the tip, served as the cathode and a needle electrode placed in a wound muscle acted as the anode stimulus. Pulse duration was 100 ms for constant voltage stimulation. Rusyniak et al. (1992) reported using monopolar, constant current stimulation with an intensity of 0.1 mA. They applied the stimulation for 1.0 s. They estimated that when using these stimulation parameters, the current spread from a monopolar electrode was 0.5 mm. In a separate article, Katsuta et al. (1993) reported electrical stimulation of the facial colliculus using bipolar silver-ball electrodes. Square wave pulses of 0.2 ms and an intensity of 1 mA, with a frequency of 1 Hz were applied. A combination of mapping and continuous monitoring was employed by Eisner et al. (1995). They used stimulation forceps (GK 675, Aeskulap, Germany) to apply constant current, square wave impulses at 0.1–3 mA with a repetition rate of 4.7 Hz. Morota et al. (1995) reported using monopolar stimulation and applying 1–2 s trains of stimuli of 0.2 ms duration delivered at 4 Hz. Distinct and stable muscle responses were obtained at stimulation intensities of 1.5–2.0 mA. The intensity was then reduced and the threshold level that was established (0.3–2.0 mA) was used for mapping. In 1999, Chang et al. reported using stimulation intensities as high as 10.2 mA with stimulus duration varying from 0.02 to 0.05 ms in patients undergoing resection of pontine cavernous malformations. Stimulation was increased at 0.1 mA increments, after starting at 0, until a threshold response was identified. Stimulation was then increased until a maximum compound motor action potential (CMAP) or spread to other nuclei was seen. No adverse outcomes were reported from the higher stimulus intensities. However, it should be noted that the higher stimulus intensities (above 4 mA) reported by the authors were applied to tissue felt to be necrotic or to areas adjacent to the original hemorrhage and not to normal appearing tissue.

23.5. Stimulation techniques 23.6. Electromyographic recordings There are several different stimulation parameters, using both bipolar and monopolar techniques, reported in the literature. The following will be a summary of

The goal of brainstem stimulation is to activate motor nuclei and/or pathways. Thus, recordings need to be

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obtained from muscles corresponding to the motor CNN and tracts. Because of the complex structures of the rhomboid fossa, different sets of muscle recordings have been reported by the different groups. However, all groups reported electromyography (EMG) recordings from at least two facial nerve innervated muscles. The following is a summary of the recording techniques reported. Rusyniak et al. (1992) reported “EMG responses from electrodes placed in the face and tongue.” It also appears that they visually inspected the face for movement, since they state that “gross motor responses were noted.” Katsuta et al. (1993) report recording evoked myographic responses from surface electrodes placed on ipsilateral orbicularis oculi and oris muscles. The EMG signal was amplified with a bandpass filter of 10–3,000 Hz. No averaging was required to obtain the EMG response (Figs. 1 and 2). A higher number of muscles were used for recordings by Strauss et al. (1993). Monopolar stainless steel needles were used. For facial nerve recordings, the active electrodes were placed in the orbicularis oris and oculi muscles, and an indifferent electrode was placed at the frontal midline. The genioglossus muscle was the site for the active electrode for hypoglossal recordings. Eisner et al. (1995) used custom-made, noninsulated, steel-needle recording electrodes. Active and reference electrodes were placed in muscles corresponding to the CNNs being monitored and consisted of the following: superior rectus, medial rectus, superior oblique, masseter, orbicularis oculi, orbicularis oris, trapezius, velum palatinum, and lingual muscle. In addition to recording-triggered EMG responses, they also monitored continuous EMG activity using auditory feedback

Fig. 1. Placement of orbicularis oris needle recording electrodes.

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Fig. 2. Needle electrodes placed in the orbicularis oculi muscle, prior to being taped onto the skin.

to the surgeon via a loudspeaker. Recording parameters are outlined in Table 1. Morota et al. (1995) used custom-made, 30-gauge, stainless steel, Teflon-coated wires with a 2-mm bare hook tip, encased in a 27-gauge needle as their recording electrodes. After inserting the needle into the muscle, the needle was then withdrawn leaving the tip of the electrode wire in the muscle. Recordings were obtained from obricularis oris and oculi to record facial nerve responses, posterior pharyngeal wall for cranial nerves (CNs) IX and X activity, and lateral tongue to monitor hypoglossal nerve responses. Four EMG responses were recorded using epoch lengths of 20 ms, amplified 10,000 times, filtered between 50 and 2,133 Hz and averaged. Intramuscular hook-wire electrodes were also used by Chang et al. (1999). These were and still are commercially available (Xomed Surgical Products, Jacksonville, FL). Recordings were obtained from the masseter, orbicularis oculi, and orbicularis oris muscles. The active and reference electrodes were placed in the same muscle and spaced a few millimeters apart. In addition to recording electronically triggered compound action potentials, continuous monitoring of neurotonic discharges from the muscles monitored was also performed. Tables 1 and 2 summarize the different stimulation and recording parameters reported in numerous studies. The differences in the techniques highlight that there is no single method which is clearly superior. Adequate and reliable recordings can be obtained using monopolar, bipolar, constant current, or constant voltage stimulation. Furthermore, stimulation can be either nonrecurrent with only single stimuli, or recurrent with frequencies reported as high as 10 Hz.

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Table 1 Recording parameters Setting

Continuous EMG

Time base Amplitude gain (mV/unit) High filter (Hz) Low filter (Hz)

1000 msa 20 1500 100

Triggered EMG 200 ms per divisionb 50–100 2000 100

20 msa 20–100 1500 100

3–5 ms per divisionb 50–200 1500 100

a

Eisner et al., 1995. Chang et al., 1999.

b

23.7. Stimulation parameters and safety Experimental studies on the effects of electrical stimulation on the brain indicate that certain variables are important in determining neural damage (Agnew and McCreery, 1987; McCreery et al., 1990; Harnack et al., 2004). Current density (I/A ¼ amperes/cm2), charge per phase (Q/phase ¼ I  PD ¼ C/phase), and charge density per phase (QD/phase ¼ J  PD ¼ C/cm2  phase), where I ¼ stimulus pulse amplitude (ampere); PD ¼ stimulus pulse duration (sec); C ¼ coulombs; and A ¼ surface area of the electrode (cm2), are important stimulus parameters related to neural damage (Agnew and McCreery, 1987). Agnew and McCreery (1987) reported that neural damage occurred in tissue immediately subjacent to the subdural stimulating electrodes when the charge density at the surface of the electrodes exceeded 40 mC/cm2  phase and the charge per phase was greater than 0.4 mC per phase at a pulse frequency of 50 Hz. They also found that charge density, rather than charge per phase, correlated more closely with the severity of neural damage when using small electrodes. Possible mechanisms of neural damage include charge transfer across an electrode–tissue interface such as

electrochemically produced toxic products or passage of current through tissue causing neuronal hyperactivity or through power dissipation possibly leading to thermal injury (Agnew and McCreery, 1987). In the study by Chang et al. (1999), they subsequently reported using an average stimulation intensity of 3.4 mA and a pulse duration of 0.02 ms. Based on these stimulation parameters and the surface area of the stimulating electrode, they calculated the charge per phase to be 0.068 mC per phase and the charge density per phase to be 17.4 mC/cm2  phase (Chang et al., 2000). Strauss et al. (1999) reported a charge density of 0.59 mC/cm2  phase using constant voltage stimulation and charge densities up to 0.0014 mC/cm2  phase when using constant current stimulation. The stimulus parameters reported by both groups are well below the safety limits. Clinically, patients seem to tolerate this type of electrical stimulation well. There have been only a few reports of ventricular arrhythmia in patients with a known history of cardiac arrhythmia (Strauss et al., 1999). Possible cardiovascular side effects need to be monitored during brainstem stimulation since the parasympathetic dorsal motor nucleus of the vagus is lateral to the hypoglossal trigone

Table 2 Stimulation parameters Stimulation

Intensity

Stimulation duration

Frequency

Rusyniak et al., 1992 Strauss et al., 1993 Strauss et al., 1993 Katsuta et al., 1993 Eisner et al., 1995 Morota et al., 1995 Chang et al., 1999

Monopolar Both Both Bipolar

1.0 s 50–400 ms 100 ms 0.2 ms 0.2 ms 0.02–0.05 ms

10 Hz 10 Hz 1.0 Hz 1.0 Hz 4.7 Hz 1–2 s trains at 4 Hz 1.1 Hz

Morota and Deletis, 2006

Monopolar

0.1 mA 0.1–2 mA 0.1–1 V 1 mA 0.1–3 mA 1.5–2.0 mA 0.1–10.2 mA (average ¼ 3.4 mA) 2.0 mA for screening

0.2 ms

1–4 Hz

Monopolar Monopolar

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(Strauss et al., 1999). At our institution, no patient has experienced side effects as a result of brainstem stimulation. During the stimulation protocol, we carefully monitor a patient’s blood pressure and heart rate and to date have not encountered any alterations in these parameters. 23.8. Structures stimulated The fact that triggered EMG responses can be obtained with relatively low-level stimulation intensities, as low as 0.1 mA and stimulus duration of 20–50 ms (Chang et al., 1999), has been suggested to indicate that the peripheral motor neuron is the site of stimulation (Strauss et al., 1999). In their review of the literature, Shannon et al. (1997) reported that the time constant for stimulating myelinated central nervous system axons ranges from 50 to 100 ms, 200 to 300 ms for large cortical neurons, and 1 to 10 ms for other neurons and their dendrites. Based on the calculated estimates required to activate neural structures within the brainstem and comparing those with motor threshold measured stimulation intensities, Strauss et al. (1999) determined that the axons of the peripheral motor neurons are the site of intraoperative electrical stimulation. 23.9. Anesthetic considerations Different anesthetic protocols can be successfully used during these procedures, but the most important aspect is that muscle relaxants are not used and that the patient not be under the influence of neuromuscular blocking agents during the time that EMG monitoring is to take place. These drugs are also likely to have adverse effects on MEPs, which are frequently used as part of a multimodality approach for monitoring these cases. The typical anesthetic protocol at our institution is induction with a short-acting barbiturate, an intravenous narcotic agent, and a short-acting neuromuscular blocking agent. Thereafter, anesthesia is usually maintained with a combination of isoflurane, with a maximum end-tidal not exceeding 0.6%, and a maximum of 50% nitrous oxide. Very short-acting intravenous narcotics, such as remifentanyl, are used after induction to supplement the inhaled agents. 23.10. Typical protocol at our institution IOM techniques used, in addition to brainstem mapping, include SEPs after bilateral median and

Table 3 Motor cranial nerves and their corresponding muscles suitable for EMG monitoring Cranial Nerve

Muscles

III IV V VI VII

Inferior rectus Superior oblique Masseter Lateral rectus Frontalis, orbicularis oris, orbicularis oris, mentalis Posterior pharyngeal muscles Crycothyroid or vocalis Sternocleidomastoid Tongue or genioglossus

IX X XI XII

posterior nerve stimulation, bilateral BAEPs, and transcranial electrical motor evoked potentials (TcMEPs) with muscle recordings obtained from all four limbs. These techniques will allow monitoring of the intrinsic brainstem auditory pathways as well as the somatosensory and motor tracts passing through the brainstem. For mapping and monitoring of cranial motor nerve nuclei, we use the technique similar to the one described by Chang et al. (1999). Needle or “hookwire” electrode pairs are placed in the muscles corresponding to the CNN at risk for injury (Table 3). At a minimum, we will monitor bilateral masseter (CN V), orbicularis oculi and oris (CN VII), and trapezius (CN XI) (Fig. 3). The trapezius is used mainly as a control muscle and is useful in

Fig. 3. Needle recording electrodes placed into the orbicularis oris and masseter muscles. The needle electrodes were later taped onto the skin in a similar fashion as the ones in the orbicularis oris.

BRAINSTEM AND AUDITORY EVOKED POTENTIALS

1

3 ms 50 µV

2

3 ms 50 µV

3

3 ms 100 µV

4

3 ms 50 µV

5

3 ms 50 µV

6

3 ms 50 µV

Fig. 4. Stimulation of CN XI (1.1 mA and 0.05 ms duration) as a test of the stimulation and recording system prior to brainstem stimulation. Traces 1–6 are EMG recordings from the following muscles: left masseter, left orbicularis oris, left trapezius, right masseter, and right orbicularis oris, respectively. Trace 6 is recorded from the right posterior pharynx (for CN IX/X activity).

differentiating neurotonic discharges from electrical noise. In addition, if the glossopharyngeal nerve is exposed, it can be used to test the stimulation set-up before the actual stimulation of the brainstem. This will ensure that the stimulation and recording capabilities of the equipment and the electrodes are functioning properly (Fig. 4). With regard to monitoring of CNs III, IV, VI, IX, and X, it is my opinion that placement of extraocular muscle and posterior pharyngeal electrodes should be performed by physicians experienced in the insertion of electrodes into these sites. Baseline EMG recordings from appropriate muscles are made prior to the start of surgery, and continuous monitoring is performed until surgical closure. At intervals during the surgery, when desired by the operating surgeon, a small sterile monopolar electrode probe (Xomed Surgical Products) is placed on the brainstem in areas suspected to correspond to nondiseased CNN, and a small electrical stimulus is applied. Stimulation intensity begins at 0, and is increased at 0.1-mA increments until a threshold response is identified. Then, the stimulation is increased until a maximum CMAP is seen or EMG activity from another motor nucleus is triggered. We will then use this maximal stimulation level to search for excitable tissue in the surgical target area. By observing the stimulus intensities required for a threshold response or a maximum CMAP, the approximate locations of the CNN are determined. Over the years, the stimulus intensities we have used range from 0.1

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to 10.2 mA, with the stimulus duration varying from 0.02 to 0.1 ms. However, triggered EMG responses are usually obtained with stimulus intensities below 3 mA and a stimulus duration of 0.02–0.1 ms. The stimulation is presented as a single pulse with a rate of 1.1 Hz. Such a slow stimulation frequency rate reduces the overall number of stimuli to the brainstem, but in order to acquire responses this technique requires that the surgeon has the patience to hold the stimulating electrode at each site of interest for a few seconds. If the surgeon prefers to search for excitable areas by quickly moving the probe across the brainstem, then the stimulation frequency should be increased. We have found that stimulation frequencies of 6.1 and 7.1 Hz work well in those situations. 23.11. Monopolar versus bipolar stimulation Although we have no experience using bipolar stimulation at the brainstem, the literature suggests that either technique, monopolar or bipolar, is useful and provides adequate stimulation to activate the motor nuclei and tracts. However, in one study bipolar electrodes were reported to be difficult to use for mapping and that a monopolar handheld probe defined the stimulation area more easily (Strauss et al., 1993). 23.12. Constant current versus constant voltage stimulation There appears to be no significant differences in the ability to easily and reliably obtain triggered EMG responses when using either of these two techniques. Strauss et al. (1993) reported that in cases using constant current, shunting effects were noted as a result of the presence of cerebrospinal fluid but that a preliminary review of their data revealed no differences between these two stimulation techniques. In our experience, we have also found no appreciable differences between the two. 23.13. Special technical considerations Simultaneous IOM of somatosensory, brainstem, and motor evoked potentials should be performed in conjunction with continuous EMG monitoring. This may present some difficulty if one is using older IOM equipment, because of the limited number of channels. However, newer equipment typically has a sufficient number of electrode inputs and channels to be

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Fig. 5. A: Monopolar stimulation on the floor of the fourth ventricle in a 46-year-old male with history of multiple episodes of vertigo with new onset right facial numbness and right VI nerve paresis but no facial weakness. Stimulation at site in B: localized the right facial nerve motor fibers immediately superficial to the site of the cavernous malformation. Resection was not performed.

able to monitor the evoked potentials mentioned as well as multiple, bilateral CNs. With regard to the stimulating electrodes, there are several commercially available monopolar electrodes that function equally well. However, the one which our surgeons prefer to use is a monopolar stimulating probe with a ball end, attached by a small flexible wire to the handle (Medtronic Xomed Surgical Products; SKU 82–25251) (Fig. 5A and B). Prior to stimulating any neural structures, the stimulation system should be tested to see if electrical current is being delivered.

A simple and easy method to do this is by stimulating a muscle adjacent to the surgical site. The surgeon should be able to visually confirm the presence of muscle contraction in relation to the stimulation. It is important to remember that to reduce current spread and not activate other more distant brainstem regions, the surgeon should take special care to keep the area to be stimulated clear of blood and fluids. The types of recording electrodes that can be used include surface disk or disposable electrodes commonly used for diagnostic nerve conduction studies,

Fig. 6. A: Placement of a pair of hookwire electrodes into the right genioglossus muscle. B: Note two small wire electrodes which are still in the needle which is used to introduce the wires into the muscle. The wire electrodes taped above were placed in the right posterior pharyngeal wall.

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357

conventional subdermal needle electrodes, or intramuscular wire (also referred to as “hookwire”) electrodes. We have found that the needle and hookwire electrodes seem to provide the best responses without decay in the signal characteristics over lengthy surgical cases. In addition, when properly secured, these electrodes will easily stay in place. The biggest technical problem we have encountered is that the electrodes may inadvertently be pulled out during the positioning of the patient. For this reason, we usually wait until the patient is fully positioned and placed in the headholder device prior to placing the electrodes into the masseter, orbicularis oculi, orbicularis oris, trapezius, and genioglossus muscles (Fig. 6A and B). Unfortunately, this cannot be done for electrodes inserted into the posterior pharyngeal wall, which require placement with the aid of a laryngoscope. We usually place these electrodes with the assistance of the anesthesiologist who will hold the patient’s mouth open, move the tongue to the side, and provide a light source with the laryngoscope. 23.14. Interpretation of the electrophysiologic data Obviously, one cannot obtain preoperative or preincision data regarding the characteristic responses from brainstem stimulation. Thus, each patient must serve as his own control. If the brainstem lesion lies primarily on one side, one should stimulate the opposite side and record the triggered EMG response. This will provide an estimate of the stimulus intensity needed to obtain the EMG signal, as well as, some of the characteristics of the recorded potential, such

Fig. 7. Magnetic resonance imaging (MRI) showing the location and extent of the cavernous malformation and the associated hemorrhage.

4 ms Trig 50 µV Amp 1

1 N2

1

4 ms Trig Amp 1 50 µV

2

2

4 ms Trig Amp 2 50 µV

3

3

4 ms Trig Amp 3 100 µV

4

4

4 ms Trig 50 µV Amp 4

5

A

4 ms Trig 50 µV Amp 2 4 ms Trig 200 µV Amp 3

R

4 ms Trig 50 µV Amp 4 P1

Off

B

Fig. 8. A: Preresection monopolar brainstem stimulation at 0.2 mA, 0.05 ms duration, and 1.1 Hz using single stimuli. Traces 1–4 correspond to triggered EMG recordings from the following muscles: left masseter, left orbicularis oris, right masseter, and right orbicularis oris, respectively. B: Postresection monopolar brainstem stimulation, using the same stimulation parameters and the same muscles for EMG recordings.

I

IV

III

II

. r c

III IV I

N1

V

1 II N1

N1 P1

2 N1 P1

P1

3

N1

N1 I r c

P1 V III

I

IV

III

I

IV

II

P1

4

V

P1 1

V

III

I 5 II

II

N1

2

N1

6

I 3 N1

V

III II

N1

P1 N1

IV

N1

4

N1 P1

P1

P1

8 5

A

P1

7

B

P1

P1

C

Fig. 9. A: Baseline brainstem auditory evoked potentials (BAEPs) after left and right ear stimulation (traces 1 and 5, respectively); cortical somatosensory evoked potentials (SEPs) after left (traces 2 and 3) and right (traces 6 and 7) median nerve stimulation. Traces 4 and 8 were recorded from the C7 cervical spinal level. B: During resection, note loss of left median nerve SEP (trace 2) without changes in left BAEP (trace 1), right BAEP (trace 3), or right median nerve SEP cortical recording (trace 4). C: After resection, note recovery of left median nerve cortical SEP (traces 2 and 3).

BRAINSTEM AND AUDITORY EVOKED POTENTIALS

N1

P1 N1

359

N2

N2 1

N2

2

P1 N2

P2 N2

N1

P1

P2

P2 P1 P2

P1

P2

3

P2 N2 P1

N1 P1

N2

4

N2

5

N2

N1 P1

P2 P1

N1 P1

N2

P2

N2

P1 N1

P2

6

P1 P2

P2

7 N2 P1

P2 8

A

B

Fig. 10. A: Baseline somatosensory evoked potentials (SEPs) after lower extremity stimulation. Traces 1–3: cortical SEPs after left posterior tibial nerve stimulation; traces 5–7: cortical SEPs after right posterior nerve stimulation. B: Note smaller cortical SEP amplitudes after leg stimulation, which is most pronounced after left leg stimulation (traces 5–7).

as latency and amplitude. Mapping should be done prior to initiating the resection. Once an EMG response is obtained, the stimulus intensity should be adjusted in order to obtain a threshold and a maximal response. Latencies and amplitudes should be recorded for both levels. Although it is unclear what constitutes a significant or critical change in the triggered EMG potentials occurring during or following resection, one study reported a patient developed a transient VI and VII CN palsy after postresection stimulation revealed an 80% amplitude reduction in the EMG response when compared to the preresection baseline (Chang et al., 1999). In our experience, we have found that patients do not develop new CN

deficits if the postresection triggered EMG responses remain unaltered from baseline. However, if the CMAP amplitudes are smaller or if higher stimulus intensities are required in order to obtain the CMAP after postresection stimulation, these patients have a higher probability of developing a new CN deficit, or a worsening of a preexisting CN deficits. In addition, in these patients, it cannot be ascertained whether the deficit will be transient or permanent. However, in our experience, in those patients where the CMAP cannot be registered after resection, the probability of a new and permanent deficit is the highest. We have not appreciated any significant changes in latencies, other than those secondary to temperature. This is

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c 1

2

3

4

5

6

20 ms 100 µV

20 ms 100 µV

20 ms 100 µV

20 ms 100 µV

20 ms 200 µV

20 ms 200 µV

7

8

Fig. 11. Transcranial electrical motor evoked potentials (TcMEPs): traces 1–3: EMG recordings from left first dorsal interosseus, left tibialis anterior, and left abductor hallucis muscles, respectively. Traces 4–7 show EMG recordings obtained from the same muscles on the right. Note lack of left arm and leg muscle activity after stimulation. Baseline TcMEPs originally showed symmetrical responses bilaterally.

activity of short duration which coincided with the start and end of a surgical manipulation and was similar to the EMG bursts typically seen during facial nerve monitoring. They also described “pathological spontaneous activity” (PSA) and classified it as “slight PSA” if it lasted for a few seconds or “extreme PSA” if it persisted for several hours after the surgical manipulation had been terminated. As a result of these findings, the surgeon’s dissection strategy was guided and modified based on the amount of audible EMG produced by surgical manipulation. One of their patients developed transient, followed by gradually permanent EMG discharges in the lingual muscles. This patient suffered from severe bilateral and permanent tongue weakness. In the remaining 15 patients, the surgeons modified their dissection strategy by reducing pressure or traction on tissue, or by changing the direction and location of dissection based on the occurrence of EMG discharges. They felt that this resulted in EMG activity of shorter duration and lower amplitude, and in these patients new postoperative deficits were mild, transient, or absent. 23.15. Summary The literature and electrophysiologic techniques reviewed indicate that brainstem electrical stimulation for localization of motor CNN is safe and reliable. Brainstem stimulation is currently the only technique available which can identify CN motor pathways in the operative field and can guide the neurosurgeon in where to place the incision on the brainstem. Although there are no outcome studies using these techniques, it is generally considered advantageous to utilize brainstem stimulation in these procedures, especially since the floor of the fourth ventricle is often distorted. Many neurosurgeons and neurophysiologists consider its use to be indispensable. 23.16. Clinical examples

important to keep in mind, especially if the surgery is done under hypothermia. The literature also does not provide clear criteria on how to interpret neurotonic discharges. In our practice, we use a strategy similar to that described by Eisner et al. (1995). In addition to the triggered EMG brainstem mapping, they used a standard audible and video-displayed EMG to monitor neurotonic discharges. They defined “contact activity” as EMG

23.16.1. Case 1 This case follows a 40-year-old male with history of migraine headaches diagnosed with a pontine cavernous malformation after an MRI was obtained (Fig. 7). He was followed over a period of two years and was taken to surgery after he suffered two hemorrhages, which resulted in mild right face and left body numbness, mild right facial weakness, and diplopia. IOM using multimodality recordings of

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arm and leg (Fig. 11). After reducing traction and altering slightly the direction of the dissection, there was a gradual improvement in the SEPs and their amplitudes returned to near baseline levels. By the end of the case, the TcMEPs from the left side remained absent. No significant neurotonic discharges were seen during the case and the stimulation parameters and evoked EMG responses remained unchanged from baseline (Fig. 8B). Postoperatively, the patient awakened with a left hemiplegia but no new or worsened CN abnormalities. His weakness quickly began to improve and by one week he displayed only mild left leg weakness. Four months after surgery, he was neurologically normal.

bilateral median and posterior nerve SEPs, bilateral BAEPs, TcMEPs, continuous EMG monitoring of bilateral CNs V and VII, and brainstem mapping of CN motor nuclei was performed. Prior to resection, brainstem stimulation was performed which identified the brainstem trigeminal motor pathways via triggered EMG responses from the right masseter muscle (Fig. 8A). During the resection, there was a loss of the cortical SEP after left median nerve stimulation and a reduction in the amplitudes of the cortical SEPs after posterior tibial nerve stimulation, but most prominent after left leg stimulation (Figs. 9 and 10). In addition, there was

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Fig. 12. EMG recordings after brainstem stimulation. Traces 1–5 correspond to the following muscles: left lateral rectus, left orbicularis oris, right masseter, right lateral rectus, and right orbicularis oris, respectively. A: Preresection monopolar brainstem stimulation at 0.3 mA, 0.05 ms duration, and 5.1 Hz using single stimuli. Compound motor action potential (CMAP) recorded from the right masseter. B: Increasing the stimulation intensity to 0.7 mA while maintaining the other stimulation parameters unchanged reveals triggered responses from the right masseter and right orbicularis oris. C: Slight movement of the monopolar probe along the brainstem surface and away from the area of hemorrhage triggers a large CMAP from the right masseter and smaller responses from the right lateral rectus and the right orbicularis oris. Stimulation parameters were the same as those used in (B). D: Using the same stimulation parameters as in (B) and (C) and stimulating inferiorly to the site at (C), reveal a small but isolated CMAP from the right orbicularis oris.

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23.16.2. Case 2 A 15-year-old female was admitted after experiencing a 2.6  2.9 cm pontine hemorrhage secondary to a brainstem tumor. Initial physical examination revealed multiple cranial neuropathies, including abnormal extraocular movements, asymmetric pupils, and absent gag and cough. She was also quadreparetic and her muscle stretch reflexes were hyperactive. IOM using multimodality recordings of bilateral median and posterior nerve SEPs, bilateral BAEPs, TcMEPs, continuous EMG monitoring of bilateral CNs VI and VII, and right V, as well as, brainstem mapping of these CN motor nuclei was performed (Fig. 12). These stimulation examples demonstrate that important CN motor pathways can be localized even in patients with significant CN palsies. There were no significant intraoperative changes in the sensory or motor evoked potentials. Postoperatively, the patient exhibited no new neurological deficits. References Agnew, WF and McCreery, DB (1987) Considerations for safety in the use of extracranial stimulation for motor evoked potentials. Neurosurgery, 20: 143–147. Baker, GS (1965) Physiologic abnormalities encountered after removal of brain tumors from the floor of the fourth ventricle. J. Neurosurg., 23: 338–343. Chang, SD, Lo´pez, JR and Steinberg, GK (1999) Intraoperative electrical stimulation for identification of cranial nerve nuclei. Muscle Nerve, 22: 1538–1543. Chang, SD, Lo´pez, JR and Steinberg, GK (2000) Reply: identification of cranial nerve nuclei. Muscle Nerve, 23: 1446. Eisner, W, Schmid, UD, Reulen, HJ, Oeckler, R, OlteanuNerbe, V, Gall, C and Kothbauer, K (1995) The mapping and continuous monitoring of the intrinsic motor nuclei during brainstem surgery. Neurosurgery, 37: 255–265. Fahlbusch, R and Strauss, C (1991) Surgical significance of cavernous hemangioma of the brainstem. Zentralbl. Neurochir., 52(1): 25–32. Harnack, D, Winter, C, Meissne, W, Reum, T, Kupsch, A and Morenstern, R (2004) The effects of electrode material, charge density and stimulation duration on the safety of high-frequency stimulation of the subthalamic nucleus in rats. J. Neurosci. Methods, 138: 207–216. Heffez, DS, Zinreich, J and Long, DM (1990) Surgical resection of intrinsic brainstem lesions: an overview. Neurosurgery, 27: 789–798.

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