BAEPs in surgery

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 22

BAEPs in surgery Alan D. Legatt* Departments of Neurology and Neuroscience, Montefiore Medical Center, and the Albert Einstein College of Medicine, Bronx, NY 10467, USA

22.1. Introduction Following the delivery of a brief acoustic stimulus, such as a click or tone pip, a series of electrical signals with latencies as long as hundreds of milliseconds can be recorded from human subjects. The earliest signals, which originate from the cochlea, constitute the electrocochleogram (ECochG). The ECochG was originally recorded from needle electrodes inserted through the tympanic membrane to a location in the middle ear, in close proximity to the cochlea (Ruben et al., 1961). It can also be recorded from extratympanic recording sites, such as the external ear canal, but at substantially smaller amplitude; signal averaging is used to record these volumeconducted signals with an adequate signal-to-noise ratio. The longer-latency signals, called auditory evoked potentials (AEPs), are most often recorded from the skin surface. They can be further divided into short-latency AEPs, with latencies of under 10 ms; long-latency AEPs, with latencies over 50 ms; and middle-latency AEPs, with latencies of 10–50 ms. The long-latency AEPs, which are predominantly generated within the cerebral cortex, including cortical association areas, are profoundly changed by whether the subject is attending to the acoustic stimuli and extracting information from them, for example, by performing discrimination tasks based on stimulus characteristics or recognizing that novel stimuli have been presented (Linden, 2005). The long-latency AEPs are suppressed by surgical anesthesia, and are not useful for intraoperative monitoring. The middle-latency AEPs are most likely generated within the cerebral cortex, including primary *

Correspondence to: Alan D. Legatt, M.D., Ph.D., Department of Neurology, Montefiore Medical Center, 111 East 210th Street, Bronx, NY 10467, USA. Tel.: þ1-718-920-6530; fax: þ1-718-920-8509. E-mail: [email protected] (A.D. Legatt).

auditory cortex and surrounding areas (Yvert et al., 2001). They are also markedly affected by surgical anesthesia, so much so that anesthetic-related variability impedes their use in continuous intraoperative monitoring for focal neurologic dysfunction. However, this anesthetic sensitivity has led to application of the middle-latency AEPs as an indicator of the depth of anesthesia (Schneider et al., 2005). The short-latency AEPs, most often called “brainstem auditory evoked potentials” (BAEPs) (Fig. 1), are the AEPs most often used for clinical diagnostic purposes because they are relatively easy to record and their waveforms and latencies are highly consistent across normal subjects. They are almost identical in the waking and sleeping states (Campbell et al., 1992). Sedation (Loughnan et al., 1987) and surgical anesthesia (Stockard et al., 1992; Legatt, 2002; Banoub et al., 2003) produce only minor changes in the BAEPs (Fig. 2). Some of the intraoperative BAEP changes are attributable to changes in body temperature rather than anesthetic effects (Markand et al., 1987; Litscher, 1995; Rodriguez et al., 1999). Because of their resistance to anesthetic agents, BAEPs can be used for intraoperative monitoring of the ears and the infratentorial auditory pathways. The ECochG can also be used for intraoperative monitoring. However, since the ECochG is generated in the inner ear, it may not detect dysfunction within the more proximal portion of the auditory pathway, that is, the eighth nerve or the brainstem auditory pathways. Extraoperative diagnostic BAEP tests are evaluated by comparing the BAEPs to those of a control normal population. In order for this comparison to be valid, the techniques used and the state of the subjects in the patient’s study and the control studies must be identical. This is difficult to ensure during intraoperative monitoring, where the anesthetic regimen, the body temperature, the delivered stimulus intensity, and other factors may differ from patient to patient. Therefore, during intraoperative BAEP monitoring,

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I

III

[ISOFLURANE]A = 2.0% BP 94/55 TNP = 35.9 ⬚C

IV

II

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V

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FP1-C3

VII Cz-Ai

C3-O1 IN

VN Cz-Ac

FP2-C4

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0.2 µV 1 ms

Ac-Ai

Fig. 1. Brainstem auditory evoked potentials (BAEPs) recorded simultaneously from three different recording electrode linkages following monaural stimulation in a normal subject. The vertical dashed lines indicate the peak latencies of waves IV and V in the Cz-Ai waveforms; these peaks are more widely separated in the Cz-Ac waveforms. (Reprinted from Legatt, 2005, with permission from Elsevier.)

T3-CZ

CZ-T4

EMG/ECG 15 µv 1s II III IV V

I

each patient serves as his/her own control; BAEPs recorded at a time when elements of the auditory pathways are at risk are compared to those recorded earlier during the same operation (Legatt, 1991). 22.2. Components and sources

BAER

CZ + 0.25 µV

60 dBHL click

2

4

6

8

10

12

ms

22.2.1. The ECochG The ECochG includes the cochlear microphonic and the eighth nerve action potential. The cochlear microphonic is generated in the receptor cells — the hair cells — within the cochlea. It is so named because its waveshape approximates the sound pressure waveform of the acoustic stimulus. Therefore, if the waveshape of the acoustic stimulus is reversed in polarity, the cochlear microphonic is also inverted. The eighth nerve compound action potential is generated by depolarization within the distal (cochlear) ends of the auditory nerve axons, which have been activated by excitatory synaptic input from the cochlear hair cells. It is recorded as a phasic negativity in the middle ear or extratympanic recording site irrespective of the stimulus polarity. Sounds in the intensity range typically used for BAEP recordings typically elicit more than one volley within the auditory nerve, producing the N1 and N2 components of the eighth nerve compound action potential, and sometimes an N3 as well.

VI

Fig. 2. Brainstem auditory evoked potentials (BAEPs) recorded during surgery in a patient anesthetized with isoflurane at a concentration sufficient to render the electroencephalogram isoelectric. The component amplitudes were reduced somewhat, but the latencies of waves I through V were not significantly different from those recorded in this patient in the unanesthetized state. (Reprinted from Stockard et al., 1992, with permission from Elsevier.)

22.2.2. BAEPs BAEPs are most often recorded between electrodes on the surface of the head, including an electrode at the vertex (position “Cz” of the International 10– 20 system) and electrodes at both earlobes (labeled “Ai” ipsilateral to the stimulated ear and “Ac” contralateral to it) or at both mastoids (labeled “Mi” and “Mc”). Recordings should include, at the minimum, a vertex-to-ipsilateral-ear (Cz-Ai) recording channel. The vertex-positive peaks in this channel are typically labeled with Roman numerals according

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to the convention of Jewett and Williston (1971). Other channels, such as Cz-Ac, may help in the identification of components (Legatt, 2005) (Fig. 1). Most of the BAEP components are recorded from the skin surface as far-field potentials, which mean that small displacements of the recording electrodes do not significantly alter the BAEP waveform. The exceptions to this are wave I and part of wave II, which are generated in the distal auditory nerve (see below) and are therefore recorded as near-field potentials in the vicinity of the stimulated ear. Changes in the location of the Ai/Mi recording electrode can substantially alter these components, and can therefore be used in an attempt to improve their recording during intraoperative BAEP monitoring. Wave I of the BAEP arises from the first volley of action potentials in the auditory nerve in the most distal portion of the nerve (Legatt et al., 1988). It represents the same electrical phenomenon as the N1 component of the eighth nerve compound action potential in the ECochG, as confirmed by simultaneous BAEP and ECochG recordings (Gersdorff, 1982). This produces a skin-surface negativity in a circumscribed area around the stimulated ear (Hughes and Fino, 1985; Grandori, 1986); the negativity at Ai appears as a positive peak in the Cz-Ai recording. Since wave I is a near-field potential around Ai, repositioning of the Ai recording electrode can substantially alter it, and alternate Ai electrode positions can be used to obtain a clearer wave I. Because wave I arises from the most distal portion of the auditory nerve, it may persist after the nerve is sectioned at a more proximal location, such as during surgery for eighth nerve tumors (Raudzens and Shetter, 1982; Legatt et al., 1986) (Fig. 3). Although some investigators have postulated a one-peak-to-one-generator correspondence, research has shown that Jewett and Williston (1971) were correct in their assertion that most of the BAEP components are composites of contributions of multiple generators. The complexity of the generators of human BAEPs (Fig. 4) derives in part from the pattern of connections within the auditory pathways, with ascending fibers both synapsing in and bypassing various relay nuclei (Strominger and Strominger, 1971; Strominger, 1973; Strominger et al., 1977). It also reflects the presence of at least two bursts of activity in the auditory nerve (corresponding to the N1 and N2 components of the eighth nerve compound action potentials in the ECochG), which can drive the more rostral pathways. Because of both of

A.D. LEGATT

0.1 µV 1 ms

Fig. 3. Intraoperative brainstem auditory evoked potentials (BAEPs) to left ear stimulation recorded during surgery for left acoustic neuromas in two different patients, showing persistence of wave I (arrows) after transection of the intracranial eighth nerve. The nerves were intentionally sacrificed to permit total resection of the tumors. (Reprinted from Legatt, 2002, with permission from Lippincott, Williams and Wilkins.)

these factors, several different structures within the infratentorial auditory pathways may be active and generating field potentials simultaneously. Wave II originates, in part, in neural activity that began as the N1 component of the eighth nerve compound action potential and has propagated from the distal auditory nerve to its proximal end and to the cochlear nucleus. However, the activity at this point in the auditory pathway occurs simultaneously with the second auditory nerve volley, the N2 component of the eighth nerve compound action potential, in the distal nerve (Gersdorff, 1982). The latter contributes to the scalp-recorded BAEP in the same manner as the N1 component did when it was at the same location. This can cause persistence of a wave II in cases where the proximal eighth nerve has been destroyed (Legatt, 2005). With regard to the more proximal generator of wave II, the relative contribution of activity in auditory nerve fibers within the proximal nerve and of activity in cochlear nucleus neurons has been a subject of controversy (Legatt et al., 1988). This proximal generator is the major determinant of the scalp topography of this BAEP component over the dorsal part of the head (Hughes and Fino, 1985). Wave III predominantly originates in the caudal pontine tegmentum, including the region of the superior olivary complex, though a contribution from continued activity at the level of the cochlear nucleus cannot be

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AC AC

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MGN

IC L V L IV

IC V L IV L

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BIC

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8th Nerv

e II

S O C

III

II,III?

III

S O C

III IV

IN IIN

VI

VII

SN

Fig. 4. Diagram showing the probable generators of the human brainstem auditory evoked potentials (BAEPs). SN, slow negativity after wave V; AC, auditory cortex; AR, auditory radiations; BIC, brachium of the inferior colliculus; CN, cochlear nucleus; IC, inferior colliculus; LL, lateral lemniscus; MGN, medial geniculate nucleus; SOC, superior olivary complex. (Reprinted from Legatt et al., 1988, with permission from Elsevier.)

ruled out (Legatt, 2005). Ascending projections from the cochlear nucleus are bilateral, so wave III may receive contributions from brainstem auditory structures both ipsilateral and contralateral to the stimulated ear. In patients with asymmetrical lesions of the brainstem, wave III abnormalities are usually most pronounced following stimulation of the ear ipsilateral to the lesion (Brown et al., 1981; Oh et al., 1981; Faught and Oh, 1985), though occasionally they are more pronounced following contralateral stimulation (Stockard and Rossiter, 1977). Waves IV and V are often fused into a IV–V complex, and their anatomical generators are most likely in close anatomical proximity or overlapping, since they are usually either both affected or both unaffected by brainstem lesions (Starr and Hamilton, 1976; Stockard and Rossiter, 1977; Stockard et al., 1977). They may, however, be differentially affected (Stockard and Rossiter, 1977; Legatt et al., 1988; Hirsch et al., 1996) by intraoperative brainstem damage (Fig. 5). Wave IV appears to reflect activity predominantly in ascending auditory fibers within the dorsal

and rostral pons, just caudal to the inferior colliculus, while wave V predominantly reflects activity at the level of the inferior colliculus, perhaps including activity in the rostral portion of the lateral lemniscus as it terminates in the inferior colliculus (Legatt, 2005). As is the case with wave III, wave V abnormalities due to unilateral brainstem lesions are usually most pronounced following stimulation of the ear ipsilateral to the lesion (Brown et al., 1981; Oh et al., 1981; Faught and Oh, 1985; York, 1986; Scaioli et al., 1988), though there are exceptions (Zanette et al., 1990; Fischer et al., 1995). Waves VI and VII are absent in some normal subjects. While they may in part reflect activity in more rostral structures such as the medial geniculate nucleus, they also receive contributions from activity in the inferior colliculus (Legatt, 2005); the latter generator may cause persistence of these waves in patients with auditory pathway damage rostral to the inferior colliculus. Therefore, BAEPs cannot be used to assess or monitor the auditory pathways rostral to the mesencephalon.

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A.D. LEGATT

BAEPs to left ear stimulation

SEPs to left median SEPs to right median nerve stimulation nerve stimulation 18:30, aneurysm in view

19:30, dissecting around aneurysm

19:40, aneurysm ruptured

19:45, clip placed on basilar artery

19:55, clip taken off basilar artery ?

20:20, closing

?

20:40, closing

0.25 µV

2 µV 1 ms

2 µV 8 ms

8 ms

Fig. 5. Intraoperative brainstem auditory evoked potentials (BAEPs) to left ear stimulation and cortical somatosensory evoked potentials (SEPs) to stimulation of both median nerves recorded during surgery for a basilar artery aneurysm. The cortical SEP to left median nerve stimulation disappeared when the aneurysm ruptured, most likely reflecting a loss of perfusion pressure within the brainstem. The cortical SEP to right median nerve was still present at that point, but subsequently disappeared when the basilar artery was clipped in order to control the bleeding. A BAEP run was not obtained between aneurysm rupture and basilar artery clipping, but following the clipping BAEP wave V (arrow) became delayed and attenuated, and eventually disappeared, while BAEP wave IV (triangle) persisted. The patient suffered a brainstem infarct. In the SEP waveforms, cortical negativity is shown as an upward deflection. The first 8 ms of each SEP waveform was cropped off to remove the large stimulus artifacts. (Reprinted from Legatt, 2002, with permission from Lippincott, Williams and Wilkins.)

22.3. Recording techniques 22.3.1. Stimulation BAEPs are most commonly elicited by brief acoustic click stimuli, produced by delivering trains of 100 ms duration electrical square pulses to the acoustic transducer; brief tone pips can also be used. Since the responses to rarefaction and compression clicks may differ (Emerson et al., 1982; Schwartz et al., 1990), extraoperative diagnostic BAEP studies typically employ a single click polarity. Summation of the responses to alternating click polarities are useful to cancel a large stimulus artifact and/or the cochlear

microphonic, and are often employed during intraoperative BAEP monitoring. The same click polarity (single or alternating) should be used throughout the operation. Since headphones are impractical for intraoperative monitoring, the acoustic stimuli are most often delivered using ear inserts, incorporating foam cylinders that can be compressed and then gradually expand to achieve a tight fit with the ear canal. The foam can be covered with a thin layer of metal foil, to serve as a near-field electrode for recording of the ECochG and to record BAEP wave I at higher amplitude. The ear insert can be held in place with

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bone wax or cotton padding, secured with nonporous tape or an adhesive waterproof dressing pad (Little et al., 1983; Legatt, 1991). This is to prevent fluids such as blood, skin prep, or irrigation fluid from entering the ear canal, where they might interfere with transmission of sound to the inner ear. The ear insert is connected to the acoustic transducer via a length of plastic tubing. Care should be taken to ensure that this tubing remains in place during positioning of the patient and is not kinked. The time required for the acoustic signal to propagate through the tubing typically prolongs the latencies of all BAEP components by approximately 0.9–1.0 ms. This causes no problems in the evaluation of the BAEPs, since each patient serves as his own control and the acoustic propagation delay is constant. Moreover, the delay helps to prevent obscuration of wave I by the electrical stimulus artifact, because (1) it prolongs the latency of wave I, helping to separate it in time from the electrical stimulus artifact (which remains simultaneous with the activation of the acoustic transducer), and (2) it permits increasing the distance between the acoustic transducer and the recording electrodes, thus reducing the amplitude of the electrical stimulus artifact. In a clinical diagnostic BAEP recording, the stimulus intensity must be equal to that which was used to obtain the normative data. The stimulus intensity delivered during intraoperative BAEP monitoring may be difficult to control precisely due to variability in the positioning of the ear insert, but this again does not cause a problem since each patient serves as his or her own control. The intensity setting chosen should be loud enough to produce a clear BAEP but not loud enough to cause ear damage. A stimulus rate of 10/s is typical, but a rate of exactly 10 Hz or another submultiple of the power line frequency should be avoided. If a line-frequency or harmonic artifact appears in the averaged BAEPs and examination of the raw data does not show increased line frequency artifact, the stimulus rate should be adjusted slightly, because timing circuits can drift. As is the case with extraoperative diagnostic studies, each ear should be stimulated separately; binaural stimulation should not be employed. Contralateral white noise masking is typically used during extraoperative diagnostic BAEP studies to prevent acoustic crosstalk — air or bone conduction of the acoustic stimulus to the nonstimulated ear. Most current intraoperative monitoring equipment can

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deliver interleaved left- and right-sided stimuli and sort the responses into separate averages, in effect acquiring averaged BAEPs to left-ear and to rightear stimulation simultaneously. This has the advantage of reducing the time during which one of these BAEPs is not being examined. Contralateral noise masking cannot be used when interleaved stimuli are delivered, however. This does not pose a major problem for intraoperative BAEP monitoring, since the major reason for white noise masking is to prevent the appearance of a BAEP when a deaf ear is stimulated during a diagnostic BAEP study; it will not prevent recognition of auditory pathway compromise when a functioning ear is stimulated. Also, the magnitude of acoustic crosstalk is less with earinsert transducers than with headphones (Roeser and Clark, 2000). 22.3.2. Recording Recording electrodes are placed at the vertex (Cz) and at each ear or mastoid. Cup electrodes or needle electrodes can be utilized. Duplicate or “backup” electrodes are useful because it is usually difficult or impossible to replace an electrode that becomes unusable in the middle of an operation, when the patient is positioned and draped. Electrodes and part of the adjacent connecting wires should be attached to the patient securely, to prevent dislodgement. The electrodes should be oriented so the connecting wires are directed away from the surgical field (Legatt, 1991). Modern evoked potential recording systems typically have enough channels to permit recording of both the Cz-Ai and the Cz-Ac waveforms. Wave V is identifiable in both of these recording linkages, and recording both of them provides a measure of redundancy should one of the ear electrodes become unusable. An Ac-Ai recording channel can improve the detection of wave I; although this component is picked up mainly as a near-field negativity at the Ai electrode, the horizontal orientation of its dipole projects a small positivity to the contralateral ear (Legatt, 2005). If the auditory nerve is at risk, such as during resection of an eighth nerve tumor, and the surgical exposure permits it, an electrode can be placed on the proximal eighth nerve to record a near-field compound action potential (Mller and Jannetta, 1983; Legatt, 1991) (Fig. 6). This signal is typically much larger than the far-field BAEP, permitting signal averaging using fewer epochs and thus providing

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A.D. LEGATT

22.4. Intraoperative use of BAEPs and the ECochG 1 µV

8th N–CZ

CZ+ up 0.08 µV M1–CZ

1 2 3 4 5 6 7 8 9 10 ms

Fig. 6. Brainstem auditory evoked potentials (BAEPs) recorded from a platinum pad electrode placed on the intracranial eighth nerve (top) compared to surface-recorded BAEPs (bottom) during surgery in a 52-year-old woman with a left-sided intracanalicular acoustic neuroma. Note the voltage calibrations; the near-field response is considerably larger. The patient had transient BAEP changes during the resection but BAEPs were at baseline at its end, and postoperative hearing was normal. (Courtesy of Dr. Timothy A. Pedley.)

more frequent assessment of the cochlea and of the auditory nerve distal to the near-field electrode. A typical analog filter bandpass for BAEP recording is 100 or 150 Hz to 3,000 Hz (3 dB points). While line-frequency (e.g., 60 Hz) “notch” filters should not be used for somatosensory evoked potential (SEP) recordings because they can cause a “ringing” oscillatory artifact (Yamada, 1988), they can be used for BAEP recordings. The analog gain depends on the input window of the analog-to-digital converter; a value of 100,000 is typical. An averaging epoch duration of 10 ms is often used for extraoperative diagnostic BAEP recordings in adults. A longer epoch duration, typically 15 ms, is preferable during intraoperative BAEP monitoring because component latencies can be prolonged by preexisting pathology, hypothermia, or intraoperative compromise of the auditory system. The choice of the number of sweeps per average will depend on the signal-to-noise ratio of the raw data. A value of 1,000 sweeps per average is typical, but more may be required if the raw data are noisy and the BAEPs are small. Near-field recording from the proximal eighth nerve (Fig. 6) may permit averaging using a much smaller number of sweeps.

22.4.1. Surgical procedures As noted above, BAEPs can be used to monitor acoustically evoked activity within the auditory pathways up through the level of the mesencephalon; they are not useful for monitoring the pathways rostral to this. They are most often used to monitor surgery for eighth nerve tumors such as vestibular schwannomas (formerly called acoustic neuromas) and for tumors or vascular abnormalities within the posterior fossa, both extra-axial and within the substance of the brainstem. BAEP monitoring can help to avoid excessive eighth nerve stretch from cerebellar retraction, which can cause hearing loss, during surgery in the cerebellopontine angle. Intraoperative monitoring of the ECochG has also been used during cerebellopontine angle surgery. It may be a useful adjunct when combined with BAEP monitoring, because it requires less averaging (fewer epochs) than the scalp BAEPs and thus may contribute to more rapid recognition of cochlear dysfunction; also, it may detect cochlear dysfunction that does not cause BAEP changes (Ojemann et al., 1984; Levine et al., 1994; Schlake et al., 2001). However, the ECochG may not detect eighth nerve damage that spares its distal end and the cochlea, and some patients in whom the ECochG is preserved are deaf postoperatively (Symon et al., 1988). Therefore, ECochG monitoring by itself is not sufficient for posterior fossa surgery. 22.4.2. Analysis and interpretation of BAEPs Because BAEP component amplitudes are highly variable across a population of normal human subjects, extraoperative diagnostic BAEP studies are typically evaluated based on latency criteria — examination of absolute component latencies, interpeak intervals (the I–V interpeak interval is often called the “central transmission time”), and the right–left differences of these measures. The sole exception to this is the IV–V:I amplitude ratio, which may demonstrate abnormality in subjects in whom the latencies are normal. The interpretation of these BAEP studies is also based on the most reliable peaks — waves I, III, and V (American Clinical Neurophysiology Society, 2006). In contrast to the large intersubject variation in component amplitudes, amplitudes on repeated testing

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in the same subject are usually quite consistent, if the recording techniques are not altered. Moreover, intraoperative compromise of neural pathways may cause amplitude changes earlier than, or in the absence of, latency changes. Therefore, both the amplitudes and the latencies of the BAEP components are used in the interpretation of intraoperative BAEPs monitoring data. The amplitudes of the vertexpositive peaks of waves I, III, and V are measured with respect to the troughs that follow them. Typical threshold criteria for the identification of an adverse BAEP change are a 50% decrease in the amplitude of a component (most often of wave V), or a 1-ms increase in the absolute latency of wave V or in the I–V interpeak interval. A IV–V complex with a dominant wave IV and a poorly identifiable wave V is a normal variant pattern. If this occurs, the latency and amplitude of wave IV can be followed. The Cz-Ac recording channel may also be useful in obtaining a clearer wave V, since the peaks of waves IV and V are often more separated and better differentiated in this recording channel than in the Cz-Ai recording channel (Legatt, 2005).

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A

B

C

22.5. Causes of intraoperative BAEP changes µV

Intraoperative BAEP changes can be classified into three categories: “true positive” changes, which reflect compromise of the structures that the monitoring is intended to safeguard, changes produced by other physiologic mechanisms such as anesthetic effects or hypothermia, and changes due to technical problems (Legatt, 2002). These categories will be considered separately. 22.5.1. Technical problems As with any evoked potential, signals may be lost due to equipment malfunction, dislodged electrodes, disconnected or broken wires, and operator error (the use of incorrect protocols or settings). Additional technical problems specific to BAEPs include dislodging or kinking of the plastic tubing through which the acoustic stimuli reach the ear and the entry of liquids into the ear canal. Artifacts (Fig. 7) can obscure the BAEPs and prevent their identification and measurement (Legatt, 1995). Automatic artifact rejection and avoidance of a stimulus repetition rate that is a submultiple of the line frequency

1 ms

D Fig. 7. Single, unaveraged data epochs recorded during intraoperative brainstem auditory evoked potential (BAEP) monitoring. A: An electrical stimulus artifact is present at the beginning of the epoch. The BAEP, which is less than 1 mV in amplitude, is not visible in this single epoch of raw data. B: Bipolar cautery produces a large artifact that triggers automatic artifact rejection and also causes clipping during analog-to-digital conversion. C: The cavitational ultrasonic surgical aspirator (CUSA) device produces a very high frequency but low voltage artifact that completely obliterates the neurophysiologic data but does not trigger automatic artifact rejection. D: The light source of the operating microscope produces a repetitive sharply contoured artifact that recurs at a harmonic of the line frequency but is composed of higher frequencies that would not be removed by a line-frequency notch filter. In A–C, the horizontal dotted lines show the input window of the analog-to-digital converter and the threshold for automatic artifact rejection. In D, the amplifier gain was reduced to show the light source artifacts in their entirety. Voltage calibration bar ¼ 10 mV in A–C, and 40 mV in D. (Reprinted from Legatt, 2002, with permission from Lippincott, Williams and Wilkins.)

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can help to reduce artifact in the averaged BAEPs. A line frequency notch filer can also be employed. However, some equipment, notably the light sources of operating microscopes, may generate higher harmonics of the line frequency (Fig. 7D) that are not removed by filtering and are more difficult to remove by signal averaging than a pure 50 or 60 Hz sine wave. Electrocautery artifact is typically large enough to trigger artifact rejection (Fig. 7B). However, monopolar electrocautery may saturate the amplifier input stages for a considerable time after the cautery current stops. Since DC and low frequencies are removed by analog filtering, the voltages at the inputs to the analog-todigital converter rapidly return to near zero. The subsequent data epochs, which do not contain any evoked potential, will not be rejected as artifacts, and their incorporation into the average will cause an apparent amplitude attenuation of the BAEPs. This problem can be avoided by manually pausing the averager until examination of the raw data shows that the amplifiers have recovered (Legatt, 1991). Some commercial evoked potential recording systems suspend averaging when they detect an amplifier saturation condition. The high-frequency artifact caused by cavitational ultrasonic surgical aspirator (CUSA) devices may also completely obliterate the neural signals without triggering automatic artifact rejection (Fig. 7C), causing an apparent amplitude attenuation of the BAEPs. Therefore, averaging should be manually paused during CUSA use (Legatt, 1991).

A.D. LEGATT

is lowered enough, the BAEPs may disappear completely; the longer-latency components usually disappear before wave I does. The degree of hypothermia required to obliterate the BAEPs varies in different reports, ranging from 25  C (Stockard et al., 1978a, 1978b) to 20  C (Markand et al., 1987; Hett et al., 1995), though Rosenblum et al. (1985) reported recording interpretable BAEPs at temperatures as low as 14  C. These temperatures are most often encountered during hypothermic cardioplegia, but body temperature decreases of a lesser degree are commonly seen in anesthetized patients and may produce mild BAEP latency prolongations. Localized hypothermia within the surgical field, caused by irrigation with cold fluids, can also cause BAEP alterations in the absence of tissue damage (Fig. 8). Irrigation with cold fluids is also undesirable during posterior fossa surgery because it can produce neurotonic facial EMG discharges resembling those caused by facial nerve injury (Kartush and Bouchard, 1992). Drilling of bone, such as the roof of the internal auditory canal during resection of an eighth nerve tumor, will produce high noise levels in both ears via bone conduction and can alter the BAEPs due to acoustic masking (Levine et al., 1994). This should be kept in mind when evaluating BAEPs acquired during drilling of bone. Alternatively, BAEP averaging can be paused during drilling. 22.5.3. Localized auditory system dysfunction

22.5.2. Physiologic effects Anesthetic agents in the usual concentrations produce only minimal changes in BAEP amplitudes and latencies (see Legatt, 2002 for more details), but BAEPs do change in response to hypothermia. Both the interpeak intervals and the latency of wave I progressively increase as the patient is cooled. Component latencies and interpeak intervals increase by about 7% for each 1  C drop in temperature, and at 26  C are about double their values at normal body temperatures (Markand et al., 1987). The latency changes are reversible upon rewarming, but there is hysteresis — latencies at the same temperature may differ between the cooling and rewarming phases (Markand et al., 1990). BAEP component amplitudes may show an initial increase as the core temperature is lowered to the 25–30  C range, but then decrease as the patient is cooled further (Kusakari et al., 1984; Markand et al., 1987; Rodriguez et al., 1995). If the temperature

Auditory system dysfunction and damage can be caused by mechanical forces such as compression or traction, by thermal injury from cauterization, or by ischemia due to compromise of the vascular supply to the tissue. Some changes may be irreversible, but detection of these may, nonetheless, improve the surgical outcome, since notification about the BEP changes may prevent the surgeons from damaging more tissue in the area. The pattern of BAEP changes that occur depends on the location of the dysfunction (Legatt, 2002). Cochlear dysfunction will cause delay and attenuation of wave I (and the proximal eighth nerve compound action potential, if this is being monitored). As wave I becomes delayed, the latencies of later components increase in parallel, with little change in the interpeak intervals. Cochlear dysfunction may also decrease the amplitude of wave I to the point where it is no longer identifiable, resulting in a BAEP waveform with a delayed wave V, a delayed

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09:27, 36.6 °C, starting operation 10:38, 37.0 °C, opening dura

11:02, 37.3 °C, retracting cerebellum

11:45, 37.3 °C, resecting tumor

13:05, 37.4 °C, resecting tumor

13:34, 37.6 °C, irrigating

14:03, 37.5 °C, irrigating 14:15, 37.3 °C, irrigating 14:23, 37.3 °C, stopped irrigating

15:07, 37.4 °C, closing

0.25 µV 1 ms

Fig. 8. Intraoperative brainstem auditory evoked potentials (BAEPs) to right ear stimulation during surgery for a meningioma in the right cerebellopontine angle. The BAEPs were stable during cerebellar retraction and tumor resection. After the tumor had been removed, copious irrigation of the surgical field with cold fluids produced a transient prolongation of the I– III interpeak interval, reflecting slowing of the conduction velocity within the eighth nerve due to local cooling. The peaks latencies of waves I, III, and V are marked by the small diamonds, and the clock times, esophageal temperatures, and surgical procedures corresponding to each of the BAEP waveforms are noted at the right. (Reprinted from Legatt, 2002, with permission from Lippincott, Williams and Wilkins.)

or absent wave III, and an absent wave I. With more severe cochlear dysfunction, all BAEP components are lost (Fig. 9). Dysfunction of the eighth nerve proximal to its cochlear end will cause a prolongation of the I–III interpeak interval, attenuation of waves III and V, or both. The latencies of waves III and V increase in parallel, with relatively little change in the III–V interpeak interval unless the auditory pathways within the brainstem are also affected (Figs. 8 and 10). If the damage is severe enough, waves III and V will be lost (Fig. 3). Changes such as these have been correlated with dissection of cerebellopontine angle tumors off the eighth nerve (Levine et al., 1984). Wave I may also become delayed or disappear if there is concurrent cochlear dysfunction due to compromise of the internal auditory artery (see below); according to Sekiya et al. (1985), obliteration

of wave I during manipulation of the eighth nerve is always due to such vascular compromise. If the cochlea is unaffected, however, and the damage to the eighth nerve is all proximal to its cochlear end, wave I may persist, even if the eighth nerve is completely transected (Fig. 3). Wave II could also persist in this situation due to its contribution from the distal eighth nerve. Damage to the lower pons, around the area of the cochlear nucleus or the superior olivary complex, will also delay waves III and V or cause them both to be lost; wave I will be preserved if the ear and eighth nerve are intact. Damage to the brainstem that is entirely rostral to the lower pons, but at or below the level of the mesencephalon will affect wave V, but not waves I or III. Changes in wave IV tend to parallel those in wave V, though occasionally these components may be differentially affected (Fig. 5).

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0.2 µV I

V

2 ms

Fig. 9. Consecutive brainstem auditory evoked potentials (BAEPs) to left ear stimulation (earliest waveform at the top) recorded in a patient undergoing surgery for a left acoustic neuroma. A clear wave I and a poorly formed wave V were initially present and were stable during the initial dissection, but all BAEP components disappeared simultaneously during dissection within the internal auditory canal and remained absent through the end of the operation. This was most likely due to interruption of the blood supply to the cochlea via the internal auditory artery. (Reprinted from Legatt, 2002, with permission from Lippincott, Williams and Wilkins.)

Brainstem compromise can also cause an increase in the amplitude of wave I, reflecting dysfunction of descending inhibitory pathways within the auditory system (Musiek, 1986; Legatt et al., 1988). Intraoperative loss of wave V does not rule out the possibility of preserved postoperative hearing, even if wave V remains absent through the end of the operation (Levine et al., 1994; Harner et al., 1996). This may be due to temporal dispersion without conduction block of activity in the ascending auditory pathways. It may also reflect damage that affects only a portion of the brainstem auditory pathways; BAEPs reflect activity in a subset of the brainstem auditory

system that subserves sound localization, and hearing can be audiometrically normal in patients with grossly abnormal BAEPs (Legatt et al., 1988). Several specific surgical situations that can cause “true positive” BAEP changes are discussed in the following sections. Further details can be found in Legatt (2002). 22.5.3.1. Direct mechanical damage to the cochlea or labyrinth During drilling of the temporal bone, the membranous labyrinth may be inadvertently entered. This generally leads to deafness and a loss of all BAEP components

BRAINSTEM AND AUDITORY EVOKED POTENTIALS 1.68

4.20 2.52

345

6.06 1.86

0.2 µV 2 ms

3.54 1.83

2.13 5.37

7.50 ms

Fig. 10. Intraoperative brainstem auditory evoked potentials (BAEPs) to right ear stimulation recorded during surgery for a right acoustic neuroma, showing two runs recorded before (top) and after (bottom) retraction of the cerebellum. The most prominent change in the BAEPs was an increase in the I–III interpeak interval of more than 1 ms, reflecting stretching of the eighth nerve. The smaller change in the III–V interpeak interval may reflect effects of the retraction on the brainstem. (Reprinted from Legatt, 2002, with permission from Lippincott, Williams and Wilkins.)

to stimulation of the affected ear. However, hearing can sometimes be preserved when a semicircular canal is entered during drilling if it is immediately closed with bone wax (Molony et al., 1992; Ojemann, 2001). 22.5.3.2. Cochlear ischemia or infarction The cochlea receives its blood supply from the intracranial circulation via the internal auditory artery, which is usually a branch of the anterior inferior cerebellar artery and passes through the internal auditory canal alongside the eighth nerve (Kim et al., 1990). Damage to this artery will cause cochlea ischemia or infarction, affecting wave I and all subsequent BAEP components. The effects occur rapidly, though complete recovery can occur if flow is restored within several minutes (Perlman et al., 1959). Damage to the internal auditory artery probably accounts for most cases of sudden loss of all BAEP components, including wave I (Fig. 9), during surgery for cerebellopontine angle tumors (Nadol et al., 1987). Although BAEP changes due to compression of this artery may be reversible (Perlman et al., 1959), they often reflect obstruction, disruption, or coagulation of the artery during tumor

resection within the internal auditory canal, which causes irreversible cochlear damage and postoperative deafness. Levine et al. (1994) reported that, when monitoring the ECochG in conjunction with the BAEPs during surgery for cerebellopontine angle tumors, if the eighth nerve compound action potential suddenly disappeared and remained absent for more than 15 min, hearing was never preserved. 22.5.3.3. Eighth nerve stretch due to cerebellar retraction Retraction of the cerebellum to gain access to the cerebellopontine angle also moves the brainstem away from the internal auditory meatus and stretches the eighth nerve, which may cause hearing loss. Intraoperative BAEP monitoring may serve to notify the surgeons when the eighth nerve is being stretched and the retraction needs to be reduced or readjusted (Mller and Jannetta, 1983) (Fig. 10). 22.5.3.4. Direct mechanical or thermal damage to the eighth nerve The eighth nerve can be directly traumatized during posterior fossa surgery, such as for cerebellopontine angle tumors, either mechanically or by heat from

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tissue cauterization. Pressure on the nerve is a potentially reversible cause of nerve dysfunction. BAEP changes during manipulation of the eighth nerve may also reflect vasospasm within the nerve (Levine et al., 1984; Nadol et al., 1987). 22.5.3.5. Distal avulsion due to traction on the eighth nerve Complete resection of eighth nerve tumors may require scraping fragments of tumor off the nerve, which may cause BAEP changes either due to direct auditory nerve damage or to the effects of the traction on the nerve. At its distal (cochlear) end, the auditory nerve breaks up into fine fascicles that enter the bony modiolus. These fascicles are mechanically fragile, and may be avulsed if the traction on the nerve is from the ear towards the brainstem, whereas traction on the nerve from the brainstem towards the ear is relatively benign. Excessive cerebellar retraction is another potential cause of distal eighth nerve avulsion (Sekiya and Mller, 1987). 22.5.3.6. Brainstem damage during posterior fossa vascular surgery BAEP changes during posterior fossa vascular surgery may reflect ischemia or infarction to the brainstem auditory pathways due to clipping or compression of arteries perfusing the brainstem (Fig. 5); also, in the event of aneurysm rupture, they may reflect loss of perfusion pressure within the posterior circulation, effectively a “steal phenomenon” (note the changes in the SEP to left median nerve stimulation in Fig. 5) (Legatt, 2002). However, BAEPs may also remain unchanged in patients who suffer brainstem damage that anatomically spares the auditory pathways (Little et al., 1987). While preservation of the BAEPs does not guarantee a good outcome, patients with significant BAEP changes that persist to the end of the operation almost always have new postoperative neurologic deficits (Little et al., 1983; Manninen et al., 1994). 22.5.3.7. Brainstem damage during tumor surgery Mechanisms of brainstem damage during posterior fossa tumor surgery include compression, ischemia/ infarction due to compromise of the blood supply, direct mechanical damage from dissection (including CUSA), and thermal injury from cautery or laser use. The presence or absence of BAEP changes, and their pattern if present, will depend on the areas of the brainstem that are involved. As in the case of vascular surgery, brainstem damage that spares the auditory

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pathways may leave the BAEPs unchanged, even in patients who suffer significant neurologic morbidity. 22.5.3.8. BAEP changes with closing of the dura Adverse BAEP changes can occur at or after closure of the dura, even if BAEPs were stable prior to that point (Ojemann et al., 1984; Mller and Mller, 1989; Wahlig et al., 1999). These may reflect shifts of posterior fossa contents with compression of auditory pathway structures and, if untreated, may correspond to significant postoperative hearing loss (Mller and Mller, 1989). 22.6. Reaction to BAEP changes A variety of responses are possible when significant BAEP changes are reported to the surgeons, including readjustment of retraction, measures to reverse vasospasm within the eighth nerve, and modification of the dissection techniques. Accurate localization of the area of dysfunction that is causing the evoked potential changes will permit selection of the most appropriate responses. During surgery for cerebellopontine angle tumors, BAEP and ECochG findings that indicate that hearing has been irreversibly lost (disappearance of the eighth nerve compound action potential for more than 15 min) may permit the surgeon to abandon attempts to preserve the eighth nerve, and thus resect the remainder of the tumor more quickly (Levine et al., 1994). It should be noted, however, that loss of wave V does not rule out the possibility of preserved postoperative hearing, even if wave V remains absent through the end of the operation during tumor (Levine et al., 1994) or microvascular decompression (Friedman et al., 1985; Radtke et al., 1989) surgery. Neu et al. (1999) feel that patients with postoperative hearing despite loss of wave V may be at high risk for a delayed postoperative hearing loss. References American Clinical Neurophysiology Society (2006) Guideline 9C: guidelines on short-latency auditory evoked potentials. J. Clin. Neurophysiol., 23: 157–167. Banoub, M, Tetzlaff, JE and Schubert, A (2003) Pharmacologic and physiologic influences affecting sensory evoked potentials: implications for perioperative monitoring. Anesthesiology, 99: 716–737. Brown, RH, Jr., Chiappa, KH and Brooks, E (1981) Brainstem auditory evoked responses in 22 patients with intrinsic brainstem lesions: implications for clinical interpretations. Electroencephalogr. Clin. Neurophysiol., 52: 38P.

BRAINSTEM AND AUDITORY EVOKED POTENTIALS Campbell, KB, Bell, I and Bastien, C (1992) Evoked potential measures of information processing during natural sleep. In: RJ Broughton and RD Ogilvie (Eds.), Sleep, Arousal, and Performance. Birkhauser, Boston, pp. 89–116. Emerson, RG, Brooks, EB, Parker, SW and Chiappa, KH (1982) Effects of click polarity on brainstem auditory evoked potentials in normal subjects and patients: unexpected sensitivity of wave V. Ann. N. Y. Acad. Sci., 388: 710–721. Faught, E and Oh, SJ (1985) Brainstem auditory evoked responses in brainstem infarction. Stroke, 16: 701–705. Fischer, C, Bognar, L, Turjman, F and Lapras, C (1995) Auditory evoked potentials in a patient with a unilateral lesion of the inferior colliculus and medial geniculate body. Electroencephalogr. Clin. Neurophysiol., 96: 261–267. Friedman, WA, Kaplan, BJ, Gravenstein, D and Rhoton, AL, Jr. (1985) Intraoperative brainstem auditory evoked potentials during posterior fossa microvascular decompression. J. Neurosurg., 62: 552–557. Gersdorff, MCH (1982) Simultaneous recordings of human auditory potentials: transtympanic electrocochleography (ECoG) and brainstem-evoked responses (BER). Arch. Otorhinolaryngol., 234: 15–20. Grandori, F (1986) Field analysis of auditory evoked brainstem potentials. Hear. Res., 21: 51–58. Harner, SG, Harper, CM, Beatty, CW, Litchy, WJ and Ebersold, MJ (1996) Far-field auditory brainstem response in neurotologic surgery. Am. J. Otol., 17: 150–153. Hett, DA, Smith, DC, Pilkington, SN and Abbott, TR (1995) Effect of temperature and cardiopulmonary bypass on the auditory evoked response. Br. J. Anaesthiol., 75: 293–296. Hirsch, BE, Durrant, JD, Yetiser, S, Kamerer, DB and Martin, WH (1996) Localizing retrocochlear hearing loss. Am. J. Otol., 17: 537–546. Hughes, JR and Fino, JJ (1985) A review of generators of the brainstem auditory evoked potential: contribution of an experimental study. J. Clin. Neurophysiol., 2: 355–381. Jewett, DL and Williston, JS (1971) Auditory-evoked far fields averaged from the scalp of humans. Brain, 94: 681–696. Kartush, JM and Bouchard, KR (1992) Intraoperative facial nerve monitoring. Otology, neurotology, and skull base surgery. In: JM Kartush and KR Bouchard (Eds.), Neuromonitoring in Otology and Head and Neck Surgery. Raven Press, New York, pp. 99–120. Kim, HN, Kim, YH, Park, IY, Kim, GR and Chung, IH (1990) Variability of the surgical anatomy of the neurovascular complex of the cerebellopontine angle. Ann. Otol. Rhinol. Laryngol., 99: 288–296. Kusakari, J, Inamura, N, Sakurai, T and Kazutomo, K (1984) Effect of hypothermia on brainstem auditory

347 evoked potentials in humans. Tohoku J. Exp. Med., 143: 351–359. Legatt, AD (1991) Intraoperative neurophysiologic monitoring. In: EAM Frost (Ed.), Clinical Anesthesia in Neurosurgery. Butterworth-Heinemann, Boston, MA, pp. 63–127. Legatt, AD (1995) Intraoperative neurophysiologic monitoring: some technical considerations. Am. J. EEG Technol., 35: 167–200. Legatt, AD (2002) Mechanisms of intraoperative brainstem auditory evoked potential changes. J. Clin. Neurophysiol., 19: 396–408. Legatt, AD (2005) Brainstem auditory evoked potentials: methodology, interpretation, and clinical application. In: MJ Aminoff (Ed.), Electrodiagnosis in Clinical Neurology. Churchill Livingstone, New York, pp. 489–523. Legatt, AD, Pedley, TA, Emerson, RG, Stein, BM, Abramson, M, Dowling, K and Gallo, E (1986) Electrophysiological monitoring of seventh and eighth nerve function during surgery for acoustic neuromas. Electroencephalogr. Clin. Neurophysiol., 64: 30P. Legatt, AD, Arezzo, JC and Vaughan, HG, Jr. (1988) The anatomic and physiologic bases of brainstem auditory evoked potentials. Neurol. Clin., 6: 681–704. Levine, RA, Ojemann, RG, Montgomery, WW and McGaffigan, PM (1984) Monitoring auditory evoked potentials during acoustic neuroma surgery. Insights into the mechanism of the hearing loss. Ann. Otol. Rhinol. Laryngol., 93: 116–123. Levine, RA, Ronner, SF and Ojemann, RG (1994) Auditory evoked potential and other neurophysiologic monitoring techniques during tumor surgery in the cerebellopontine angle. In: CM Loftus and VC Traynelis (Eds.), Intraoperative Monitoring Techniques in Neurosurgery. McGraw-Hill, New York, pp. 175–191. Linden, DE (2005) The P300: where in the brain is it produced and what does it tell us? Neuroscientist, 11: 563–576. Litscher, G (1995) Continuous brainstem auditory evoked potential monitoring during nocturnal sleep. Int. J. Neurosci., 82: 135–142. Little, JR, Lesser, RP, Lu¨ders, H and Furlan, AJ (1983) Brainstem auditory evoked potentials in posterior circulation surgery. Neurosurgery, 12: 496–502. Little, JR, Lesser, RP and Lu¨ders, H (1987) Electrophysiological monitoring during basilar aneurysm operation. Neurosurgery, 20: 421–427. Loughnan, BL, Sebel, PS, Thomas, D, Rutherfoord, CF and Rogers, H (1987) Evoked potentials following diazepam or fentanyl. Anaesthesia, 42: 195–198. Manninen, PH, Patterson, S, Lam, AM, Gelb, AW and Nantau, WE (1994) Evoked potential monitoring during posterior fossa aneurysm surgery: a comparison of two modalities. Can. J. Anaesth., 41: 92–97.

348 Markand, ON, Lee, BI, Warren, C, Stoelting, RK, King, RD, Brown, JW and Mahomed, Y (1987) Effects of hypothermia on brainstem auditory evoked potentials in humans. Ann. Neurol., 22: 507–513. Markand, ON, Warren, C, Mallik, GS and Williams, CJ (1990) Temperature-dependent hysteresis in somatosensory and auditory evoked potentials. Electroencephalogr. Clin. Neurophysiol., 77: 425–435. Mller, AR and Jannetta, PJ (1983) Monitoring auditory functions during cranial nerve microvascular decompression operations by direct recording from the eighth nerve. J. Neurosurg., 59: 493–499. Mller, AR and Mller, MB (1989) Does intraoperative monitoring of auditory evoked potentials reduce incidence of hearing loss as a complication of microvascular decompression of cranial nerves? Neurosurgery, 24: 257–263. Molony, TB, Kwartler, JA, House, WF and Hitselberger, WE (1992) Extended middle fossa and retrolabyrinthine approaches in acoustic neuroma surgery: case reports. Am. J. Otol., 13: 360–363. Musiek, FE (1986) Neuroanatomy, neurophysiology, and central auditory assessment. Part III: Corpus callosum and efferent pathways. Ear Hear., 7: 349–358. Nadol, JB, Jr., Levine, R, Ojemann, RG, Martuza, RL, Montgomery, WW and De Sandoval, PK (1987) Preservation of hearing in surgical removal of acoustic neuromas of the internal auditory canal and cerebellar pontine angle. Laryngoscope, 97: 1287–1294. Neu, M, Strauss, C, Romsto¨ck, J, Bischoff, B and Fahlbusch, R (1999) The prognostic value of intraoperative BAEP patterns in acoustic neurinoma surgery. Clin. Neurophysiol., 110: 1935–1941. Oh, SJ, Kuba, T, Soyer, A, Choi, IS, Bonikowski, FP and Vitek, J (1981) Lateralization of brainstem lesions by brainstem auditory evoked potentials. Neurology, 31: 14–18. Ojemann, RG (2001) Retrosigmoid approach to acoustic neuroma (vestibular schwannoma). Neurosurgery, 48: 553–558. Ojemann, RG, Levine, RA, Montgomery, WM and McGaffigan, P (1984) Use of intraoperative auditory evoked potentials to preserve hearing in unilateral acoustic neuroma removal. J. Neurosurg., 61: 938–948. Perlman, HB, Kimura, R and Fernandez, C (1959) Experiments on temporary obstruction of the internal auditory artery. Laryngoscope, 69: 591–613. Radtke, RA, Erwin, CW and Wilkins, RH (1989) Intraoperative brainstem auditory evoked potentials: significant decrease in postoperative morbidity. Neurology, 39: 187–191. Raudzens, PA and Shetter, AG (1982) Intraoperative monitoring of brainstem auditory evoked potentials. J. Neurosurg., 57: 341–348.

A.D. LEGATT Rodriguez, RA, Audenaert, SM, Austin, EH, III and Edmonds, HL, Jr. (1995) Auditory evoked responses in children during hypothermic cardiopulmonary bypass: report of cases. J. Clin. Neurophysiol., 12: 168–176. Rodriguez, RA, Edmonds, HL, Jr., Auden, SM and Austin, EH, III (1999) Auditory brainstem evoked responses and temperature monitoring during pediatric cardiopulmonary bypass. Can. J. Anaesth., 46: 832–839. Roeser, RJ and Clark, JL (2000) Clinical masking. In: RJ Roeser, M Valente and H Hosford-Dunn (Eds.), Audiology: Diagnosis. Thieme, New York, pp. 253–279. Rosenblum, SM, Ruth, RA and Gal, TJ (1985) Brainstem auditory evoked potential monitoring during profound hypothermia and circulatory arrest. Ann. Otol. Rhinol. Laryngol., 94: 281–283. Ruben, RJ, Bordley, JE and Lieberman, AT (1961) Cochlear potentials in man. Laryngoscope, 71: 1141–1164. Scaioli, V, Savoiardo, M, Bussone, G and Rezzonico, M (1988) Brainstem auditory evoked potentials (BAEPs) and magnetic resonance imaging (MRI) in a case of facial myokymia. Electroencephalogr. Clin. Neurophysiol., 71: 153–156. Schlake, HP, Milewski, C, Goldbrunner, RH, Kindgen, A, Riemann, R, Helms, J and Roosen, K (2001) Combined intra-operative monitoring of hearing by means of auditory brainstem responses (ABR) and transtympanic electrocochleography (ECochG) during surgery of intra- and extrameatal acoustic neurinomas. Acta Neurochir. (Wien), 143: 985–995. Schneider, G, Hollweck, R, Ningler, M, Stockmanns, G and Kochs, EF (2005) Detection of consciousness by electroencephalogram and auditory evoked potentials. Anesthesiology, 103: 934–943. Schwartz, DM, Morris, MD, Spydell, JD, Brink, CT, Grim, MA and Schwartz, JA (1990) Influence of click polarity on the brainstem auditory evoked response (BAER) revisited. Electroencephalogr. Clin. Neurophysiol., 77: 445–457. Sekiya, T and Mller, AR (1987) Avulsion rupture of the internal auditory artery during operations in the cerebellopontine angle: a study in monkeys. Neurosurgery, 21: 631–637. Sekiya, T, Iwabuchi, T, Kamata, S and Ishida, T (1985) Deterioration of auditory evoked potentials during cerebellopontine angle manipulations. An interpretation based on an experimental model in dogs. J. Neurosurg., 63: 598–607. Starr, A and Hamilton, AE (1976) Correlation between confirmed sites of neurological lesions and abnormalities of far-field auditory brainstem responses. Electroencephalogr. Clin. Neurophysiol., 41: 595–608. Stockard, JJ and Rossiter, VS (1977) Clinical and pathologic correlates of brainstem auditory response abnormalities. Neurology, 27: 316–325.

BRAINSTEM AND AUDITORY EVOKED POTENTIALS Stockard, JJ, Stockard, JE and Sharbrough, FW (1977) Detection and localization of occult lesions with brainstem auditory responses. Mayo Clin. Proc., 52: 761–769. Stockard, JJ, Sharbrough, FW and Tinker, JA (1978a) Effects of hypothermia on the human brainstem auditory response. Ann. Neurol., 3: 368–370. Stockard, JJ, Stockard, JE and Sharbrough, FW (1978b) Nonpathologic factors influencing brainstem auditory evoked potentials. Am. J. EEG Technol., 18: 177–209. Stockard, JJ, Pope-Stockard, JE and Sharbrough, FW (1992) Brainstem auditory evoked potentials in neurology: methodology, interpretation, and clinical application. In: MJ Aminoff (Ed.), Electrodiagnosis in Clinical Neurology. Churchill Livingstone, New York, pp. 503–536. Strominger, NL (1973) The origins, course and distribution of the dorsal and intermediate acoustic striae in the rhesus monkey. J. Comp. Neurol., 147: 209–234. Strominger, NL and Strominger, AI (1971) Ascending brainstem projections of the anteroventral cochlear nucleus in the rhesus monkey. J. Comp. Neurol., 143: 217–242. Strominger, NL, Nelson, LR and Dougherty, WJ (1977) Second-order auditory pathways in the chimpanzee. J. Comp. Neurol., 172: 349–366.

349 Symon, L, Sabin, HI, Bentivoglio, P, Cheesman, AD, Prasher, D and Barratt, H (1988) Intraoperative monitoring of the electrocochleogram and the preservation of hearing during acoustic neuroma excision. Acta Neurochir. Suppl. (Wien), 42: 27–30. Wahlig, JB, Kaufmann, AM, Balzer, J, Lovely, TJ and Jannetta, PJ (1999) Intraoperative loss of auditory function relieved by microvascular decompression of the cochlear nerve. Can. J. Neurol. Sci., 26: 44–47. Yamada, T (1988) The anatomic and physiologic bases of median nerve somatosensory evoked potentials. Neurol. Clin., 6: 705–733. York, DH (1986) Correlation between a unilateral midbrainpontine lesion and abnormalities of brainstem auditory evoked potential. Electroencephalogr. Clin. Neurophysiol., 65: 282–288. Yvert, B, Crouzeix, A, Bertrand, O, Seither-Preisler, A and Pantev, C (2001) Multiple supratemporal sources of magnetic and electric auditory evoked middle latency components in humans. Cereb. Cortex, 11: 411–423. Zanette, G, Carteri, A and Cusumano, S (1990) Reappearance of brainstem auditory evoked potentials after surgical treatment of a brainstem hemorrhage: contributions to the question of wave generation. Electroencephalogr. Clin. Neurophysiol., 77: 140–144.