NEUROPELVEOLOGY

The basic functional neuroanatomy of the genitourinary and anorectal systems is briefly described. These systems are involved in the so-called sacral functions (micturition, defecation, erection, ejaculation, etc.). In this section we describe clinical neurophysiological tests of the functional integrity of the sacral neuromuscular system used for diagnostic purposes. Later we deal with intraoperative neurophysiological monitoring of the lumbosacral nervous system. The validity of different intraoperative monitoring techniques of this system is summarized.

The functions involving the genitourinary and anorectal systems are uniquely controlled by the complex interaction of the vegetative and the somatic nervous system. Insofar as it is the sympathetic, sacral parasympathetic and somatic systems that constitute the most important peripheral nervous structures controlling these functions, they may also be referred to as sacral functions. The functions themselves (micturition, defecation, erection, etc.) are now better understood because with introduction of methods of measuring the different functional parameters (urodynamics, faecodynamics, measurements of the sexual response) that provide for better diagnosis of dysfunction. The awareness that such dysfunction is also a consequence of damage to neural structures has also greatly increased. On the other hand, it has become possible to better define the various lesions to the nervous system by electrophysiological methods. However, these methods by and large document only the somatic sacral nervous system and its central pathways [1]. Nevertheless, such information is clinically relevant because (1) the somatic nervous system plays a part in all sacral functions, and (2) the somatic and parasympathetic sacral systems are closely related, and information on the somatic system may therefore be a relevant indicator of the overall neurogenic lesion in several clinical situations.
In fact, the common denominator of lower urinary tract, anorectal, and sexual functions is that many of their efferent and afferent pathways travel at least partly in close vicinity. They “share” common spinal cord regulatory segments (the upper lumbar segments—sympathetic efferents; the middle and lower sacral segments—parasympathetic and somatic efferents). Even the long pathways connecting the relevant spinal cord segments with higher levels of the central nervous system are situated close together. Thus it is not uncommon that in lesions to the nervous system, and particularly in lesions affecting the spinal cord, cauda equina, sacral plexus, and pudendal nerve, the sacral functions are affected together. Dysfunctions may arise not only from disease or trauma, but also from inadvertent lesions to the previously named structures during invasive procedures, particularly several surgeries involving the pelvic organs and the spinal canal. The consequences of lesions to the neurocontrol of sacral functions include disturbing sensory phenomena like pain, dysethesia, urgency and frequency, loss of genital sensation, bladder or rectal fullness, and subsequent retention, obstipation, soiling, incontinence, and erectile dysfunction.
Neurogenic damage may lead to lost coordination between detrusor and sphincter function, leading to high bladder pressures and upper urinary tract dysfunction. Incontinence may—particularly in motor-disabled persons—lead to problems with hygiene, skin problems, infections, and decubiti.
Although neurogenic sexual dysfunction may not be life-threatening, it can be extremely disruptive psychologically and can lead to severe emotional and interpersonal problems. All these may be particularly tragic when they are a consequence of an inadvertent intraoperative lesion.
A whole array of clinical neurophysiological diagnostic methods has been modified for use in the anogenital area, including electromyographic methods and reflex, conduction, and evoked potential studies [2,3]. These methods are routinely employed in uroneurological and neuro-urological laboratories for diagnostics and follow-up in patients with (suspected) neurogenic sacral dysfunction.
Trials were performed to establish some of these neurophysiological methods in the operating room, to help the surgeon identify particular sacral nervous structures, and to monitor the function of the sacral neuromuscular system during surgery [4–7].
2 FUNCTIONAL ANATOMY
Although the functional anatomy of the genitourinary and anogenital systems is highly complex, it need not be considered in detail because only the gross anatomy of the relevant somatic nervous structures can be approached by clinical neurophysiological methods that are applicable in the operating room environment.
Most of the information relevant for intraoperative neurophysiology can be summarized as follows. Afferent fibers from the mucosa and skin of the genitoperineal region travel mostly with the pudendal nerves. The distally most accessible group of sensory fibers are the dorsal nerves of the penis (or clitoris). The sensory fibers from the genital, perineal, and anal region enter through the dorsal spinal roots S2–S5 into the spinal cord and synapse (through interneurons) with sphincteric motor neurons. The afferent information also ascends (the primary sensory neurons synapsing to higher-order sensory neurons at various levels) via the spinothalamic and dorsal column tracts, the lemniscal system and thalamocortical tracts, and finally to the somatosensory cortex (at its interhemispheric location) [8].
The sphincteric lower motor neurons in the midventral spinal grey matter of the second to fourth sacral spinal cord segments (the “Onuf nucleus”) are under voluntary control from the motor cortex. Somatic motor nerve fibers leave through the ventral roots and the sacral plexus, combining into the pudendal nerves; direct branches innervate the levator ani and the anal sphincter [8]. The external urethral sphincter may be innervated by sacral somatic fibers traveling via splanchnic nerves [9] or the pudendal nerve [10], or possibly both.

2.1 NEURAL CONTROL OF THE LOWER URINARY TRACT
The lower urinary tract (LUT) is innervated by three sets of peripheral nerves. The pelvic parasympathetic nerves arise at the sacral level of the spinal cord (they excite the bladder and relax the urethra). The sympathetic nerves arise from the upper lumbar segments and inhibit the bladder body, modulate transmission in bladder parasympathetic ganglia, and excite the bladder base and urethra. The somatic efferents and afferents from the S2–S4 sacral roots innervate pelvic floor muscles (levator ani) both through direct branches and by the pudendal nerve, which innervates also the perineal muscles, including the anal and urethral sphincter.
All of these nerves contain both efferent and afferent nerve fibers that are controlled by centers in the brain and particularly important centers in the brainstem. Long tracts in the spinal cord subserve the spinobulbospinal reflex pathway, which is relevant for coordinated detrusor-sphincter function and normal micturition. The dorsal pontine tegmentum is established as an essential control center for micturition (with a close anatomical relationship with the locus coeruleus). While different types of sensation of the lower urinary tract travel both in the anterolateral and the dorsal part of the spinal cord, the descending (motor) pathways lie within the lateral aspects of the spinal cord.

2.2 ANORECTUM
Touch, pin-pricks, and hot and cold stimuli can be perceived in the anal canal to a level of up to 15 mm above the anal valves. The epithelium in the area from about 10–15 mm above the valves has a rich sensory nerve supply made up of both free and organized nerve endings. The sensory endings in the hairy perianal skin are similar to those in hairy skin elsewhere. The afferent nerve pathway for anal canal sensation is by the inferior hemorrhoidal branches of the pudendal nerve. Sensory pathways from the rectum and the bladder travel in the pelvic visceral nerves to the sacral cord, but some afferent information is probably also related to hypogastric nerves entering the spinal cord at the thoracolumbar level.
Functionally, the most important part of the smooth musculature of the anorectum is the internal anal sphincter, which is responsible for about 85% of the resting pressure in the lumen of the canal. The smooth musculature of rectal walls (and of the detrusor) receives extrinsic motor innervation from the sacral parasympathetic outflow arising in the intermediolateral cell columns of sacral cord segments S2–S4. These first-order neurons send axons that emerge with the ventral spinal nerve roots to synapse with second-order neurons lying within the pelvic plexus or the visceral walls. The sympathetic nerve supply arises from the thoracolumbar chain and travels in the hypogastric nerve to innervate visceral smooth muscle directly, and also via a modulatory influence on parasympathetic function at the level of the pelvic plexus. The internal anal sphincter is probably controlled both by sympathetic (hypogastric) and sacral parasympathetic pathways, but the inhibition brought about by rectal distention (the important rectoanal inhibitory reflex) is predominantly an intramural one.
The external anal sphincter is innervated by the pudendal nerve and occasionally also by a perineal branch of S4. The neurons of the sphincter motor nucleus (Onuf’s nucleus) are under voluntary control via corticospinal pathways.
Normal defecation is probably triggered by filling of the rectum from the sigmoid colon, and the signals from stretch receptors in the rectal wall and pelvic floor muscles are interpreted at the conscious level as a desire to defecate. The extension of the rectum causes reflex relaxation of the smooth internal sphincter muscle. Voluntary relaxation of the striated sphincter muscle permits defecation, which is assisted by colonic pressure waves and abdominal straining. If defecation is to be deferred, brief conscious contraction of the voluntary sphincter allows time for recovery of internal sphincter tone and relaxation of the rectum to accommodate filling. Conscious appreciation of the desire to defecate and intentional control over defecation are conferred by suprasacral neural influences. The precise way in which the autonomic, pyramidal, extrapyramidal, and sensory pathways integrate to achieve a reliable and predictable anorectal function is not yet fully understood [11].

2.3 SEXUAL ORGANS
Of the sexual functions affected by neurogenic lesions, research has centered on the male functions, and particularly on erection. Erection can be initiated in the brain and/or follow genital stimulation; in sexual activity a combination of both is probably involved.
Neurogenic erectile dysfunction due to peripheral lesions can be secondary to the disruption of sensory nerves contributing to the afferent arm of reflex erection or to the disruption of autonomic nerves that mediate arterial dilatation and trabecular smooth muscle relaxation. Erectile dysfunction can occur from disruption of the relevant pathways in centers within the spinal cord (both suprasacral and sacral), cauda equina, the sacral plexus, the pelvic plexus, the cavernosal nerves, and the pudendal nerves. Particular pelvic surgeries such as radical prostatectomy or cystoprostatectomy lead to a high percentage of mostly neurogenic erectile dysfunction; the lesion occurs in the pelvic plexus or in the cavernosal nerves located in the posterolateral aspect of the prostate.
Ejaculation can be abolished by a lesion to the sympathetic innervation of the bladder neck (leading to a retrograde ejaculation) and by disruption of the sensory and (particularly) motor nerves innervating the perineal muscles, whose contraction leads to expulsion of the semen. It can also be abolished by central lesions.
A disturbed sexual response in females is due to (1) afferent lesions leading to loss of sensitivity of the perineal area, and (2) efferent lesions leading to a loss of lubrication, loss of clitoral erection, and pelvic floor muscle denervation.

3 CLINICAL NEUROPHYSIOLOGICAL TESTS IN DIAGNOSTICS
Since the function of all the aforementioned systems relies on neural control, clinical neurophysiological tests have been introduced to support and supplement clinical evaluation in patients. The tests comprise electrophysiologic methods of testing conduction through motor and sensory pathways (both peripheral and central) and electromyographic methods. Traditionally, in testing both the lower urinary tract and anorectal function, the EMG signal obtained from sphincter muscles has been used to delineate the sphincter activity patterns in relationship to micturition or defecation. In addition to that, electromyographic methods have been used to distinguish between normal and neuropathic pelvic floor muscles. Conduction tests have been introduced to evaluate the integrity of different reflex pathways (sacral reflexes), the individual motor pathways (pudendal nerve terminal latency, MEP), and sensory pathways (penile sensory neurography, SEP). In addition, autonomic tests have also been introduced (sympathetic skin response, corpus cavernosum EMG). For diagnostic purposes a single testing is performed without knowledge of the previous status of the investigated structure. In this diagnostic situation, results have to be compared to values obtained from healthy subjects. The tests of conduction have been found to be relatively insensitive to axonal lesions because amplitudes of responses vary widely in the control population (particularly due to technical reasons), and conduction may remain normal in partial lesions.
Thus, in the diagnostic situation, the ability of the concentric needle EMG to detect abnormal spontaneous activity as an indicator of denervation, and changes of motor unit potentials as indications of reinnervation, has been found to be particularly helpful. EMGs and recordings of the bulbocavernosus reflex (indicating the potency of the lower sacral reflex arc) have been proposed as the basic battery of tests for evaluation of patients with sacral dysfunctions and suspected neurogenic involvement [12]. From conduction tests, only recordings of the sacral reflex and SEP after dorsal penile or clitoral nerve stimulation have been suggested since they have been validated by extensive clinical studies.
They may be of value in selected patients with suspected peripheral (i.e., bulbocavernosus reflex testing) and central nervous system (i.e., SEP testing) lesions [3, 13]. The other neurophysiological tests have been suggested as useful in further research. The corpus cavernosum EMG is the most controversial of the tests so far described. It is not yet well clarified whether the signal really originates from penile smooth muscle; validation of the method would offer a most important source of information on penile innervation status, which is necessary for erection.

4 INTRAOPERATIVE CLINICAL NEUROPHYSIOLOGY
With appropriate modifications of methods it is technically feasible to record in anesthetized patients (a) dorsal root action potentials (DRAPs) after pudendal nerve stimulation, (b) pudendal somatosensory evoked potentials over the conus, the spinal cord, and the scalp, (c) sphincter muscle EMG responses to sacral ventral root stimulation and motor cortex stimulation, and (d) the bulbocavernosus reflex. Only one of the aforementioned techniques has been used extensively enough to gather pertinent information regarding the practical relevance of sacral nervous system monitoring during surgical interventions. However, the techniques are expected to be valuable safeguards against inadvertent lesioning of nervous structures that would lead to some (neurogenic) dysfunction of micturition, defecation, or the sexual response. Further studies are required to clarify these issues.

4.1 BASIC TECHNICAL ASPECTS OF STIMULATION FOR INTRAOPERATIVE SACRAL MONITORING
In order to obtain bioelectrical signals useful for monitoring purposes in the different segments of the sacral neuromuscular system, it is necessary to depolarize the nervous system at particular segments. Up to now only electrical stimulation has been appropriate for this purpose. Stimulation can be applied to either the sensory part or the motor part of the system (afferent versus efferent events; Fig. 9.1). At present, most intraoperative monitoring of the sacral system has relied on responses evoked from stimulation of the sensory system, apart from recording of anal sphincter muscle responses upon stimulation of ventral spinal roots or the motor cortex.

The appropriate peripheral sensory structures that are available for stimulating purposes are the two adjacent dorsal penile or clitoral nerves. These nerves are stimulated by silver/silver chloride cup EEG-type electrodes (EEG electrodes) placed on the dorsal surface of the penis or clitoris (this electrode representing the cathode). The other electrode (anode) is placed either distally on the penis (1–2 cm apart from the proximal electrode) or on the adjacent labia (Fig. 9.2). In small children with short penises, the anode may be attached on the ventral side of the penis. The dorsal side of the penis must be scrubbed gently with Nuprep (D. O. Weaver & Co., Aurora, CO) before placing electrodes in order to avoid stimulus artifacts. The electrodes are filled with electrode cream and secured appropriately (Tegaderm; Smith and Nephew Medical Limited, Hull, England). The electrode sites are then bandaged with a few layers of gauze to prevent them from being displaced when the patient is moved onto the
operating table. Electrode impedances should be kept below 5 kΩ.
As a general rule, stimuli of 20 mA intensity at 0.2 ms duration have been delivered in procedures involving stimulation of the penis or clitoris (at various frequencies for different measurements, up to 13.3 Hz).
Stimulation can also be performed at the level of the spinal roots; a handheld sterile monopolar electrode can be placed under the appropriate roots (or rootlets, after the root is freed from neighboring roots and lifted outside the spinal canal). Square wave pulses of 1 to 2 mA intensity and 0.2 ms duration are delivered (Fig. 9.1, right).

4.2 BASIC TECHNICAL ASPECTS OF RECORDING FOR INTRAOPERATIVE SACRAL MONITORING
Bioelectrical activity from the sacral neuromuscular system has up to now been recorded from the sacral dorsal spinal roots, the spinal cord, the somatosensory cortex, and the anal sphincter muscle.
Recordings from dorsal spinal roots (dorsal root action potentials, DRAPs) are obtained by hand-held sterile bipolar hook electrodes (after the root is freed from neighboring roots and lifted outside the spinal canal). In this case, the electrode closer to the point of stimulation is the G1 (active) electrode. Epoch lengths of 0 to 50 ms are used for these recordings (Figs. 9.1, 9.2).
Recordings of pudendal spinal somatosensory evoked responses (SSEPs, stationary wave) are obtained by a spinal epidural electrode placed over the conus (S2–S4). These potentials are generated by interneurons of the grey matter within the S2–S4 segments of the spinal cord. Typically 100 responses are averaged together; epoch lengths of 0–50 ms are used (Fig. 9.1).
Recordings of pudendal spinal somatosensory evoked responses (SSEPs, traveling wave) are obtained by a spinal epidural electrode inserted anywhere over the dorsal column of the spinal cord. These potentials are generated by pudendal afferents traveling within the dorsal columns. Typically 100 responses are averaged together; epoch lengths of 0–50 ms are used (Fig. 9.1).
To obtain pudendal cerebral somatosensory evoked responses (CSEPs), Screwtype recording electrodes are placed on the scalp 2 cm behind CZ (G1 or active electrode) and at FZ (G2 or reference electrode), according to the somatotopic representation in the primary somatosensory cortex related to the International 10–20 System of scalp electrode placement. The active electrode is placed in the
midline because the sacral segments are represented deep within the medial longitudinal interhemispheric fissure. For CSEPs, 100–200 traces are typically averaged together. Epoch lengths of 0–200 ms are used.
To record anal sphincter (EMG) responses, either surface-type electrodes or hook wire electrodes can be used. Given the close anatomical relationship between the small sphincter muscle and neighboring larger muscle groups, recording must be selective (e.g., with intramuscular hook wire electrodes) if the stimulation technique is “nonselective” (such as in the case of ventral root stimulation, as a consequence of which neighboring muscles are also excited).
When the stimulation procedure is more specific (e.g., in bulbocavernosus or pudendoanal reflex monitoring), the recording may be obtained with properly attached surface-type electrodes. Sterile hook wire recording electrodes (Teflon-coated, 76 μm diameter wire with a 3 mm bare tip) are introduced into the left and right sides of the external anal sphincter with sterile needles; these are immediately removed carefully from the sphincter (the hooked wires remaining in place). The integrity of the electrodes can be tested by passing a short train of 50 Hz current at 10 mA and observing sphincter contraction (if the patient is not paralyzed at the time of electrode placement). The electrode impedances of these electrodes should be checked, although clean recordings are usually still possible with high electrode impedances.
The epoch length used for anal sphincter EMG recordings varies according to the type of response; either single or few averaged responses can be obtained upon stimulation (of course, the patient should not be under the influence of a muscle relaxant during this procedure).

In the treatment of spasticity (e.g., in cerebral palsy), the sacral roots are increasingly being included during rhizotomy procedures. Lang [14] demonstrated that children who underwent L2–S2 rhizotomies had an 81% greater reduction in plantar/flexor spasticity compared to children who underwent only L2–S1 rhizotomies. But, as more sacral dorsal roots have been included in rhizotomies, neurosurgeons have experienced an increased rate of postoperative complications, especially with regards to bowel and bladder functions.
In order to spare sacral function, we attempted to identify those sacral dorsal roots that were carrying afferents from pudendal nerves. To do this, we used recordings of dorsal root action potentials (DRAPs). Patients were anesthetized with isoflurane, nitrous oxide, fentanyl, and a short-acting muscle relaxant introduced only at the time of intubation. The cauda equina was exposed through a T12–S2 laminotomy or laminectomy and the sacral roots were identified using bony anatomy. The dorsal roots were separated from the ventral ones, and DRAPs were recorded by a hand-held sterile bipolar hooked electrode (the root being lifted outside the spinal canal) (Fig. 9.2). The DRAPs were evoked by electrical stimulation of the penile or clitoral nerves. One hundred responses were averaged together and filtered between 1.5 and 2100 Hz. Each average response was repeated to assess its reliability. Afferent activity from the right and left dorsal roots of S1, S2, and S3 was always recorded, along with occasional recordings from the S4–S5 dorsal roots. DRAP recording was successfully obtained in the majority of patients, the DRAPs were present in the S2 and S3 roots bilaterally in 19 patients, whereas in 7 patients DRAPs were also present in both S1 roots (in 8 patients they were present in the S1 root unilaterally). However, the response in the S1 root was never larger than the S2 or S3 root responses. The range of amplitudes was 2.9–18.3 μV in S1 roots, 3.2–129.9 μV in S2 roots, and 4.6–333 μV in S3 roots.
Of special relevance was the finding that in 7.6% of these children, all afferent activity was carried by only one S2 root (Fig. 9.3, C and F). These findings were confirmed by a later analysis of the results of mapping in 114 children (72 male, 42 female, mean age 3.8 years) [5]. Mapping was successful in 105 out of 114 patients; S1 roots contributed 4.0%, S2 roots 60.5%, and S3 roots 35.5% of the overall pudendal afferent activity. The distribution of responses was asymmetrical in 56% of the patients (Fig. 9.3, B, C, and F). Pudendal afferent distribution was confined to a single level in 18% (Fig. 9.3, A), and even to a single root in 7.6% of patients (Fig. 9.3, C and F). Fifty-six percent of the pathologically responding S2 roots during rhizotomy testing were preserved because of the significant afferent activity, as demonstrated during pudendal mapping. None of the 105 patients developed long-term bowel or bladder complications.
All our results in the early series of dorsal root mapping with 19 patients [4] have been confirmed by analysis of the larger series of 105 patients [5]. With this series we showed that selective S2 rhizotomy can be performed safely without an associated increase in residual spasticity, while at the same time bowel and bladder function are preserved by performing pudendal afferent mapping [14].
Therefore, we suggest that the mapping of pudendal afferents in the dorsal roots should be employed whenever these roots are considered for rhizotomy in children with cerebral palsy without urinary retention. Preoperative neurourological investigation of the children should help in making appropriate decisions; for example, in children with cerebral palsy with hyperreflexive detrusor dysfunction, sacral rhizotomy may be considered to alleviate the problem. In any case, intraoperative mapping of sacral afferents should make selective surgical approaches possible and provide the maximal benefit for children with cerebral palsy.

Our results so far support the hypothesis that the root distribution of afferent fibers that are important for the control of micturition may be similar to the distribution of mucocutaneous afferent fibers from the pudendal nerve. Only further studies will clarify the complex functional anatomic issues involved.

Recordings were performed in four children of both sexes, 2.5 to 7.0 years of age. Small-amplitude (up to 1 μV) SSEPs, which were very stable, could be recorded with subdurally placed electrodes over the thoracic spinal cord (traveling waves), while a stationary wave could be recorded with a much higher amplitude (up to 10 μV) over the conus region. The latencies of the spinal SEP over the conus region ranged from 6.0 to 10.4 ms (Fig. 9.1, left). The recordings were made as a pilot study, and thus far only demonstrate the ability to obtain such recordings intraoperatively. Further employment of this technique showed that traveling waves are difficult to record, and successful recording of a stationary wave necessitates that the electrode be placed strictly over the S2–S4 sections of the spinal cord.

4.3.3 Pudendal Cerebral Somatosensory Evoked Potentials (CSEPs)
Well-formed cerebral SEPs with amplitudes of 0.5–0.7 μV were recorded on dorsal penile nerve stimulation throughout spinal neurosurgical procedures in two adult male patients, 50 and 78 years of age. Stable P40 peaks were obtained.
The recordings were made as a pilot study and thus far only demonstrate the ability to obtain such recordings intraoperatively. Further employment of this method showed that this potential is very sensitive to anesthetics; a formal feasibility study has not yet been performed.

4.3.4 Anal Sphincter Motor Response Monitoring
In five children of both sexes, 2.5 to 9.0 years old, anal sphincter muscle EMG responses were recorded by stimulation of the ventral spinal roots (L5, S1, S2, S3, and S4) to identify ventral roots carrying motor fibers to the sphincter muscle. Recordings were obtained by surface conductive rubber electrodes (applied para-anally) and intramuscular hooked wire electrodes. In surface recordings, no unilateral responses could be identified, and responses were also obtained on stimulation of the L5 and S1 roots (on stimulation of L5 and S1 roots no adequate responses could be discerned from simultaneous recordings from intramuscular electrodes). The surface recorded responses were recognized as “nonspecific” (derived from neighboring muscles, most probably glutei [15]).

The latency of surface recorded responses was, as a rule, shorter than the latency of responses obtained from intramuscular electrodes, which was between 5 and 8 ms. On electrical stimulation of the motor cortex, anal sphincter responses were recorded in a large group of anesthetized patients without pyramidal involvement. Because of polysynaptic connections of the corticospinal tract to the α-motoneuron of S2–S4, these responses are moderately sensitive to anesthetics (Fig. 9.1).

4.3.5 Bulbocavernosus Reflex (BCR) Monitoring
Intraoperative recordings were first performed in 15 neurosurgical patients (11 males, 4 females, 2–6 years old). Patients were without sacral dysfunction and were anesthetized with fenatyl and propofol or nitrous oxide without the influence of a muscle relaxant. Recordings from the anal sphincter were obtained by hooked wire electrodes and were recorded as a single response.
Very reproducible responses could be obtained on double-pulse stimulation, the optimum interstimulus interval being found to be 3 ms and the optimum stimulation rate 2.3 Hz. Continuous periods of stimulation and recording for up to 10 min were repeatedly performed with very reproducible results (Fig. 9.4). The reflex response was suppressed by the administration of isoflurane and nitrous oxide and was completely abolished by muscle relaxants [16]. After this pilot study, 119 patients were tested, 38 of which underwent surgery without risk and 81 of which underwent surgery with risk of damage to sacral structures. In all, 51 adults (19 to 64 years old, 32 male and 19 female) and 68 children (24 days to 17 years old, 30 male and 38 female) took part in the study. Patients were anesthetized with propofol, fenatyl, or nitrous oxide with a short-acting relaxant. Clinically, most patients had mild to moderate upper motor neuron deficits in the lower extremities, and no patient had major urinary problems. In all patients it was possible to record reproducible reflex response with the previously described method. In patients without risk to the sacral system, only a few minutes of the responses were recorded to test their feasibility, whereas in the patients at risk, continuous monitoring was conducted.

The influence of volatile anesthetic was tested in 6 patients. In 3 patients, BCR was suppressed by the administration of 1.25% isoflurane for 15 min (Fig. 9.5). Administration of nitrous oxide (60% inspired concentration) for 15 min reduced the BCR in 3 patients, and the response was completely abolished by muscle relaxant in 2 patients [6].
Preliminary results conducted in 50 patients with a lumbosacral tethered cord showed no clear correlation between BCR and postoperative sphincter control. The authors concluded that the complexity of sphincter innervation and segmental or suprasegmental control probably accounts for this discrepancy [17].

Up to now, close to 250 patients have been monitored using this method. In the last 100 patients, a train of four consecutive stimuli [7] was used rather than a double stimulus, providing even more robust responses. Some problems have been encountered in female patients in whom the stimulation method is not as robust as required; this problem needs particular attention from the technician.

The impetus to include intraoperative monitoring of sacral nervous structures came from concerns over optimizing care for children with cerebral palsy. These were successfully treated for their spasticity by performing selective dorsal rhizotomy; surgeons have always sought to minimize the side-effects of this procedure while maintaining its benefits (benefits being a reduction in muscle hypertonia, the side-effects being a partial or complete loss of sensory modalities). The first sacral dorsal roots have always been a target for rhizotomy in this procedure, but the S2 dorsal roots have become increasingly considered for rhizotomy. Not to treat the S2 dorsal roots is to leave potentially abnormal reflexive circuits that will continue to drive spasticity in the musculature of the leg. For this reason, the lesion zone was extended to include S2 dorsal roots, and the result was a greater reduction in spasticity as compared with children in whom the lesion was extended only to the S1 segment. Unfortunately, the extension to include S2 roots was also associated with disorders in micturition.
In one group of patients, before DRAP mapping was introduced, 24% experienced urinary retention (which was only transient in most children). Although most of these children had both the left and right S2 roots cut, 2 of the children had only one S2 root cut, and they also experienced retention. The selective dorsal rhizotomy procedure should be performed in young children who are certainly too young to assess sexual function; they are even too young to be completely confident that all symptomatic complaints regarding micturition or defecation and perineal sensation were being relayed. It was this concern over the preservation of genitourinary afferent function that led us to develop the technique of intraoperative neurophysiological identification of the sacral roots responsible for perineal sensation. In the first 31 children, neurophysiological identification of roots and rootlets carrying afferent activity from the penile or clitoral nerves led to zero micturition disturbances and allowed for rhizotomy of S2 roots or rootlets not carrying such afferent activity. Therefore, maximum possible antispastic effects could be achieved. The particularly important lesson we learned by doing very systematic recordings in S1–S2 and S3 roots bilaterally (and in some children also S4 and S5 roots) is that although most of our patients showed evidence of pudendal afferents in S2 and S3 roots bilaterally, about half of them also showed evidence of some afferent activity in S1 (either unilaterally or bilaterally). In slightly more than half of our patients, the root potentials were symmetrical, but the pudendal afferents of many were irregularly distributed across the sacral roots. In a few of the children the afferentactivity was confined to a single root (either S2 or S3 root). Since this may be the most important afferent contribution from the genitourinary area, even if only the S2 dorsal roots are checked for relevant afferent activity, they should not be sacrificed if they show any such activity. The finding of asymmetrical distribution of fibers that may be confined to a single root is consistent with the work of Junemann et al. [18], who found that the majority of motor fibers for the urethral sphincter are carried by a single variable lower sacral root. Therefore, for some patients undergoing an operation in the area of the cauda equina, the sacrifice of one single root may have dire functional consequences.
For other neurosurgical procedures in the lumbosacral spinal canal (e.g., the release of a tethered cord or the removal of a tumor), other authors have proposed, and in a small series have performed, the identification of motor and sensory nerve roots. This has been achieved through continuous monitoring of electromyographic activity in muscles innervated by lumbosacral segments, and through monitoring of tibial nerve somatosensory evoked potentials [19]. In addition, monitoring pudendal SEPs should provide very relevant complementary information, and, as we have demonstrated, should not be technically demanding if the structures are preserved preoperatively. Kothbauer et al. [19] claim that intraoperative recordings saved operating time by allowing the surgeon more rapid and decisive preparation than would be possible on an anatomical basis alone, and they also gave the impression that the procedures were safer. The recordings of spontaneous anal sphincter electromyographic activity during such operations have been described earlier [20]. To accomplish the two goals of neurophysiology (i.e., first, immediate identification of structures as functional nervous tissue and their distinction from other tissue; and second, continuous monitoring of the function of the relevant nervous structures), a battery of methods needs to be applied, and a whole set of structures needs to be assessed bilaterally. Therefore, both the lower sacral segments and sphincter muscles, and also the upper sacral segments and the lumbar segments, need to be included. Also, all these segments and several functional modalities need to be monitored more or less simultaneously. The appropriate setup for each surgical situation would need to be selected on the basis of anatomical and physiological considerations, and a compromise between the possible and the necessary would be sought.
Other authors have claimed that continuous EMG recording of bursts or trains of motor unit potentials or repetitive neurotonic discharges elicited by injury to the peripheral motor fibers have correlated with postoperative transient or permanent neurological deficit [21, 22] in the area of facial nerves. The predictive value of these “manipulation-evoked” discharges is only based on empirical data, but has been proposed to also be of value in the lumbosacral segments [19]. The electrophysiological identification of motor nerves is already an integral part of cranial nerve surgery [22] and should also provide a similar service in the region of the cauda equina.
Up to now, only recordings of DRAPs have been made in a large number of subjects (to identify sacral roots carrying genitourinary afferents), and the electrophysiological procedure decreased postoperative voiding disturbances [4, 5].
We propose, however, that the other intraoperative electrophysiological recordings of the sacral neuromuscular system that have been described (spinal SEP, CMAP of sphincter muscles, bulbocavernosus reflex recordings) should prove relevant in surgeries involving the sacral roots, the cauda equina, and the conus and should aid the surgeon in preventing inadvertent damage to these structures.
These other procedures have not, however, been performed in an adequate number of patients, and their relevance cannot yet be appraised. The most interesting question is whether monitoring of the bulbocavernosus reflex for conus and cauda equina surgery could, as we are proposing, replace and even improve upon separate monitoring of motor and sensory fibers of the lower sacral roots.
As for surgeries involving the spinal cord above the conus, the procedures of pudendal SSEPs, cortical SEPs, and (possibly) motor evoked potentials of the anal sphincter muscle might be interesting in some selected patient groups.
These would include groups in whom the preservation of sacral function may be particularly important (for instance, in scoliosis surgery in patients with advanced neuromuscular diseases who have heavily compromised motor function but no sacral dysfunction).
In other contexts, authors have argued that recordings from the anal sphincter cannot be taken as completely adequate information on the functional status of the urethral sphincter [18]. Since innervation of both sphincters originates from the same sacral segments (which also provide innervation for the detrusor), the monitoring of sphincter ani should generally mirror the function of relevant urethral structures.
As previously stated, the relatively limited experience with the monitoring of sacral structures cannot as yet prove that surgeries accompanied by such monitoring are easier and safer. For the time being, there is anecdotal evidence that difficult surgical decisions that have relied on the results of intraoperative neurophysiological measurements have not resulted in unexpected neurological deficits. Although the techniques described clearly provide the surgeon with additional information about nerve location and function, the value of these techniques must be further defined and documented. As Daube [23] suggests, it will be necessary to demonstrate that these techniques indeed save operative time, save anesthesia time, or—most importantly—improve outcomes.
It will be difficult to demonstrate this without doing a randomized study of patients who are undergoing surgery with and without such monitoring techniques.

The main purpose of intraoperative neurophysiologic monitoring is to reduce postoperative neurological deficits, but more recently it has become apparent that intraoperative recording of sensory evoked potentials and electromyographic (EMG) potentials can also aid the surgeon during many operations. The use of intraoperative monitoring of sensory evoked potentials and EMG potentials to reduce permanent postoperative deficits is based on the assumption that changes in recordable electrical responses occur as a result of injury, and that the injury is still reversible at the time of detection if proper surgical intervention occurs.

Monitoring of brain stem auditory evoked potentials (BAEPs) during operations in which the vestibulocochlear nerve (cranial nerve VIII) may be manipulated is now widespread, and the use of monitoring to reduce the incidence of hearing loss due to surgical manipulation of the vestibulocochlear nerve is steadily increasing. However, intraoperative monitoring of visual evoked potentials (VEPS), has not gained similar acceptance, mainly because of the technical problems involved in generating a suitable stimulus. Intraoperative recording of somatosensory evoked potentials (SSEPs) is valuable during aneurysm surgery and during other vascular operations, as well as during the removal of tumors in which the tumor itself or the surgical manipulation used to remove the tumor can be expected to affect brain structures that are involved in the somatosensory system and thus affect the generation of SSEPs.

The most frequent use of intraoperative monitoring of SSEPs is in operations involving the spinal cord, in which such monitoring is now well established. More recently, intraoperative transcranial stimulation of the motor cortex, by using either a high-voltage electrical stimulation or a strong magnetic field impulse in connection with recording of EMG potentials from the motor system, has been introduced to reduce intraoperative injuries to the spinal cord.

The recording of EMG responses from muscles innervated by different cranial nerves has been shown to be valuable in identifying cranial motor nerves during operations to remove tumors when the anatomy has been altered by the tumor or by previous operations; this is particularly true for operations to remove acoustic tumors and it has more recently been shown to be of value also in operations to remove large tumors of the skull base. It has been possible in a few types of operations to use electrophysiologic methods to guide the surgeon in the operation and to ensure before the operation has ended that the therapeutic goal of the operation has been achieved.

The objective of intraoperative monitoring of evoked potentials (BAEPs, SSEPs. and VEPs) when used for the purpose of reducing permanent postoperative neurological deficits is to detect changes that occur during the operation. This differs from the goal of the use of evoked potentials for diagnostic purposes, in which a deviation from a normal value is of interest. In intraoperative monitoring, normal values are of little interest; instead, it is important to obtain a baseline recording from an individual patient and then to compare the potentials that are recorded during the operation to that baseline recording. Such a baseline can usually be obtained after the patient has been anesthetized but before the operation has begun.

Monitoring of contractions of the facial muscles is performed during operations in the ccrebellopontine angle to help the surgeon locate the facial nerve (CN VII) when it is not identifiable visually. Possibly just as important, this technique makes it possible to determine which portions of an acoustic tumor do not contain any part of the facial nerve. This thus allows the surgeon to remove portions of a tumor without risk of injuring the facial nerve. Currently most such monitoring involves the surgeon using a handheld stimulating electrode, which carries short pulses of electrical current, to probe the surgical field to identify the facial nerve. Various methods are used to record the subsequent contractions of the facial musculature. The facial muscle contractions that are elicited by irritation and manipulation of the facial nerve are just as important as the contractions elicited by electrical stimulation of the facial nerve for the purpose of assessing injuries to the facial nerve.

Earlier, it was customary to have an assistant observe any movement of the face and then to communicate that fact to the surgeon. More recently, the recording of EMG potentials from the facial musculature and the recording of movements of the face using electronic sensors have also been used to verity that the facial nerve has been stimulated. The use of EMG recordings makes it possible to assess the degree of facial muscle contraction quantitatively, which was not possible when facial muscle activity was assessed by visual observation of movements of the face. The capability of making the recorded EMG potentials audible allows the surgeon to hear when the facial nerve has been stimulated and thus the surgeon has no need to rely on communication with an assistant. For this purpose, only a conventional audio amplifier and loudspeakers need to be connected to the output of the EMG amplifier. Some commercial equipment makes use of amplitude-sensing devices that elicit a tone signal when the EMG potentials reach a preset amplitude. However, making the (original) EMG signal audible is advantageous because it provides valuable information that is lost when such amplitudesensing devices are used. Although the audible EMG signal provides most of the information that is needed when monitoring the facial nerve, an oscillographic display of the recorded EMG potentials is also advantageous, in that it allows assessment of the amplitudes and latencies of the recorded EMG potentials. When the movements of the face are recorded by electronic sensors, the movements can be made to elicit a sound (horn), but an oscillographic display of the electrical signals produced by movement detectors has limited value.

Because the facial nerve is often split into several fascicles when a large acoustic tumor has displaced it, it is important that recordings be made from the entire face. If only portions of the facial musculature (e.g., the lower face or the upper face) are monitored, failure to locate all parts of the facial nerve could result in inadvertent removal of or injury to portions of the facial nerve: this would result in postoperative paralysis of part of the face. Usually the record EMG activity is performed between two electrodes, one placed on the forehead and one on the lower face (Fig.-1A), when monitoring facial function intraoperatively. In addition to recording activity from all muscles on the side of the face on which the electrodes have been placed, this particular arrangement of recording electrodes will also record contractions of the masseter and temporal muscles. These muscles are innervated by the motor portion of the trigeminal nerve (portio minor), and there is the possible risk of mistaking the fifth (motor) nerve for the seventh nerve when probing the cerebellopontine angle for the facial nerve in operations to remove large acoustic tumors that have progressed rostral to the trigeminal nerve. The EMG response to stimulation of the trigeminal nerve, recorded in the way illustrated in Fig-1A, however, can easily be distinguished from the response to stimulation of the facial nerve, because the latency of the recorded EMG signal differs in the two situations [1.5 ms and 5 to 6 ms. respectively,(Fig-1B). An alternative way to distinguish between the response to facial nerve stimulation and that to stimulation of the motor portion of the trigeminal nerve (CN V) is to record from the masseter muscle using a pair of electrodes connected to a separate differential EMG amplifier (Fig-1A). This recording will almost exclusively yield the response of the masseter muscle, and thus is a good indicator of stimulation of the motor portion of the trigeminal nerve.

Fig-1: A-Electrode placement for recording EMG potentials from facial muscles and a separate recording of the response from the masseter muscle. B- EMG potentials recorded from electrodes, placed as shown in A, elicited by electrical stimulation of the trigeminal and facial nerves in the CPA. C- Hand held stimulating electrodes for intracranial localization of the cranial nerves.

There are several advantages to using EMG recordings as a measure of muscle contraction rather than using a single sensor that records movements of the face. First, EMG potentials from practically all of the facial muscles can be recorded on a single channel [Fig-1A), whereas several sensors are needed to cover the entire face when movements are being recorded. Second. recording EMG potentials makes it possible to measure the latencies of the responses accurately, which enables one to differentiate between activation of the trigeminal nerve and activation of the facial nerve (Fig-1B). Third, the amplitude of the EMG response is roughly a measure of how many nerve fibers are functioning. and it therefore provides valuable quantitative information about the degree of injury to the facial nerve.

There are essentially two ways that electrical stimulation can be applied to the facial nerve: one is by using a bipolar stimulating electrode, and the other is by using a monopolar electrode. the difference being that the bipolar electrode has a higher degree of spatial specificity. However, because it is only the negative phase of the stimulus that is effective, only one of the two prongs of a bipolar stimulus electrode will stimulate the facial nerve effectively. Therefore, the orientation of a bipolar electrode is important. A monopolar. hand-held, stimulating electrode does not have these disadvantages and although it is less selective than a bipolar stimulating electrode it is preferable for intraoperative use (Fig-1C). A monopolar stimulating electrode is easy to use and its stimulating power is not affected by its orientation, as is the case for a bipolar stimulating electrode. By using a monopolar, handheld, stimulating electrode and having EMG potentials made audible, the surgeon can probe a large area of a tumor quickly and "map" the tumor to locate portions of the tumor where no part of the facial nerve is present so that it can be removed safely. The use of this technique can often reduce considerably the time required to remove the tumor because large portions of the tumor can be removed without risk of causing injury to the facial nerve. Later during removal of the tumor, when it becomes important to identify the facial nerve accurately so that injury to the nerve can be avoided, the same monopolar stimulator can be used and the area of tissue that it stimulates can be varied by varying the voltage that is applied through the electrode.

The electrical stimulation should consist of negative (rectangular) impulses of short duration (0.1 to 0.2 ms), and the stimulus strength should be no greater than necessary to produce a contraction. Some older types of stimulators make use of large current and some even make use of direct current. Such stimulators should not be used because of poor specificity and, particularly, because of the risk of injuring the nervous tissue with the electrical current used to stimulate the facial nerve.

Because shunting of electrical current from the stimulating probe can vary widely when the surgical field is wet compared to when it is relatively dry, it is advantageous to use a relatively constant-voltage stimulator rather than the more conventional constant-current type of stimulator. Constant-current stimulation in connection with the use of a "flush tip" stimulating electrode (i.e., an electrode that is insulated all the way to its tip) has been advocated by some investigators. When constant-voltage stimulation is used, the same amount of stimulus current will flow through a specific tissue (e.g., the facial nerve), regardless of how much shunting occurs. If constant-current stimulation is used, the same total current is delivered, but the amount of current that passes through a specific volume of tissue depends greatly on how much current is shunted away; in this case the stimulus strength depends heavily on whether the field is wet or dry.

When a facial nerve stimulator is used to identify regions of a tumor where no part of the facial nerve is present, the stimulus strength should be set so that it will activate the facial nerve if the nerve is within a small distance of the tip of a monopolar stimulating electrodes.

Audible monitoring (by means of a loudspeaker) of the EMG activity of the facial muscles that is evoked by mechanical stimulation of the facial nerve provides valuable feedback to the surgeon during the delicate resection of portions of an acoustic tumor that involve the facial nerve. Such continuous monitoring of facial EMG activity (without electrical stimulation) is of great value, particularly when the surgeon is removing a large tumor, parts of which may be firmly adherent to the facial nerve. If the facial nerve is being heated by electrocoagulation, or heated by the drilling of bone adjacent to the facial nerve, transient or sustained facial muscle activity will result. Although such monitoring of facial EMG activity is important in reducing the risk of permanent damage to the facial nerve, it must be pointed out that the facial nerve can be injured permanently from surgical manipulation without any EMG response being noted; thus, injury from sharp dissection will most likely not result in recordable EMG activity (or any movement of the face). For this reason, when the surgeon is dissecting near the facial nerve spontaneous EMG activity should not be relied upon for assurance that the facial nerve remains intact; in this situation, electrical stimulation of the facial nerve should be used frequently to identify the facial nerve so that the surgeon remains aware at all times of the exact location of the facial nerve.

In operations to remove tumors of the skull base, several cranial motor nerves are often in the operative field and are thus at risk of injury from surgical manipulation. This is particularly true in operations within the cavernous sinus, where the nerves that innervate the extraocular muscles [the oculomotor (CN III), trochlear (CN IV), and abducens (CN VI) nerves] may be difficult to identify visually or may be displaced by the tumor. Recording EMG potentials from the extraocular muscles while the surgical field is being probed with a hand-held stimulating electrode similar to that used for stimulating the facial nerve (Fig-1C) can aid the surgeon in locating the respective nerves. EMG potentials can easily be recorded from these muscles via needle electrodes inserted percutaneously into the respective muscle (Fig-2). The potentials recorded from the extraocular muscles in response to electrical stimulation of the respective nerves are easy to distinguish (Fig-3A).

More recently, surface electrodes for recording EMG activity from the extraocular muscles have been developed. Facial nerve function should also be monitored in these operations, using the methods just described. Continuous recording of EMG potentials from these muscles is also important, because injury to the respective nerves from mechanical manipulation and from heat during electrocoagulation will often result in transient or sustained EMG activity, as was described for the facial nerve. Thus, such activity can be an important aid in preserving these nerves.

Fig-2: A-Electrode placement for recording from facial, extraocular muscles and the tongue. The reference electrodes are all placed on the forehead on the opposite side, to avoid recording from the facial muscles at the same time. B-Electrode placement with intraoperative recordings from extraocular and facial muscles. BAEPs and VEPs included.

Fig-3: A- EMG potentials recorded from the extraocular and facial muscles in response to intracranial electrical stimulation of the respective cranial nerves, using the electrode arrangement as seen in Fig-2. B-EMG potentials from the tongue in response to stimulation of the hypoglossal nerve.

Identification of the hypoglossal nerve (CN XII) can be facilitated by recording EMG potentials from the tongue (Figs-2A and 3B), and monitoring of the accessory nerve (CN XI) can conveniently be done by placing pairs of needle EMG electrodes in the trapezius muscle (Fig-2A). The motor portions of the glossopharyngeal (CN IX) and vagus (CN X) nerves can be monitored by stimulating the respective nerves electrically and recording EMG activity from the muscles that these nerves innervate in a way similar to that just described for the facial nerve and the nerves that innervate the extraocular muscles. A pair of needle electrodes placed in the soft palate will record the EMG response to stimulation of the glossopharyngeal nerve and electrodes placed in the supraglottic region are suitable for recording of the EMG response from laryngeal muscles that are innervated by the recurrent nerve of the vagus nerve. Electrodes placed on the endotracheal tube can record surface EMG potentials from laryngeal muscles. A balloon placed on the tip of an endotracheal tube as a pressure recording device has been used to record contractions of the laryngeal muscles for monitoring of the recurrent laryngeal nerve. This technique could be useful in monitoring the more central portions of the vagus nerve.

One should be aware when monitoring the glossopharyngeal, vagus, and accessory nerves using electrical stimulation that there are risks involved. For example, a supramaxial stimulation of the accessory nerve may result in so strong a muscle contraction that dislocation of joints or physical injury to muscles and tendons may result. Electrical stimulation of the glossopharyngeal and vagus nerves may cause cardiovascular effects and should therefore be done cautiously.

Microvascular decompression to relieve hemifacial spasm is one of only a few operations in which intraoperative neurophysiologic monitoring can aid the surgeon in achieving the therapeutic goal of the operation. It is generally accepted that hemifacial spasm is caused by vascular compression of the facial nerve as it exits the brain stem. and that microvascular decompression of the root exit zone of the facial nerve is the most effective treatment of this disorder. However, it is not always obvious from an exploration of the root exit zone of the facial nerve which of several vessels is causing the spasm, and a certain (small) number of patients who have undergone this operation have experienced spasm postoperatively. Some of these patients had to be reoperated upon, depending on the severity of the spasm.

In studies of the pathophysiology of hemifacial spasm, it was found that an abnormal muscle response that seems to be characteristic of the disorder disappears instantaneously when the offending blood vessel is moved off the intracranial portion of the facial nerve (Fig-4). This abnormal muscle response, which has a latency of about 10 ms is seen when one branch of the facial nerve is stimulated electrically and recordings are made from muscles that are innervated by other branches of the facial nerve. By monitoring this abnormal muscle response intraoperatively, it is possible to identify the offending blood vessel and to ensure that the nerve has been fully decompressed by watching for the cessation of the abnormal response (Fig.4B) When using this method it was found that even veins can cause hemifacial spasm and that in many cases there was more than one blood vessel compressing the facial nerve. There are reasons to assume that at least some of the patients who experienced only partial relief from their symptoms before this type of monitoring was introduced did so because more than one vessel was affecting the facial nerve and only one of the offending vessels was moved off the facial nerve during the operation.

Intraoperative monitoring of BAEPs is commonly performed to reduce the risk of hearing loss as a result of intraoperative manipulation of the vestibulocochlear nerve in operations in the cerebellopontine angle. This is important in operations on acoustic tumors, in which hearing preservation is anticipated, as well as in microvascular decompression operations on cranial nerves and in other operations in the cerebellopontine angle. BAEPs are commonly recorded between electrodes placed on the vertex and on the earlobe (or mastoid) of the ear to which the sound is applied. BAEPs are best elicited by click sounds presented at a rate of 20 to 40 pulses/s (pps) at intensities of 100 to 110 peak equivalent sound pressure (Pe SPL), The normal BAEPs are characterized by 5 to 7 vertex-positive peaks that are generated as the different structures of the ascending auditory pathway are successively activated (Fig.-5). Because the BAEPs are generated by fiber tracts and nuclei of the ascending auditory pathway in the brain stem, the vestibulocochlear nerve, the cochlear nuclei, and the lateral lemniscus being the most important generators of BAEPS-recording of these potentials is not only useful for detecting injury to the vestibulocochlear nerve but may also be of value in operations in which the brain stem is being manipulated or when circulation to the brain stem may be compromised. The nuclei of the ascending auditory pathway are sensitive to manipulations of the brain stem, and there are indications that BAEPs may be more sensitive in detecting such effects than are changes in heart rate and blood pressure. A change in the latency of peak V while that of peak III remains unchanged (increased III - V interpeak latency) indicates an effect from surgical manipulation on structures located in the region of the superior olivary complex on either side or on the lateral lemniscus and its nucleus on the side contralateral to the side on which the BAEPs are being elicited (tumor side) (Fig-6). It is therefore more valuable to monitor BAEPs during other operations in which manipulation of the brain stem may occur, such as the removal of large acoustic tumors or other tumors of the cerebellopontine angle.
Fig-5: Neural generators of BAEPs. DCN: dorsal cochlear nucleus, VCN: ventral cochlear nucleus. SO: superior olivary complex. LL: lateral lemniscus. IC: inferior colliculus. MG: medial geniculate.

Fig-6: Changes of latencies and amplitudes of peaks III and V of BAEPs as a function of time during surgery. BAEPs were elicited by stimulating the opposite ear relative to the tumor location.

SSEPs are important in monitoring sensory conduction in the spinal cord. SSEPs elicited by stimulation of the median nerve and recorded from the contralateral parietal region of the scalp (C3 or C5) using a noncephalic reference are characterized by a series of positive and negative peaks (Fig-7). P₉, P₁₁, and P_I4 are short-latency, positive peaks that are generated at the level of the brachial plexus (P9). spinal entry (P11). and termination of the dorsal column in the dorsal column nuclei (P_I4). The bilateral N₁₈ is generated in brain stem nuclei, such as the superior colliculus. whereas the contralateral N₂₀ is assumed to be generated in the primary cortex. The waveform of the SSEPs and the presence of certain components depend on the recording sites (Fig-7). For monitoring the spinal cord, SSEPs are elicited by electrical stimulation of sensory nerves on the leg (peroneal or posterior tibial nerve).

Only when the cervical spine is considered is it appropriate to use SSEPs elicited by stimulation of the upper limb (median nerve at the wrist). The response to stimulation of the lower limb is recorded from electrodes placed on the scalp, vertex to a midline front reference or vertex to a noncephalic reference. The different components appear with longer latencies than those of SSEPs elicited from the median nerve. and the pattern of the peaks is more complex (Fig-8). One reason that lower limb SSEPs are more complex than those elicited from the upper limbs is related to the fact that ascending neural activity elicited by stimulating lower limbs travels in two separate fiber tracts in the spinal cord. Only part of the sensory information is relayed in the dorsal column nuclei (nucleus gracilis).

Fig-7: SSEPs in response to electrical stimulation of the median nerve. A- The thick line is a record from the contralateral parietal region with a noncephalic reference. B- Records from prerolandic region with a noncephalic reference.

Fig-8: SSEPs in response to stimulation of the left posterior tibial nerve at the ankle. A-Records from a midfrontal (pF_z). B- Record from midpaietal (P_z) with a noncephalic reference on the shoulder. C- Difference between A and B.

Neural activity that travels in the dorsal column is mainly elicited by skin receptors. Fast-conducting afferents that conduct activity elicited by stretch receptors, group Ia and II afferents from muscle spindles, and tendon organs travel in a spinothalamic pathway in the dorsal lateral funiculus of the spinal cord and synapse in the nucleus gracilis, after which they join other afferents in the medial lemniscus traveling toward the thalamic relay nuclei. The slow cutaneous afferents from the lower limbs that travel in the dorsal column are relayed in the dorsal column nuclei (gracilis nucleus). These afferents have a large range of conduction velocities, which causes a temporal dispersion in the elicited activity, which is the cause of the low amplitude of the early response from stimulation of lower limbs. This makes the SSEPs from lower limbs qualitatively different from the SSEPs elicited by stimulation of upper limbs and, together with the longer distance from the location of the stimulation to the brain stem structures, explains why the far field SSEP responses to electrical stimulation of lower limbs are less well defined than the SSEPs elicited by stimulation of the upper limbs, where all somatic afferents trawl in the dorsal column and are all relayed in the dorsal column nuclei (cuneate nucleus). Although recording using a noncephalic reference is appropriate for identifying the neural generators of SSEPs, the unfavorable signal-to-noise ratio in such recordings has made it more common to place the reference electrode on the scalp when SSEPs are used for intraoperative monitoring. This reduces the pick-up of electrical interference signals. When the spinal cord is to be monitored, all components of SSEPs that originate from structures that are rostral to the location where injury may occur can be utilized for detecting injuries. However, late components of the SSEPs are affected by anesthesia, and it would therefore be advantageous to use early components such as the P₁₄ in upper limb SSEPs. Unfortunately, the early components of lower limb SSEPs are less well-defined and usually cannot be used for intraoperative monitoring.

Because the blood supply to the portion of the spinal cord that comprises the ascending somatosensory pathway is different from that of the descending motor tracts, there is a possibility that the motor system can be injured without any noticeable change occurring in SSEPs. Thus, it seems possible that severe injury could go unnoticed when only SSEPs are monitored. Although it has been disputed whether this is in fact a real risk, there is a need to be able to monitor both motor and sensory systems during operations in which the spinal cord is at risk. Although traditional techniques can be used to monitor the somatosensory system intraoperatively, there are considerable technical obstacles in eliciting motor responses upon stimulation of the motor cortex. Therefore, such monitoring of the descending motor tracts is not done routinely. It has, however, been shown that it is indeed possible to elicit motor responses by electrical and magnetic transcranial stimulation of the cortex, thus a prerequisite for developing routine methods for intraoperative monitoring of motor tracts.

Intraoperative monitoring of SSEPs is valuable as an indicator of decreased cerebral perfusion in regions of the brain on which the generation of more long-latency components of the SSEPs depend. The development of these methods, which are now in routine use, had been pioneered by Symon et. al, who made use of recordings of SSEPs elicited by electrical stimulation of the median nerve at the wrist. The use of this method is based on the finding that there is a rather close relationship between the disappearance of electrical activity and a decrease in the cerebral blood flow to 15 to 18 ml/100 g per min (or below), and there are changes in the late components of the SSEPs that occur before the perfusion reaches these low levels. SSEPs are therefore valuable in estimating changes in cerebral blood flow.

The most useful parameter of SSEPs as an indicator of a decrease in cerebral blood flow is the central conduction time, which is the time difference between the occurrence of the components of the SSEPs that can be recorded at the neck (P₁₄) and the N₂₀ component that is recorded at the contralateral parietal skull (C3-C5) (Fig-9). Central conduction time is not affected by changes in peripheral neural conduction or by age, and it has been shown to correlate with cerebral blood flow when blood flow is reduced below a certain value.

Fig-9: Measures of central conduction time from recordings of the SSEPs that are elicited by electrical stimulation of the median nerve at the wrist. All recordings were done with a noncephalic reference. A- Parietal scalp. B- Frontal scalp. C- Spinal C6 spine.

During operations in which the optic nerve or the optic tract is being manipulated it would seem to be beneficial to monitor VEPS. However, the results of such monitoring have been generally disappointing because the changes in the recorded potentials correlate poorly with postoperative changes in vision. This is most likely due to limitations inherent in the techniques currently available for intraoperative stimulation of the visual system, and perhaps to inadequate knowledge of how to interpret the changes in the VEPs that may occur during surgical manipulations of the optic nerve or optic tract: however, essentially there are no practical problems involved in recording VEPs intraoperatively. At present, the only practical type of visual stimulation that can be used intraoperatively is the "flash" type. It has been shown that VEPs elicited by a changing pattern (pattern reversal-checkerboard pattern) are much more useful diagnostically than VEPs recorded in response to flash stimulation, however, eliciting VEPs by pattern reversal technique requires that a pattern be focused on the retina, which is not possible to accomplish intraoperatively.

Although recordings of BAEPs are not noticeably affected by any common anesthetic regimen using inhalation anesthetics. barbiturates. and other intravenous anesthetics, intraoperative monitoring of cranial motor nerves cannot be done if the patient is paralyzed, because such monitoring depends on recording muscle responses by EMG technique. Components of the upper limb SSEPs that occur with latencies longer than 16 ms are usually affected by general surgical anesthesia.

The most commonly used anesthetic regimen for neurosurgical operations involves giving a strong narcotic, such as fentanyl for analgesia together with an inhalation agent, such as nitrous oxide, and small amounts of halogenated agents ("balanced anesthesia"). Because the patient must be kept from moving, he or she must be paralyzed when such a regimen is used. Normally some form of a muscle endplate blocker (pancuronium, vecuronium. etc.) is used for this purpose. Therefore, balanced anesthesia makes it impossible to record EMG potentials because of muscle relaxation. However, intraoperative neurophysiologic monitoring is fast becoming a regular component of the surgical arena, and it is now common to adjust the anesthesia regimen to the requirements of the specific type of monitoring to be done. For instance, the requirement of being able to record EMG potentials has resulted in the use of inhalation anesthesia throughout the operation. possibly with the addition of a small amount of a narcotic agent and benzodiazepines such as midazolam. This type of anesthesia has been used for many years without any noticeable difficulties or complications and is now in common use when intraoperative monitoring of muscle activity is performed. However, while such an anesthesia regimen has no noticeable effect on recording EMG potentials or BAEPs and short-latency SSEPs. it is likely to suppress later components of SSEPs and it greatly suppresses motor evoked potentials. Some anesthetic agents such a propofol, that can be administered intravenously have less suppressive effect on cortical responses and are thus being used during operations in which several different kinds of evoked potentials and EMG responses are to be monitored.

Patients in whom intraoperative neurophysiologic monitoring of evoked potentials is to be performed should have the systems that are to be monitored quantitatively evaluated preoperatively. For example, if a patient's BAEPs are to be monitored, his or her hearing status should be evaluated preoperatively. Testing should include at least a pure tone audiogram and a determination of speech discrimination scores, and the patient's ear canals should be checked for obstruction (from cerumen. etc.). If the patient has no hearing or if it is not possible to obtain an interpretable BAEP before the operation, it will not be possible to obtain one during the operation. If, on the other hand, an interpretable BAEP can be obtained before the operation but not intraoperatively. the cause is most likely technical: such problems then must be corrected. Similarly, if SSEPs are to be recorded intraoperatively, a recording should be performed preoperatively to ascertain that the patient has normal SSEPs or to establish the degree of abnormality so that it can be taken into consideration before the intraoperative recordings are made. Factors such as neuropathies that may affect neural conduction should be ruled out or assessed quantitatively, if possible. If the extraocular museles are to be monitored, their function should be evaluated preoperatively by state-of-the-art methods. When facial EMG responses are to be monitored, the function of the facial musculature should be evaluated preoperatively. Preoperative evaluation of sensory and motor systems that may be at risk during an operation is also essential, because this, in connection with similar tests done postoperatively, the only way that deficits from the operation can be assessed quantitatively.

Intraoperative neurophysiologic monitoring of evoked potentials has been introduced for use in neurosurgical operations for long time, and it is therefore natural that the method has been viewed with skepticism in the early period of its implementation, and suffered from a demand for proof of the benefits. As with several other procedures allied to such operations, it has generally been difficult to design studies to provide quantitative estimates of the benefits in terms of reduced postoperative complications. This is largely because many surgeons believe that intraoperative monitoring is valuable in reducing postoperative deficits and therefore will not allow random selection of patients to be monitored. This makes it impossible to study the efficacy of such techniques by a double-blind methodology.

Comparing complications before and after the introduction of intraoperative monitoring thus seems to be the only practical way to assess the value of intraoperative monitoring: however, the results of such evaluations are influenced by any changes in the operative technique introduced at or after the institution of monitoring. Despite this complication. comparisons have been made between the rate of complications (such as facial palsy) of surgical procedures (such as acoustic tumor removal) before and after the introduction of intracranial monitoring of cranial nerve function. Such studies have shown a significant decrease in complication rate after the introduction of intraoperative monitoring.

It is generally accepted now that intraoperative monitoring of facial nerve function during operations on acoustic tumors is of value in preserving the facial nerve. A study of a less frequently performed operation, that to relieve hemifacial spasm, showed that the efficacy of the operation was higher after intraoperative monitoring was introduced. Further, the number of patients who needed to be reoperated upon because of recurrent or unrelieved spasm decreased from about 15 percent to almost zero. Finally, the frequency of hearing loss as a complication of microvascular decompression operations in the cerebellopontine angle decreased radically after the introduction of intraoperative monitoring of BAEPs during such operations.

Because intraoperative neurophysiologic monitoring can many times identify exactly which step in an operation that caused an injury is likely to result in a permanent neurologic deficit, it has contributed to the development of better and safer operating techniques. When evaluating the benefits of intraoperative neurophysiologic monitoring it must be pointed out that the benefit from intraoperative neurophysiologic monitoring depends on the level of experience of the surgeon. Thus a very experienced surgeon will not have the same degree of benefit from this technique as might a less experienced surgeon. There are several advantages of the use of intraoperative neurophysiologic monitoring, but they are difficult to measure quantitatively; nevertheless, they are great enough to lead most surgeons who have operated with the aid of such monitoring to demand that it continue.