Intraoperative neurophysiology and methodologies used to monitor the functional integrity of the motor system

2.1.1

Penfield’s time

When discussing the use of intraoperative electrical stimulation of the upper motoneurons in humans, it is essential to mention Wilder Penfield (1891–1976). His publication with Edwin Boldrey in the journal Brain summarized his work on the motor and somatosensory system’s organization of the cerebral cortex in humans, as explored with intraoperative electrical stimulation. Penfield’s systematic exploration of the brain with intraoperative stimulation laid the foundation for the field of intraoperative neurophysiology (ION).

After Penfield—except for the work done to intraoperatively localize epileptic foci—almost half a century passed without any significant developments in ION exploration of the nervous system. However, a transformation took place during the 1950s and 1960s when clinical neurophysiology branched into three subfields: electromyography, electroencephalography (EEG), and evoked potentials. These developments helped to widen the doors of the operating room to the use of these methods intraoperatively.

By the late 1970s, somatosensory-evoked potentials (SEPs) became routinely used to intraoperatively assess the functional integrity of the somatosensory system in the spinal cord during surgical correction for scoliosis . The same SEPs data were also routinely extrapolated to assess the functional integrity of the upper motor neuron tracts; however, as data mounted, this approach proved unreliable: (1) it provided false results when SEPs were found to be present despite postoperative motor deficits ; (2) it provided unreliable (low-quality) or un-monitorable (complete absence) SEPs in patients in whom certain pathologies affected the somatosensory system; and (3) because dorsal myelotomy often destroyed the dorsal column’s (DC) integrity in patients undergoing surgery for intramedullary spinal cord tumors, the ability to monitor SEPs was immediately nullified .

Because of these difficulties, ION was forced to search for more reliable methods to assess the motor system’s functional integrity. Initial attempts to monitor motor tracts in the spinal cord were made in both Japan and the United States. These attempts focused on two neurophysiological techniques: spinal-cord-to-spinal-cord recording and spinal-cord-to-muscle/peripheral-nerve recording.

2.1.2

Spinal cord to spinal cord

This technique operates with nonselective electrical stimulation of the spinal cord and with nonselective recordings of elicited potentials from the spinal cord. It is used to record signals from the spinal cord regardless of the direction of propagation of the action potentials (either ascending, descending, or ortho/antidromic). The type of action potential recorded depends on the position of the stimulating and recording electrodes and the direction of the traveling waves through the spinal cord with regard to the natural direction of the conducting pathways .

The evoked potentials recorded from the spinal cord using this technique are the electrical sum of activity from multiple pathways. Because of the different conduction properties of the various spinal cord pathways, the recorded potentials can show two distinctive wave morphologies. It has been speculated that one of these waves represents transmission in the DCs and the other by the corticospinal tract (CST).

This method can evaluate the integrity of ascending and descending, and probably propriospinal pathways, within the spinal cord. However, specific information about the DC or CST cannot be obtained with this method. Critical reports could not confirm the value of the spinal-cord-to-spinal-cord technique in monitoring motor pathways during surgery for intramedullary spinal cord tumors.

2.1.3

Spinal cord to peripheral nerve (muscle)

This technique operates with nonselective stimulation of the spinal cord and selective recordings from the peripheral nerves or muscles. Recordings from the muscle and peripheral nerves presume that after the electrical stimulation of the spinal cord, α-motoneurons are activated only by the CST tract. Therefore compound muscle action potentials (CMAPs) in the limb muscles or electrical activity in the peripheral nerves should be generated by CST stimulation. Unfortunately, α-motoneurons can also be activated by any of the multiple descending tracts within the spinal cord after diffuse electrical stimulation of the spinal cord and/or by antidromically activated DCs and their segmental branches that mediate the H-reflex . Electrical activity recorded from mixed peripheral nerves is a combination of α-motoneuron discharges initiated by the CST and other descending tracts. Because the sensory component of mixed peripheral nerves is a physical continuation of the DCs, part of the electrical activity recorded from mixed peripheral nerves after stimulation of the spinal cord arises from the antidromically activated DCs that convey traveling waves to the peripheral nerves . Collision studies have challenged the widely accepted presumption that potentials recorded from peripheral nerves in the lower extremities after stimulation of the spinal cord are generated by the CST . Therefore there is convincing evidence that selective recording of the electrical activity from peripheral nerves elicited by nonselective electrical stimulation of the spinal cord does not arise from the CST . Additional evidence concerning the inaccuracy of monitoring the motor pathways through potentials recorded from peripheral nerves is provided in a recent paper by Minahan et al. This paper describes two patients with postoperative paraplegia in spite of the preservation of these potentials . Recently, this problem has been resolved by using a double train–stimulation technique but only after the microstimulation of the surgically exposed spinal cord .

It is fair to say that both of the techniques described can grossly monitor the functional integrity of multiple pathways inside the spinal cord without being specific for any of them. In other words, these methods can indicate that certain lesions to the spinal cord have occurred, but they lack the ability to provide specific information as to which of the spinal cord pathways have been damaged. This methodology may be useful in orthopedic surgical procedures and other surgeries where lesioning of the nervous tissue within the spinal cord is diffuse in nature and where all pathways are usually affected. An exception to this phenomenon involves vascular lesions of the spinal cord where selective lesioning of the anterolateral columns can occur.

Unfortunately, this nonselective evaluation of multiple pathways is not sufficient during surgery of the spinal cord, during which the DCs can be independently damaged from the anterior and lateral columns . Furthermore, these two techniques (for methodological reasons) cannot evaluate the functional integrity of the CST from the motor cortex to the upper cervical spinal cord. Therefore supratentorial, brainstem, foramen magnum, and upper cervical spinal cord surgeries cannot be monitored using these techniques. This is also the case in procedures involving the clipping of an intracerebral aneurysm, where the perforating branches for the CST tract in the internal capsule can be selectively damaged while leaving the lemniscal pathways intact. This results in a so-called pure motor hemiplegia (i.e., the patient is postoperatively hemiplegic while the sensory system is intact and SEPs are present) (see Chapter 14 : Clinical and neurophysiologic features of the pure motor deficit syndrome caused by selective upper motor neuron lesion: contribution to a new neurological entity). Since it requires the motor cortex to be surgically exposed, Penfield’s technique may not be used for monitoring motor tracts within the spinal cord.

2.2.1

Single-pulse stimulation technique

A single-pulse stimulating technique involves a single electrical stimulus applied transcranially or over the exposed motor cortex, while the descending volley of the CST is recorded over the spinal cord as a direct wave (D-wave).

2.2.2

Multipulse stimulation technique

A multipulse stimulating technique involves a short train of five to seven electrical stimuli applied transcranially or over the exposed motor cortex, while muscle motor-evoked potentials (MEPs) from limb muscles in the form of CMAPs are recorded ( Fig. 2.1 ) . (This latter technique differs essentially from the Penfield’s technique in which it calls for only five to seven stimuli with a stimulating rate of up to 2 Hz.) Penfield’s technique calls for continuous stimulation over a period of a few seconds with a frequency of stimulation of 50–60 Hz, and only in the cases when the motor cortex is surgically exposed. Furthermore, at such frequencies and train durations, seizures are easily induced.

2.3.1

Electrode montage over the scalp for eliciting motor-evoked potentials (for single and multipulse stimulation techniques)

The electrode placement on the skull is based on the international 10–20 EEG system ( Fig. 2.1A ). Note that, instead of CZ, the CZ electrode is placed 1 cm behind the typical CZ point. Some laboratories have used 2 cm in front of C3 or C4 (Z. Rodi, personal communication). For transcranial stimulation, corkscrew-like electrodes (Corkscrew electrodes, Nicolet, Madison, WI) are preferable because of their secure placement and low impedance (usually 1 kΩ). Alternatively, an EEG needle electrode may be used. We do not recommend the use of EEG cup electrodes fixed with collodion since they are impractical and their placement is time-consuming. The only exception is for young children in whom the fontanel still exists. Since the CS electrodes could penetrate the fontanel during placement, the use of EEG cup electrodes is suggested.

The skull presents a barrier of high impedance to the electrode current applied transcranially; therefore we cannot completely control the spread of electrical current when it is applied. For this reason, various combinations of electrode montages may need to be explored to obtain an optimal response. The standard montage is C3/C4 for eliciting muscle MEPs in the upper extremities and C1/C2 for eliciting muscle MEPs in the lower extremities. With sufficient intensity of stimulation at C1/C2, MEPs are preferentially elicited in the right limb muscles, while stimulation at C2/C1 elicits muscle MEPs in the left limb muscles.

With stronger electrical stimulation the current will penetrate the brain more deeply, stimulating the CST at a different depth from the motor cortex ( Fig. 2.2 ). On the basis of measurements of the D-wave latency, it has been postulated that there are three favorable points that are susceptible to depolarization of the CST: cortex/subcortex (weak electrical stimulation), internal capsule (moderate electrical stimulation), and brainstem/foramen magnum (strong electrical stimulation). The selectivity of stimulation is possible at the level of the cortex (subcortex). Therefore only the application of relatively weak electrical stimuli to the cortex is selective, and it activates only a small portion of the CST fibers (e.g., activating only one extremity) or only one CST. It is important to remember that during electrical stimulation of the motor cortex, the anode is preferentially the stimulating electrode. With increasing intensity of the current the cathode becomes the stimulating electrode as well.

As an example, stimulation with the C3+/C4− will selectively activate muscles of the right arm. When stimulation intensity is increased, the cathode (C4−) becomes the stimulating electrode as well, resulting in the stimulation of the left arm. Finally, when current intensity becomes strong enough to penetrate to the internal capsule more caudally, all four extremity muscles can be activated. For anatomical reasons (deep position of the leg motor area in the interhemispheric fissure), more intense current is usually needed to obtain MEPs in the lower extremities. It is especially difficult to obtain them separately without also activating the upper extremities. Our observation has been that it can be done in certain patients, especially when using the CZ/6 cm in front montage (see Fig. 2.1 ).

By their anatomical location, recording electrodes in the limb muscles can indicate which fibers of the CST are activated predominantly (left or right, fibers for upper or lower extremities). If one would like to activate left and right CST simultaneously to obtain D-wave recordings, weak electrical stimulation should be avoided and a moderate intensity should be used. In Fig. 2.3 , it is obvious that weak electrical stimulation activates fibers of the CST for the left upper extremities only. This can result in activation of only one CST while not affecting the other CST. Therefore the intensity of electrical stimulation for eliciting a D-wave should be determined by simultaneous recordings of MEPs from limb muscles (indicating which fibers of the CST have been predominantly activated) or only moderate intensities of electrical current for eliciting D-waves should be used.

The moderate intensity of electrical current will activate both CSTs at the level of the internal capsule. If muscle MEP waves have not been simultaneously recorded with D-waves, the following guidelines should be followed: increase the intensity of the stimulation until D-waves do not increase in amplitude ( Fig. 2.2 , the third trace from the top). This is a sign that most of the fast conducting neurons of CST from the left and right CST have been activated.

The neurophysiological mechanism for eliciting MEPs by stimulating the motor cortex in patients under the influence of anesthetics is different from the mechanism in the awake subject. In the latter, electrical current stimulates the body of the motor neuron transynaptically over the chain of vertically oriented excitatory neurons, resulting in I-waves (indirect activation of the motoneurons). At the same time, electrical current activates axons of the cortical motoneurons, directly generating D-waves . In anesthetized patients, anesthetics block the synapses of the vertically oriented excitatory chains of neurons terminating on the cortical motoneuron’s body. Therefore only the D-wave is generated after electrical stimulation of the motor cortex . Patients with idiopathic scoliosis are an exception. In this group, abundant I-waves can be recorded ( Fig. 2.2 ). We believe that this is one of the neurogenic markers of the disease present in these patients . Furthermore, it has been shown that a frontally oriented cathode preferentially generates I-waves because at this stimulating montage, cortico-cortical projections of vertically oriented interneurons are optimally activated. With the cathode in the lateral position, this is not the case ( Fig. 2.4 ).