Neurophysiological identification of long sensory and motor tracts within the spinal cord

12.2.1

Neurophysiological generators of somatosensory evoked potentials in the spinal cord

On the surface of the SC, conducted and segmental evoked potentials can be easily distinguished after stimulation of peripheral nerves or roots .

Conducted spinal evoked potentials (traveling waves) recorded from the dorsal surface of the SC consist primarily of negative waves reflecting the compound action potentials traveling in the DC fibers. Their amplitudes diminish from caudal to rostral recording sites due to dispersion of the afferent volleys caused by different conduction velocities among various fibers. However they are not significantly reduced at higher stimulation frequencies. When recorded from the ventral SC surface their polarity is unchanged, suggesting that a generator is oriented along the longitudinal axis of the cord, with the negative pole caudally and the positive pole cranially .

Segmental potentials (stationary waves) represent the summated activity of cells of the SC’s gray matter (dorsal horn activity) with intermixed rootlet activity. They have a maximum amplitude at the levels corresponding to the cord entry of the stimulated nerve fibers and decrease caudally and cranially . Following the electrical stimulus, the afferent compound action potential of the dorsal root fibers is recorded as a fast, predominantly positive wave (P1) on the dorsal surface of the exposed SC. This potential is predominantly generated by fast conducting Aβ and Aγ fibers and its amplitude is not reduced by high-frequency stimulation . A negative wave (N1) follows which is representing postsynaptic potentials generated in the dorsal horn neurons of the SC. This wave has a longer duration than the traveling one due to repetitive firing and relaying of neurons in the dorsal horns. Furthermore this wave is reduced by high-frequency stimulation. A low-voltage, slow-positive wave (P2) which reflects depolarization of afferent fiber terminals follows . When recorded from the ventral cord surface, segmental potentials invert polarity since their generator dipoles are placed in the sagittal plane . After stimulation of median/ulnar or tibial nerves, the segmental responses are P9/N13 or P17/N22, respectively .

Intraoperative recordings from the exposed surface of the human SC were first reported during surgical ablative procedures for relief of chronic pain . Silver ball or stainless steel disc electrodes were used to record spinal responses after peripheral nerve stimulation. Segmental responses were recorded rostral and caudal to identify the dorsal root entry zone (DREZ) for ablative procedures. Jeanmonod et al. also reported intraoperative recordings of conducted potentials with the ball electrode on the DCs rostral to the surgical site. These recordings were used for monitoring in order to avoid injury of DCs, however not for mapping purposes .

12.2.2

Measuring the amplitude gradient of spinal SEP via miniature multielectrode grid electrodes

This method measures the amplitude gradient of the SEP recorded using a miniature multicontact electrode over the surgically exposed SC after stimulation of the peripheral median or tibial nerves. A miniature multielectrode grid, consisting of eight parallel stainless steel wires (numbered 1–8), diameter 76 μm and spaced 1 mm apart, is placed on the supposed DC . The recording wires are adjusted parallel to the long axis of the SC, with a reference needle electrode placed in a nearby muscle. Stimulation of the right and left tibial or median nerve is applied with upto 40 mA stimulation intensity with 0.2 ms pulse duration and 13.3 Hz stimulation repetition rate. Recordings are performed via the multielectrode grid by two sets of 100–200 sweeps averaged from each of the eight parallel recording surfaces . Suggested filter settings are 50–1700 Hz and epoch length around 20 ms. The midline is determined as the point lying between two maximum amplitudes of the tibial SEP traveling waves or median nerve SEP stationary waves ( Fig. 12.1 ) .

In an original series, Kržan recorded reproducible spinal SEPs in 55 of the 65 patients . In patients in whom anatomical factors prevent recordings, the responses could be recorded caudally to the site of pathology. The recordings from each of the eight parallel electrode surfaces resembled conducted spinal SEPs previously detected with a silver ball electrode or conventional epidural electrodes . They consisted of multispike activity lasting about 10 ms with mean amplitudes ranging from 0.7 to 43 μV. An amplitude gradient of SEPs across different electrode recording sites was observed. For tibial nerve SEPs, the maximum amplitude was toward the midline and decreased toward the DREZ. The neurophysiological or functional midline was determined to lie between the two recording sites with highest SEP amplitudes after stimulation of either left or right tibial nerve. In patients with cervical lesions, they also recorded spinal SEPs after median nerve stimulation. The recorded potentials consisted mainly of segmental responses (stationary waves). An amplitude gradient across eight recording sites was also observed, with highest amplitudes of SEPs laterally, close to the DREZ. Lower amplitudes were observed toward the dorsal midline contrary to recorded SEPs following tibial nerve stimulation ( Fig. 12.1 ). Median nerve stimulated segmental potentials have the maximum amplitude lateral due to the lateral position of the dorsal horn (gray matter); tibial nerve SC conducted SEP have the highest amplitude medial as they are conducted via the fasciculus gracilis. Video 12.2 (dorsal column mapping with miniature electrode- supplementary material on the web) illustrates the technique.

Contamination of recordings by activity originating from ipsilateral spinocerebellar tracts situated in the lateral columns would be unlikely since (1) the tibial nerves were stimulated at the ankles, where fibers contributing to the spinocerebellar pathways are rare ; (2) the DREZ separates the electrical activity of the DCs from that of the dorsolateral columns; and (3) more laterally situated recording sites, although being closer to the spinocerebellar pathways, showed lower amplitude activity when compared to sites closer to the dorsal midline.

The miniature multielectrode was found to reliably record high-quality and high-amplitude tibial nerve spinal SEPs over the cervical and thoracic SC. The electrode size was appropriate to the size of the DCs according to anatomical studies that showed the distance between DREZs as 6 to 7 mm at the cervical level . In the lumbar area, there was contamination with the higher amplitude segmental responses arising from activity in the dorsal roots and horns. Even with the high-pass filter set at 100 Hz, they were not able to clearly distinguish conducted waves from the segmental ones. In this area, the DCs are also narrower, making positioning of the electrode more difficult. Similar contamination with segmental waves was experienced in the cervical area with spinal SEPs recorded after median nerve stimulation. This was only helpful in determining the functional midline indirectly, indicating proximity to the DREZ. Therefore median nerve stimulation can be useful in mapping of the DREZ. Nevertheless, the midline in the cervical SC could successfully be determined using tibial nerve SEPs.

Recently, Yanni et al. conducted a retrospective analysis of surgery for intramedullary SC tumors focusing especially on posterior column functional integrity . In all patients with syringomyelia ( Fig. 12.2 ) and in two-third of the patients with tumors, the authors were unable to identify with certainty the midline using anatomical landmarks. Using the above described electrode array, they succeeded to locate the physiological midline and place the myelotomy safely, thus reducing injury to the posterior columns.