Intraoperative dorsal language network mapping by using single-pulse electrical stimulation

Abstract

The preservation of language function during brain surgery still poses a challenge. No intraoperative methods have been established to monitor the language network reliably. We aimed to establish intraoperative language network monitoring by means of cortico-cortical evoked potentials (CCEPs). Subjects were six patients with tumors located close to the arcuate fasciculus (AF) in the language-dominant left hemisphere. Under general anesthesia, the anterior perisylvian language area (AL) was first defined by the CCEP connectivity patterns between the ventrolateral frontal and temporoparietal area, and also by presurgical neuroimaging findings. We then monitored the integrity of the language network by stimulating AL and by recording CCEPs from the posterior perisylvian language area (PL) consecutively during both general anesthesia and awake condition. High-frequency electrical stimulation (ES) performed during awake craniotomy confirmed language function at AL in all six patients. Despite an amplitude decline (≤32%) in two patients, CCEP monitoring successfully prevented persistent language impairment. After tumor removal, single-pulse ES was applied to the white matter tract beneath the floor of the removal cavity in five patients, in order to trace its connections into the language cortices. In three patients in whom high-frequency ES of the white matter produced naming impairment, this "eloquent" subcortical site directly connected AL and PL, judging from the latencies and distributions of cortico- and subcortico-cortical evoked potentials. In conclusion, this study provided the direct evidence that AL, PL, and AF constitute the dorsal language network. Intraoperative CCEP monitoring is clinically useful for evaluating the integrity of the language network.

Keywords: arcuate fasciculus; awake craniotomy; cortico-cortical evoked potential; dorsal language network; subcortico-cortical evoked potential.

Copyright © 2014 Wiley Periodicals, Inc.

Figures

Figure 1

Noninvasive anatomo‐functional mapping of the dorsal language network. The left column: 3D MRI shows the long segment of the AF (green) and the tumor (red) around the AF. The middle column: The anterior and posterior perisylvian language cortices defined by shiritori word generation fMRI (dark yellow) are shown in comparison with the subdural electrodes. Only the activation areas outside the pre‐ and postcentral gyri are shown for clarity. White circles denote visible electrodes in the operative view, and gray circles invisible electrodes. Note that the frontal CCEP stimulus site (a black pair of electrodes) corresponded with the anterior language area defined by fMRI in all patients. The right column: The AF tracts (green) were shown in comparison with subdural electrodes.

Figure 2

Behavior of the CCEP N1 amplitude during tumor removal in the awake condition. The left column shows the CCEP distribution with a circle map in each patient in the awake condition. The diameter of the circle at each electrode represented the percentile to the largest amplitude at the maximum CCEP response site. The right column shows the N1 waveform at the maximum CCEP response site in each patient. The black line represents the N1 waveform immediately after the awake condition, and the red line that after tumor removal. A N1 amplitude decrease was noted in Patient 2 (12%) and Patient 4 (32%).

Figure 3

CCEP connectivity pattern to map perisylvian language areas (Patient 4). Under general anesthesia, single‐pulse ES was delivered to four candidate sites (Plate B) according to the noninvasive anatomo‐functional mapping, and CCEPs were recorded from the temporoparietal area (Plate A). Two trials are plotted in superimposition at each electrode. The vertical bar corresponds to the time of stimulation. Note the CCEP pattern in Plate A differs evidently among the four stimulus sites. Electrode B05–13 stimulation showed the largest and most discrete CCEP response in the lateral temporoparietal area (Electrode A04 and A05). This site was regarded as the putative anterior language area. Indeed 50 Hz stimulation of this area showed language impairment in the awake condition. n.a. = CCEP was not available due to high impedance in the recording electrode. Other conventions are the same as for Figure 1.

Figure 4

Intraoperative online language network mapping by CCEPs (Patient 3). A: Electrode configuration in the intraoperative view. B: CCEP distribution map during general anesthesia. CCEP distributed over the middle to posterior part of the superior, middle and inferior temporal gyri (the maximum at Electrode B02 in the superior temporal gyrus). C: CCEP waveforms (Plate B) in the awake condition (before tumor removal). Two trials are plotted in superimposition. CCEP distribution did not change between general anesthesia and awake condition. D: Change of the N1 amplitude during surgery at the maximum CCEP response site (Electrode B02). CCEP waveforms are sequentially shown from the top to the bottom along the time course of surgery. As the patient awoke, the N1 amplitude increased from 215 to 311 µV (+45%). After tumor removal the N1 amplitude did not decline (329 µV). She did not show language dysfunction during or after surgery. Other conventions are the same as for Figure 3.

Figure 5

SCEPs in Patient 3. A: Site of white matter stimulation. Electrode pair (highlighted by a green circle) was stimulated at the floor of the removal cavity (right). The stimulus site (cross hairs) was attached to the AF (long segment) in the neuro‐navigation (left). High‐frequency (50 Hz) stimulation at this site induced the arrest of naming. B: SCEP distribution in the frontal and temporal areas. Circle maps were made separately for SCEP responses in the frontal (SCEPWM→AL) and temporal (SCEPWM→PL) areas, based on the SCEP amplitude percentage distribution. C: SCEPWM→AL (Plate B) and SCEPWM→PL (Plate A) waveforms. The largest response was highlighted with a dotted circle and its onset and peak latencies are shown in the enlarged waveform at the bottom. n.a. = SCEP was not available due to the limited number of channels available for simultaneous monitoring or high impedance in the recording electrode. Other conventions are the same as for Figure 4.