Real-Time Electrocorticography-Based Functional Mapping of Language Cortex
Ahmad Alhourani, Thomas A. Wozny, Robert Mark Richardson · Neurosurgery · 2016
Optimal surgical resection for the treatment of drug-resistant epilepsy and many brain tumors relies on balancing the competing interests of maximal removal of pathological tissue with preservation of eloquent cortex and the functions it subserves. To this end, electrocortical stimulation mapping (ESM) remains the gold standard for defining the functional role of cortical anatomy and inferring the associated risk for postoperative neurologic deficit. ESM is a cumbersome, time-consuming technique often limited not only by the patient's attentional capacity but also by the risk for stimulation-induced afterdischarge and seizure activity. In contrast to ESM, electrocorticographic mapping of task-related functional activation does not require the use of electric stimulation and may thus provide a safer alternative. Additionally, because functional activation mapping can investigate all electrode locations simultaneously, it may offer substantial reductions in the time required to perform cortical mapping compared with the serial approach of ESM. Building on advances in cognitive neuroscience and prior work exploring high-frequency electrocortical dynamics, Wang et al1 recently developed a trial-based system for bedside, recording-based, spatial-temporal functional mapping of language-related cortex. In this study, 7 patients with drug-resistant epilepsy undergoing seizure monitoring with chronic electrocorticography performed a visual object naming task and an auditory word repetition task. After completion of each trial within the task, trial-locked increases in high-gamma activity (70-110 Hz), presumed to represent increases in local neuronal population firing, were quantified and graphically represented. This real-time, trialwise approach allowed the experimenters to continually monitor estimates of functional activation and reject artifact-contaminated trials. Responses within microelectrocorticography arrays were often more robust than those within macroelectrode arrays. By depicting both the temporal evolution of high gamma activity and its relationship to neuroanatomy, the large-scale cortical networks dynamically engaging in task performance could be readily appreciated (Figure).Figure: Spatial-temporal functional mapping in 1 subject. Spatial-temporal functional mapping results are shown as a raster of high-gamma responses on the left and as brain maps of high-gamma response magnitude (represented by disc size and color) on the right. ESM maps (colored bars between electrodes) are also shown. Color-shaded areas denote anatomic boundaries of classic language areas used as regions of interest in region of interest sensitivity/specificity analysis. Each raster plot displays the spatial-temporal distribution of significant increases (red spectrum) or decreases (blue spectrum) in high-gamma energy relative to precue baseline in 16-millisecond windows. Each row corresponds to a different electrode as displayed on the right brain maps. All times are relative to cue onset (t = 0 second). To highlight the spatial pattern of cortical activation at early (visual/auditory perception) and late (response production) stages, high-gamma responses are integrated across an early and late temporal window (early stage highlighted in blue and late stage in red on raster plot) and shown in separate brain maps (early stage in the top brain and late stage in the bottom brain). Microelectrode array AMIC and PMIC are enlarged for better visualization of high-gamma responses. Second brain image and highlighting of early and late time periods on the channel raster have been added to the screenshot post hoc. Red, tongue/mouth motor; blue, tongue/mouth sensory; purple, picture naming; light green, clear for tongue/mouth motor/sensory; and dark green, clear for picture naming. Modified with permission from Wang Y, Fifer MS, Flinker A, et al. Spatial-temporal functional mapping of language at the bedside with electrocorticography. Neurology. 2016;86(13):1181-1189. Available at: http://www.neurology.org/content/86/13/1181.long. Accessed July 12, 2016.To infer the validity of this online tool for cortical mapping, the authors first compared the ability of high-gamma mapping to identify functionally active electrodes to those electrodes resulting in impairment when stimulated during ESM. Wang et al found that, when taking ESM to represent the ground truth, high-gamma mapping had an average sensitivity and specificity of 69.9% and 83.5%, respectively. These results indicate a considerable degree of concordance between the 2 modalities. The authors go on to suggest that the relatively lower sensitivity of functional activation-based mapping may be due, at least in part, to the well-documented potential for ESM to have distant effects on connected brain regions, thus leading to spurious positive findings. An alternative validation approach was used, comparing the ability of the 2 modalities to identify cortical regions of interest involved in language function, as defined by accepted anatomic locations extracted from the brain lesion literature. Real-time functional mapping was found to have a higher sensitivity (65.6% vs 47.9%) and a higher specificity (86.2% vs 78.0%) than ESM, with only the difference in sensitivity reaching statistical significance. This study offers encouraging results, suggesting that real-time functional mapping may offer a faster, safer, and potentially more accurate alternative to standard ESM. Such trial-based functional mapping can extend the possibilities of current cortical mapping by revealing dynamic cortical engagement at fine temporal scales exhibited during a wide range of cognitive tasks. Additionally, functional mapping affords graded estimates of cortical activation that, in contrast to the binary results of ESM, may be useful in inferring the relative importance of a given cortical location in particular cognitive functions. Given these promising findings, future work exploring the utility of recording-based functional mapping in predicting postoperative neurologic outcomes is eagerly anticipated.