Naming-related spectral responses predict neuropsychological outcome after epilepsy surgery.

This prospective study determined the use of intracranially recorded spectral responses during naming tasks in predicting neuropsychological performance following epilepsy surgery. We recruited 65 patients with drug-resistant focal epilepsy who underwent preoperative neuropsychological assessment and intracranial EEG recording. The Clinical Evaluation of Language Fundamentals evaluated the baseline and postoperative language function. During extra-operative intracranial EEG recording, we assigned patients to undergo auditory and picture naming tasks. Time-frequency analysis determined the spatiotemporal characteristics of naming-related amplitude modulations, including high gamma augmentation at 70-110 Hz. We surgically removed the presumed epileptogenic zone based on the intracranial EEG and MRI abnormalities while maximally preserving the eloquent areas defined by electrical stimulation mapping. The multivariate regression model incorporating auditory naming-related high gamma augmentation predicted the postoperative changes in Core Language Score with r2 of 0.37 and in Expressive Language Index with r2 of 0.32. Independently of the effects of epilepsy and neuroimaging profiles, higher high gamma augmentation at the resected language-dominant hemispheric area predicted a more severe postoperative decline in Core Language Score and Expressive Language Index. Conversely, the model incorporating picture naming-related high gamma augmentation predicted the change in Receptive Language Index with an r2 of 0.50. Higher high gamma augmentation independently predicted a more severe postoperative decline in Receptive Language Index. Ancillary regression analysis indicated that naming-related low gamma augmentation and alpha/beta attenuation likewise independently predicted a more severe Core Language Score decline. The machine learning-based prediction model suggested that naming-related high gamma augmentation, among all spectral responses used as predictors, most strongly contributed to the improved prediction of patients showing a >5-point Core Language Score decline (reflecting the lower 25th percentile among patients). We generated the model-based atlas visualizing sites, which, if resected, would lead to such a language decline. With a 5-fold cross-validation procedure, the auditory naming-based model predicted patients who had such a postoperative language decline with an accuracy of 0.80. The model indicated that virtual resection of an electrical stimulation mapping-defined language site would have increased the relative risk of the Core Language Score decline by 5.28 (95% confidence interval: 3.47-8.02). Especially, that of an electrical stimulation mapping-defined receptive language site would have maximized it to 15.90 (95% confidence interval: 9.59-26.33). In summary, naming-related spectral responses predict neuropsychological outcomes after epilepsy surgery. We have provided our prediction model as an open-source material, which will indicate the postoperative language function of future patients and facilitate external validation at tertiary epilepsy centres.

Four-dimensional functional cortical maps of visual and auditory language: Intracranial recording.

OBJECTIVE: The strength of presurgical language mapping using electrocorticography (ECoG) is its outstanding signal fidelity and temporal resolution, but the weakness includes limited spatial sampling at an individual patient level. By averaging naming-related high-gamma activity at nonepileptic regions across a large number of patients, we provided the functional cortical atlases animating the neural dynamics supporting visual-object and auditory-description naming at the whole brain level. METHODS: We studied 79 patients who underwent extraoperative ECoG recording as epilepsy presurgical evaluation, and generated time-frequency plots and animation videos delineating the dynamics of naming-related high-gamma activity at 70-110 Hz. RESULTS: Naming task performance elicited high-gamma augmentation in domain-specific lower-order sensory areas and inferior-precentral gyri immediately after stimulus onset. High-gamma augmentation subsequently involved widespread neocortical networks with left hemisphere dominance. Left posterior temporal high-gamma augmentation at several hundred milliseconds before response onset exhibited a double dissociation; picture naming elicited high-gamma augmentation preferentially in regions medial to the inferior-temporal gyrus, whereas auditory naming elicited high-gamma augmentation more laterally. The left lateral prefrontal regions including Broca's area initially exhibited high-gamma suppression subsequently followed by high-gamma augmentation at several hundred milliseconds before response onset during both naming tasks. Early high-gamma suppression within Broca's area was more intense during picture compared to auditory naming. Subsequent lateral-prefrontal high-gamma augmentation was more intense during auditory compared to picture naming. SIGNIFICANCE: This study revealed contrasting characteristics in the spatiotemporal dynamics of naming-related neural modulations between tasks. The dynamic atlases of visual and auditory language might be useful for planning of epilepsy surgery. Differential neural activation well explains some of the previously reported observations of domain-specific language impairments following resective epilepsy surgery. Video materials might be beneficial for the education of lay people about how the brain functions differentially during visual and auditory naming.