OBJECTIVE We determined the clinical impact and developmental changes of auditory-language-related augmentation of gamma activity at 50–120 Hz recorded on electrocorticography (ECoG). METHODS We analyzed data from 77 epileptic patients ranging 4 – 56 years in age. We determined the effects of seizure-onset zone, electrode location, and patient-age upon gamma-augmentation elicited by an auditory-naming task. RESULTS Gamma-augmentation was less frequently elicited within seizure-onset sites compared to other sites. Regardless of age, gamma-augmentation most often involved the 80–100 Hz frequency band. Gamma-augmentation initially involved bilateral superior-temporal regions, followed by left-side dominant involvement in the middle-temporal, medial-temporal, inferior-frontal, dorsolateral-premotor, and medial-frontal regions and concluded with bilateral inferior-Rolandic involvement. Compared to younger patients, those older than 10 years had a larger proportion of left dorsolateral-premotor and right inferior-frontal sites showing gamma-augmentation. The incidence of a post-operative language deficit requiring speech therapy was predicted by the number of resected sites with gamma-augmentation in the superior-temporal, inferior-frontal, dorsolateral-premotor, and inferior-Rolandic regions of the left hemisphere assumed to contain essential language function (r2=0.59; p=0.001; odds ratio=6.04 [95% confidence-interval: 2.26 to 16.15]). CONCLUSIONS Auditory-language-related gamma-augmentation can provide additional information useful to localize the primary language areas. SIGNIFICANCE These results derived from a large sample of patients support the utility of auditory-language-related gamma-augmentation in presurgical evaluation.

Objective We determined the utility of electrocorticography (ECoG) and stimulation for detecting language-related sites in patients with left-hemispheric language-dominance on Wada test. Methods We studied 13 epileptic patients who underwent language mapping using event-related gamma-oscillations on ECoG and stimulation via subdural electrodes. Sites showing significant gamma-augmentation during an auditory-naming task were defined as language-related ECoG sites. Sites at which stimulation resulted in auditory perceptual changes, failure to verbalize a correct answer, or sensorimotor symptoms involving the mouth were defined as language-related stimulation sites. We determined how frequently these methods revealed language-related sites in the superior-temporal, inferior-frontal, dorsolateral-premotor, and inferior-Rolandic regions. Results Language-related sites in the superior-temporal and inferior-frontal gyri were detected by ECoG more frequently than stimulation (p < 0.05), while those in the dorsolateral-premotor and inferior-Rolandic regions were detected by both methods equally. Stimulation of language-related ECoG sites, compared to the others, more frequently elicited language symptoms (p < 0.00001). One patient developed dysphasia requiring in-patient speech therapy following resection of the dorsolateral-premotor and inferior-Rolandic regions containing language-related ECoG sites not otherwise detected by stimulation. Conclusions Language-related gamma-oscillations may serve as an alternative biomarker of underlying language function in patients with left-hemispheric language-dominance. Significance Measurement of language-related gamma-oscillations is warranted in presurgical evaluation of epileptic patients.

Summary Previous studies of epileptic spasms reported that ictal events were associated with high-frequency oscillations (HFOs) or delta waves involving widespread regions. We determined whether ictal HFOs at 80–200 Hz were coupled with a phase of slow-wave, whether ictal slow-waves were diffusely or locally synchronous signals, and whether the mode of coupling between HFOs and slow-wave phases differed between ictal and interictal states. We studied 11 children who underwent extraoperative electrocorticography (ECoG) recording. The phases and amplitudes of slow-waves were measured at the peak of ictal and interictal HFOs in the seizure-onset sites. Ictal HFOs were locked tightly to the phase of slow-wave at ≤1 Hz. Ictal slow-waves propagated from the seizure-onset site to other regions. In contrast, interictal HFOs in the seizure-onset site were loosely locked to the phase of slow-wave at ≤1 Hz but tightly to that of ≥3-Hz. Ictal slow-waves coupled with HFOs can be explained as near-field and locally synchronized potentials generated by the neocortex rather than far-field potentials generated by subcortical structures. Ictal slow-waves in epileptic spasms may be generated by a mechanism different from what generates interictal HFOs–slow-wave complexes.

Reverse speech has often been used as a control task in brain-mapping studies of language utilizing various non-invasive modalities. The rationale is that reverse speech is comparable to forward speech in terms of auditory characteristics, while omitting the linguistic components. Thus, it may control for non-language auditory functions. This finds some support in fMRI studies indicating that reverse speech resulted in less blood-oxygen-level-dependent (BOLD) signal intensity in perisylvian regions than forward speech. We attempted to externally validate a reverse speech control task using intracranial electrocorticography (ECoG) in eight patients with intractable focal epilepsy. We studied adolescent and adult patients who underwent extraoperative ECoG prior to resective epilepsy surgery. All patients received an auditory language task during ECoG recording. Patients were presented 115 audible question stimuli, including 30 reverse speech trials. Reverse speech trials more strongly engaged bilateral superior temporal sites than did the corresponding forward speech trials. Forward speech trials elicited larger gamma-augmentation at frontal lobe sites not attributable to sensorimotor function. Other temporal and frontal sites of significant augmentation showed no significant difference between reverse and forward speech. Thus, we failed to validate reported evidence of weaker activation of temporal neocortices during reverse compared to forward speech. Superior temporal lobe engagement may indicate increased attention to reverse speech. Reverse speech does not appear to be a suitable task for the control of non-language auditory functions on ECoG.