Intraoperative cortical localization of music and language reveals signatures of structural complexity in posterior temporal cortex.

Language and music involve the productive combination of basic units into structures. It remains unclear whether brain regions sensitive to linguistic and musical structure are co-localized. We report an intraoperative awake craniotomy in which a left-hemispheric language-dominant professional musician underwent cortical stimulation mapping (CSM) and electrocorticography of music and language perception and production during repetition tasks. Musical sequences were melodic or amelodic, and differed in algorithmic compressibility (Lempel-Ziv complexity). Auditory recordings of sentences differed in syntactic complexity (single vs. multiple phrasal embeddings). CSM of posterior superior temporal gyrus (pSTG) disrupted music perception and production, along with speech production. pSTG and posterior middle temporal gyrus (pMTG) activated for language and music (broadband gamma; 70-150 Hz). pMTG activity was modulated by musical complexity, while pSTG activity was modulated by syntactic complexity. This points to shared resources for music and language comprehension, but distinct neural signatures for the processing of domain-specific structural features.

Decoding articulatory and phonetic components of naturalistic continuous speech from the distributed language network.

Objective.The speech production network relies on a widely distributed brain network. However, research and development of speech brain-computer interfaces (speech-BCIs) has typically focused on decoding speech only from superficial subregions readily accessible by subdural grid arrays-typically placed over the sensorimotor cortex. Alternatively, the technique of stereo-electroencephalography (sEEG) enables access to distributed brain regions using multiple depth electrodes with lower surgical risks, especially in patients with brain injuries resulting in aphasia and other speech disorders.Approach.To investigate the decoding potential of widespread electrode coverage in multiple cortical sites, we used a naturalistic continuous speech production task. We obtained neural recordings using sEEG from eight participants while they read aloud sentences. We trained linear classifiers to decode distinct speech components (articulatory components and phonemes) solely based on broadband gamma activity and evaluated the decoding performance using nested five-fold cross-validation.Main Results.We achieved an average classification accuracy of 18.7% across 9 places of articulation (e.g. bilabials, palatals), 26.5% across 5 manner of articulation (MOA) labels (e.g. affricates, fricatives), and 4.81% across 38 phonemes. The highest classification accuracies achieved with a single large dataset were 26.3% for place of articulation, 35.7% for MOA, and 9.88% for phonemes. Electrodes that contributed high decoding power were distributed across multiple sulcal and gyral sites in both dominant and non-dominant hemispheres, including ventral sensorimotor, inferior frontal, superior temporal, and fusiform cortices. Rather than finding a distinct cortical locus for each speech component, we observed neural correlates of both articulatory and phonetic components in multiple hubs of a widespread language production network.Significance.These results reveal the distributed cortical representations whose activity can enable decoding speech components during continuous speech through the use of this minimally invasive recording method, elucidating language neurobiology and neural targets for future speech-BCIs.

Intraoperative localization and preservation of reading in ventral occipitotemporal cortex.

OBJECTIVE: Resective surgery in language-dominant ventral occipitotemporal cortex (vOTC) carries the risk of causing impairment to reading. Because it is not on the lateral surface, it is not easily accessible for intraoperative mapping, and extensive stimulation mapping can be time-consuming. Here the authors assess the feasibility of using task-based electrocorticography (ECoG) recordings intraoperatively to help guide stimulation mapping of reading in vOTC. METHODS: In 11 patients undergoing extraoperative, intracranial seizure mapping, the authors recorded induced broadband gamma activation (70-150 Hz) during a visual category localizer. In 2 additional patients, whose pathologies necessitated resections in language-dominant vOTC, task-based functional mapping was performed intraoperatively using subdural ECoG alongside direct cortical stimulation. RESULTS: Word-responsive cortex localized using ECoG showed a high sensitivity (72%) to stimulation-induced reading deficits, and the confluence of ECoG and stimulation-positive sites appears to demarcate the visual word form area. Intraoperative task-based ECoG mapping was possible in < 3 minutes, providing a high signal quality, and initial intraoperative data analysis took < 3 minutes, allowing for rapid assessment of broad areas of cortex. Cortical areas critical for reading were mapped and successfully preserved, while also enabling pathological tissue to be completely removed. CONCLUSIONS: Eloquent cortex in ventral visual cortex can be rapidly mapped intraoperatively using ECoG. This method acts to guide high-probability targets for stimulation with limited patient participation and can be used to avoid iatrogenic dyslexia following surgery.