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

Yasuo Nakai, Ayaka Sugiura, Erik C. Brown, Masaki Sonoda, Jeong Won Jeong, Robert Rothermel, Aimee F. Luat, Sandeep Sood, Eishi Asano

Research output: Contribution to journalArticlepeer-review

25 Scopus citations

Abstract

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.

Original languageEnglish
Pages (from-to)255-267
Number of pages13
JournalEpilepsia
Volume60
Issue number2
DOIs
StatePublished - Feb 2019

Keywords

  • event-related high-gamma modulation
  • four-dimensional (4D)
  • intracranial electroencephalography (iEEG) recording
  • physiological high-frequency oscillations (HFOs)
  • speech

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