Three- and four-dimensional mapping of speech and language in patients with epilepsy.
We have provided 3-D and 4D mapping of speech and language function based upon the results of direct cortical stimulation and event-related modulation of electrocorticography signals. Patients estimated to have right-hemispheric language dominance were excluded. Thus, 100 patients who underwent two-stage epilepsy surgery with chronic electrocorticography recording were studied. An older group consisted of 84 patients at least 10 years of age (7367 artefact-free non-epileptic electrodes), whereas a younger group included 16 children younger than age 10 (1438 electrodes). The probability of symptoms transiently induced by electrical stimulation was delineated on a 3D average surface image. The electrocorticography amplitude changes of high-gamma (70-110 Hz) and beta (15-30 Hz) activities during an auditory-naming task were animated on the average surface image in a 4D manner. Thereby, high-gamma augmentation and beta attenuation were treated as summary measures of cortical activation. Stimulation data indicated the causal relationship between (i) superior-temporal gyrus of either hemisphere and auditory hallucination; (ii) left superior-/middle-temporal gyri and receptive aphasia; (iii) widespread temporal/frontal lobe regions of the left hemisphere and expressive aphasia; and (iv) bilateral precentral/left posterior superior-frontal regions and speech arrest. On electrocorticography analysis, high-gamma augmentation involved the bilateral superior-temporal and precentral gyri immediately following question onset; at the same time, high-gamma activity was attenuated in the left orbitofrontal gyrus. High-gamma activity was augmented in the left temporal/frontal lobe regions, as well as left inferior-parietal and cingulate regions, maximally around question offset, with high-gamma augmentation in the left pars orbitalis inferior-frontal, middle-frontal, and inferior-parietal regions preceded by high-gamma attenuation in the contralateral homotopic regions. Immediately before verbal response, high-gamma augmentation involved the posterior superior-frontal and pre/postcentral regions, bilaterally. Beta-attenuation was spatially and temporally correlated with high-gamma augmentation in general but with exceptions. The younger and older groups shared similar spatial-temporal profiles of high-gamma and beta modulation; except, the younger group failed to show left-dominant activation in the rostral middle-frontal and pars orbitalis inferior-frontal regions around stimulus offset. The human brain may rapidly and alternately activate and deactivate cortical areas advantageous or obtrusive to function directed toward speech and language at a given moment. Increased left-dominant activation in the anterior frontal structures in the older age group may reflect developmental consolidation of the language system. The results of our functional mapping may be useful in predicting, across not only space but also time and patient age, sites specific to language function for presurgical evaluation of focal epilepsy.
Department of Pediatrics, Wayne State University, Children's Hospital of Michigan, Detroit Medical Center, Detroit, MI, 48201, USA.|Department of Neurological Surgery, Wakayama Medical University, Wakayama-shi, Wakayama, 6418510, Japan.
Yasuo
Y
Nakai
Department of Pediatrics, Wayne State University, Children's Hospital of Michigan, Detroit Medical Center, Detroit, MI, 48201, USA.|Department of Neurology, Wayne State University, Children's Hospital of Michigan, Detroit Medical Center, Detroit, MI, 48201, USA.
Jeong-Won
JW
Jeong
Department of Neurological Surgery, Oregon Health and Science University, Portland, OR, 97239, USA.
Erik C
EC
Brown
Department of Psychiatry, Wayne State University, Children's Hospital of Michigan, Detroit Medical Center, Detroit, MI, 48201, USA.
Robert
R
Rothermel
Department of Pediatrics, Wayne State University, Children's Hospital of Michigan, Detroit Medical Center, Detroit, MI, 48201, USA.|Department of Pediatrics, University of California San Francisco, CA, 94143, USA.
Katsuaki
K
Kojima
Department of Pediatrics, Wayne State University, Children's Hospital of Michigan, Detroit Medical Center, Detroit, MI, 48201, USA.|Postdoctoral Fellowship for Research Abroad, Japan Society for the Promotion of Science (JSPS), Chiyoda-ku, Tokyo, 1020083, Japan.
Toshimune
T
Kambara
Department of Neurology, Wayne State University, Children's Hospital of Michigan, Detroit Medical Center, Detroit, MI, 48201, USA.
Aashit
A
Shah
Department of Neurosurgery, Wayne State University, Children's Hospital of Michigan, Detroit Medical Center, Detroit, MI, 48201, USA.
Sandeep
S
Mittal
Department of Neurosurgery, Wayne State University, Children's Hospital of Michigan, Detroit Medical Center, Detroit, MI, 48201, USA.
Sandeep
S
Sood
Department of Pediatrics, Wayne State University, Children's Hospital of Michigan, Detroit Medical Center, Detroit, MI, 48201, USA.|Department of Neurology, Wayne State University, Children's Hospital of Michigan, Detroit Medical Center, Detroit, MI, 48201, USA.
Eishi
E
Asano
D000293:Adolescent; D000328:Adult; D000367:Age Factors; D001931:Brain Mapping / Q000379:methods*; D058256:Brain Waves / Q000502:physiology; D002525:Cerebellar Cortex / Q000502:physiology*; D002648:Child; D002675:Child, Preschool; D004558:Electric Stimulation; D000069280:Electrocorticography / Q000379:methods*; D004567:Electrodes, Implanted; D004827:Epilepsy / Q000503:physiopathology*; D006801:Humans; D021621:Imaging, Three-Dimensional / Q000379:methods*; D007802:Language; D013060:Speech / Q000502:physiology*; D055815:Young Adult
developmental consolidation; electrical stimulation; epilepsy surgery; high-frequency oscillations (HFOs); intracranial electrocorticography (ECoG) recording