Volume 60, Issue 3 pp. 393-405
FULL-LENGTH ORIGINAL RESEARCH

Development of information sharing in language neocortex in childhood-onset drug-resistant epilepsy

Ravindra Arya

Corresponding Author

Ravindra Arya

Division of Neurology, Comprehensive Epilepsy Center, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio

Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, Ohio

Correspondence

Ravindra Arya, Division of Neurology, Cincinnati Children's Hospital Medical Center, 3333 Burnet Avenue, E4-145, MLC 2015, Cincinnati, Ohio 45229 U.S.A.

Email: [email protected]

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Brian Ervin

Brian Ervin

Division of Neurology, Comprehensive Epilepsy Center, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio

Department of Electrical Engineering and Computing Systems, University of Cincinnati, Cincinnati, Ohio

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J. Adam Wilson

J. Adam Wilson

Division of Neurology, Comprehensive Epilepsy Center, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio

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Anna W. Byars

Anna W. Byars

Division of Neurology, Comprehensive Epilepsy Center, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio

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Leonid Rozhkov

Leonid Rozhkov

Division of Neurology, Comprehensive Epilepsy Center, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio

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Jason Buroker

Jason Buroker

Division of Neurology, Comprehensive Epilepsy Center, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio

Division of Clinical Engineering, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio

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Paul S. Horn

Paul S. Horn

Division of Neurology, Comprehensive Epilepsy Center, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio

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Craig Scholle

Craig Scholle

Division of Neurology, Comprehensive Epilepsy Center, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio

Division of Clinical Engineering, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio

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Hisako Fujiwara

Hisako Fujiwara

Division of Neurology, Comprehensive Epilepsy Center, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio

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Hansel M. Greiner

Hansel M. Greiner

Division of Neurology, Comprehensive Epilepsy Center, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio

Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, Ohio

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James L. Leach

James L. Leach

Division of Pediatric Neuroradiology, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio

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Douglas F. Rose

Douglas F. Rose

Division of Neurology, Comprehensive Epilepsy Center, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio

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Francesco T. Mangano

Francesco T. Mangano

Division of Pediatric Neurosurgery, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio

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Tracy A. Glauser

Tracy A. Glauser

Division of Neurology, Comprehensive Epilepsy Center, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio

Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, Ohio

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Katherine D. Holland

Katherine D. Holland

Division of Neurology, Comprehensive Epilepsy Center, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio

Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, Ohio

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First published: 11 February 2019
Citations: 10

Funding information

Research presented in this article was supported by a Research Innovation Project grant (Cincinnati Children's Research Foundation) and the Procter Scholar Award (Procter Foundation). Funding sources had no role in study design, data management, writing the manuscript, or the decision to submit for publication.

Summary

Objective

We studied age-related dynamics of information sharing among cortical language regions with electrocorticographic high-gamma modulation during picture-naming and story-listening tasks.

Methods

Seventeen epilepsy patients aged 4-19 years, undergoing extraoperative monitoring with left-hemispheric subdural electrodes, were included. Mutual information (MI), a nondirectional measure of shared information, between 16 pairs of cortical regions of interest, was computed from trial-averaged 70–150 Hz power modulations during language tasks. Impact of age on pairwise MI between language regions and their determinants were ascertained with regression analysis.

Results

During picture naming, significant increase in MI with age was seen between pairwise combinations of Broca's area, inferior precentral gyrus (iPreC), and frontal association cortex (FAC); Wernicke's area and posterior association cortex (PAC); and Broca's and Wernicke's areas. During story listening, significant age-related increase in MI was seen between Wernicke's area and either Broca's area, FAC, or PAC; and between Broca's area and FAC. Significant impact of baseline intelligence quotient was seen on the relationship between age and MI for all pairs, except between Broca's area and iPreC. The mean MI was higher during naming compared to listening for pairs including iPreC with Broca's area, FAC, or PAC and was lower for pairs of Wernicke's area or PAC with anterior language regions.

Significance

Information sharing matures with age “within” frontal and temporoparietal language cortices, and “between” Broca's and Wernicke's areas. This study provides evidence for distinct patterns of developmental plasticity within perisylvian language cortex and has implications for planning epilepsy surgery.

DISCLOSURE OF CONFLICTS OF INTEREST

R.A. receives research support from the Procter Foundation and Maxon Foundation. The other authors have no conflicts of interest to report. J.A.W. currently works as a senior software developer for DRW Holdings, LLC. D.F.R. has now retired from his position. Ten patients included in this article have been reported earlier (Arya et al2,7); however, the data were reanalyzed using a different methodology for this article. All commercial software used in this research was covered under appropriate end-user licenses. Python (version 2.7, Anaconda distribution) and R (version 3.4) are free programming languages. All authors have approved the final version of this article for publication. We confirm that we have read the Journal's position on issues involved in ethical publication and affirm that this report is consistent with those guidelines.

The full text of this article hosted at iucr.org is unavailable due to technical difficulties.

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