Connectivity Gradient in the Human Left Inferior Frontal Gyrus: Intraoperative Cortico-Cortical Evoked Potential Study

Author:

Nakae Takuro12,Matsumoto Riki34,Kunieda Takeharu15,Arakawa Yoshiki1,Kobayashi Katsuya36,Shimotake Akihiro3,Yamao Yukihiro1,Kikuchi Takayuki1,Aso Toshihiko7,Matsuhashi Masao8,Yoshida Kazumichi1,Ikeda Akio8,Takahashi Ryosuke3,Lambon Ralph Matthew A9,Miyamoto Susumu1

Affiliation:

1. Department of Neurosurgery, Kyoto University Graduate School of Medicine, Kyoto 606-8507, Japan

2. Department of Neurosurgery, Shiga General Hospital, Moriyama, Shiga 524-0022, Japan

3. Department of Neurology, Kyoto University Graduate School of Medicine, Kyoto 606-8507, Japan

4. Division of Neurology, Kobe University Graduate School of Medicine, Kobe, Hyogo 650-0017, Japan

5. Department of Neurosurgery, Ehime University Graduate School of Medicine, To-on, Ehime 791-0295, Japan

6. Epilepsy Center, Cleveland Clinic, Cleveland, OH 44106, USA

7. Laboratory for Brain Connectomics Imaging, RIKEN Center for Biosystems Dynamics Research, Hyogo 650-0047, Japan

8. Department of Epilepsy, Movement Disorders and Physiology, Kyoto University Graduate School of Medicine, Kyoto 606-8507, Japan

9. MRC Cognition and Brain Sciences Unit, University of Cambridge, Cambridge CB2 7EF, UK

Abstract

Abstract In the dual-stream model of language processing, the exact connectivity of the ventral stream to the anterior temporal lobe remains elusive. To investigate the connectivity between the inferior frontal gyrus (IFG) and the lateral part of the temporal and parietal lobes, we integrated spatiotemporal profiles of cortico-cortical evoked potentials (CCEPs) recorded intraoperatively in 14 patients who had undergone surgical resection for a brain tumor or epileptic focus. Four-dimensional visualization of the combined CCEP data showed that the pars opercularis (Broca’s area) is connected to the posterior temporal cortices and the supramarginal gyrus, whereas the pars orbitalis is connected to the anterior lateral temporal cortices and angular gyrus. Quantitative topographical analysis of CCEP connectivity confirmed an anterior–posterior gradient of connectivity from IFG stimulus sites to the temporal response sites. Reciprocality analysis indicated that the anterior part of the IFG is bidirectionally connected to the temporal or parietal area. This study shows that each IFG subdivision has different connectivity to the temporal lobe with an anterior–posterior gradient and supports the classical connectivity concept of Dejerine; that is, the frontal lobe is connected to the temporal lobe through the arcuate fasciculus and also a double fan-shaped structure anchored at the limen insulae.

Funder

Ministry of Education, Culture, Sports, Science and Technology

Japan Society for the Promotion of Science

Medical Research Council

Publisher

Oxford University Press (OUP)

Subject

Cellular and Molecular Neuroscience,Cognitive Neuroscience

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