Parallel cognitive processing streams in human prefrontal cortex: Parsing areal-level brain network for response inhibition

Takahiro Osada; Akitoshi Ogawa; Akimitsu Suda; Koji Nakajima; Masaki Tanaka; Satoshi Oka; Koji Kamagata; Shigeki Aoki; Yasushi Oshima; Sakae Tanaka; Nobutaka Hattori; Seiki Konishi

doi:10.1016/j.celrep.2021.109732

Parallel cognitive processing streams in human prefrontal cortex: Parsing areal-level brain network for response inhibition

Cell Rep. 2021 Sep 21;36(12):109732. doi: 10.1016/j.celrep.2021.109732.

Authors

Affiliations

¹ Department of Neurophysiology, Juntendo University School of Medicine, 2-1-1 Hongo, Bunkyo-ku, Tokyo 113-8421, Japan.
² Department of Neurophysiology, Juntendo University School of Medicine, 2-1-1 Hongo, Bunkyo-ku, Tokyo 113-8421, Japan; Department of Neurology, Juntendo University School of Medicine, 2-1-1 Hongo, Bunkyo-ku, Tokyo 113-8421, Japan.
³ Department of Neurophysiology, Juntendo University School of Medicine, 2-1-1 Hongo, Bunkyo-ku, Tokyo 113-8421, Japan; Department of Orthopaedic Surgery, The University of Tokyo School of Medicine, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan.
⁴ Department of Radiology, Juntendo University School of Medicine, 2-1-1 Hongo, Bunkyo-ku, Tokyo 113-8421, Japan.
⁵ Department of Orthopaedic Surgery, The University of Tokyo School of Medicine, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan.
⁶ Department of Neurology, Juntendo University School of Medicine, 2-1-1 Hongo, Bunkyo-ku, Tokyo 113-8421, Japan.
⁷ Department of Neurophysiology, Juntendo University School of Medicine, 2-1-1 Hongo, Bunkyo-ku, Tokyo 113-8421, Japan; Research Institute for Diseases of Old Age, Juntendo University School of Medicine, 2-1-1 Hongo, Bunkyo-ku, Tokyo 113-8421, Japan; Sportology Center, Juntendo University School of Medicine, 2-1-1 Hongo, Bunkyo-ku, Tokyo 113-8421, Japan; Advanced Research Institute for Health Science, Juntendo University School of Medicine, 2-1-1 Hongo, Bunkyo-ku, Tokyo 113-8421, Japan. Electronic address: skonishi@juntendo.ac.jp.

PMID: 34551294
DOI: 10.1016/j.celrep.2021.109732

Abstract

Multiple cognitive processes are recruited to achieve adaptive behavior. However, it is poorly understood how such cognitive processes are implemented in temporal cascades of human cerebral cortical areas as processing streams to achieve behavior. In the present study, we identify cortical processing streams for response inhibition and examine relationships among the processing streams. Functional magnetic resonance imaging (MRI) and time-resolved single-pulse transcranial magnetic stimulation (TMS) reveal three distinct critical timings of transient disruption in the functionally essential cortical areas that belong to two distinct cerebrocortical networks. Furthermore, single-pulse TMS following suppression of the ventral posterior inferior frontal cortex (vpIFC) with repetitive TMS reveals information flow from the vpIFC to the presupplementary motor area (preSMA) within the same network but not to the dorsal posterior inferior frontal cortex (dpIFC) across different networks. These causal behavioral effects suggest two parallel processing streams (vpIFC-preSMA versus dpIFC-intraparietal sulcus) that act concurrently during response inhibition.

Keywords: areal parcellation response inhibition; cerebrocortical network; fMRI; frontal cortex; neuroimaging; noninvasive brain stimulation; stop-signal task; transcranial magnetic stimulation.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Adult
Brain / physiology*
Brain Mapping
Cognition / physiology*
Female
Humans
Magnetic Resonance Imaging
Male
Motor Cortex / physiology
Neural Pathways / physiology
Parietal Lobe / physiology
Prefrontal Cortex / physiology*
Reaction Time
Transcranial Magnetic Stimulation
Young Adult