Causal roles of prefrontal cortex during spontaneous perceptual switching are determined by brain state dynamics

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Abstract

The prefrontal cortex (PFC) is thought to orchestrate cognitive dynamics. However, in tests of bistable visual perception, no direct evidence supporting such presumable causal roles of the PFC has been reported. Here, using a novel brain-state-dependent neural stimulation system, we identified causal effects on percept dynamics in three PFC activities-right frontal eye fields, dorsolateral PFC (DLPFC) and inferior frontal cortex (IFC)-. The causality is behaviourally detectable only when we track brain state dynamics and modulate the PFC activity in brain-state-/state-history-dependent manners. The behavioural effects are underpinned by transient neural changes in the brain state dynamics, and such neural effects are quantitatively explainable by structural transformations of the hypothetical energy landscapes. Moreover, these findings indicate distinct functions of the three PFC areas: in particular, the DLPFC enhances the integration of two PFC-active brain states, whereas IFC promotes the functional segregation between them. This work resolves the controversy over the PFC roles in spontaneous perceptual switching and underlines brain state dynamics in fine investigations of brain-behaviour causality.

Data availability

The behavioural data are deposited in Dryrad (https://doi.org/10.5061/dryad.8931zcrqn) and the codes for the energy landscape analysis has been shared as a supplementary information of our previous work (Ezaki, T., Watanabe, T., Ohzeki, M. & Masuda, N. Energy landscape analysis of neuroimaging data. Philosophical Transactions Royal Soc Math Phys Eng Sci 375, 20160287 (2017), https://doi.org/10.1098/rsta.2016.0287).

The following data sets were generated

1. Watanabe T
(2021) Data from: Causal roles of prefrontal cortex during spontaneous perceptual switching are determined by brain state dynamics
Dryad Digital Repository, doi:10.5061/dryad.8931zcrqn.

https://doi.org/10.5061/dryad.8931zcrqn

Article and author information

Author details

Takamitsu Watanabe

International Research Center for Neurointelligence, The University of Tokyo, Tokyo, Japan

For correspondence
takamitsu.watanabe@ircn.jp

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-8104-6873

Funding

Japan Society for the Promotion of Science (19H03535)

Takamitsu Watanabe

Japan Science and Technology Agency (JPMJMS2021)

Takamitsu Watanabe

Astellas Foundation for Research on Metabolic Disorders

Takamitsu Watanabe

Fukuhara Foundation

Takamitsu Watanabe

Yamaha Motor Foundation of Sports

Takamitsu Watanabe

Showa University Medical Institute of Developmental Disabilities Research

Takamitsu Watanabe

The University of Tokyo Excellent Young Researcher Project

Takamitsu Watanabe

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Human subjects: This study was approved by Institutional Ethics Committees in RIKEN and The University of Tokyo. The TMS protocols used here complied with the guideline issued by the Japanese Society for Clinical Neurophysiology and that by International Federation of Clinical Neurophysiology. All the participants provided written informed consents before any experiment and were financially compensated for their participation.

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.