Causal roles of prefrontal cortex during spontaneous perceptual switching are determined by brain state dynamics
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).
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Data from: Causal roles of prefrontal cortex during spontaneous perceptual switching are determined by brain state dynamicsDryad Digital Repository, doi:10.5061/dryad.8931zcrqn.
Article and author information
Author details
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
© 2021, Watanabe
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.
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