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

  1. Takamitsu Watanabe  Is a corresponding author
  1. The University of Tokyo, Japan

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

Article and author information

Author details

  1. 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.
    ORCID icon "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

© 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.

Metrics

  • 2,319
    views
  • 448
    downloads
  • 13
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Takamitsu Watanabe
(2021)
Causal roles of prefrontal cortex during spontaneous perceptual switching are determined by brain state dynamics
eLife 10:e69079.
https://doi.org/10.7554/eLife.69079

Share this article

https://doi.org/10.7554/eLife.69079

Further reading

    1. Neuroscience
    William T Redman, Santiago Acosta-Mendoza ... Michael J Goard
    Research Article

    Although grid cells are one of the most well-studied functional classes of neurons in the mammalian brain, whether there is a single orientation and spacing value per grid module has not been carefully tested. We analyze a recent large-scale recording of medial entorhinal cortex to characterize the presence and degree of heterogeneity of grid properties within individual modules. We find evidence for small, but robust, variability and hypothesize that this property of the grid code could enhance the encoding of local spatial information. Performing analysis on synthetic populations of grid cells, where we have complete control over the amount heterogeneity in grid properties, we demonstrate that grid property variability of a similar magnitude to the analyzed data leads to significantly decreased decoding error. This holds even when restricted to activity from a single module. Our results highlight how the heterogeneity of the neural response properties may benefit coding and opens new directions for theoretical and experimental analysis of grid cells.

    1. Neuroscience
    Maren Klingelhöfer-Jens, Katharina Hutterer ... Tina B Lonsdorf
    Research Article

    Childhood adversity is a strong predictor of developing psychopathological conditions. Multiple theories on the mechanisms underlying this association have been suggested which, however, differ in the operationalization of ‘exposure.’ Altered (threat) learning mechanisms represent central mechanisms by which environmental inputs shape emotional and cognitive processes and ultimately behavior. 1402 healthy participants underwent a fear conditioning paradigm (acquisition training, generalization), while acquiring skin conductance responses (SCRs) and ratings (arousal, valence, and contingency). Childhood adversity was operationalized as (1) dichotomization, and following (2) the specificity model, (3) the cumulative risk model, and (4) the dimensional model. Individuals exposed to childhood adversity showed blunted physiological reactivity in SCRs, but not ratings, and reduced CS+/CS- discrimination during both phases, mainly driven by attenuated CS+ responding. The latter was evident across different operationalizations of ‘exposure’ following the different theories. None of the theories tested showed clear explanatory superiority. Notably, a remarkably different pattern of increased responding to the CS- is reported in the literature for anxiety patients, suggesting that individuals exposed to childhood adversity may represent a specific sub-sample. We highlight that theories linking childhood adversity to (vulnerability to) psychopathology need refinement.