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

  • 2,223
    views
  • 429
    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
    John P Veillette, Fan Gao, Howard C Nusbaum
    Research Article

    Sensory signals from the body’s visceral organs (e.g. the heart) can robustly influence the perception of exteroceptive sensations. This interoceptive–exteroceptive interaction has been argued to underlie self-awareness by situating one’s perceptual awareness of exteroceptive stimuli in the context of one’s internal state, but studies probing cardiac influences on visual awareness have yielded conflicting findings. In this study, we presented separate grating stimuli to each of subjects’ eyes as in a classic binocular rivalry paradigm – measuring the duration for which each stimulus dominates in perception. However, we caused the gratings to ‘pulse’ at specific times relative to subjects’ real-time electrocardiogram, manipulating whether pulses occurred during cardiac systole, when baroreceptors signal to the brain that the heart has contracted, or in diastole when baroreceptors are silent. The influential ‘Baroreceptor Hypothesis’ predicts the effect of baroreceptive input on visual perception should be uniformly suppressive. In contrast, we observed that dominance durations increased for systole-entrained stimuli, inconsistent with the Baroreceptor Hypothesis. Furthermore, we show that this cardiac-dependent rivalry effect is preserved in subjects who are at-chance discriminating between systole-entrained and diastole-presented stimuli in a separate interoceptive awareness task, suggesting that our results are not dependent on conscious access to heartbeat sensations.

    1. Neuroscience
    Julien Rossato, François Hug ... Simon Avrillon
    Tools and Resources

    Decoding the activity of individual neural cells during natural behaviours allows neuroscientists to study how the nervous system generates and controls movements. Contrary to other neural cells, the activity of spinal motor neurons can be determined non-invasively (or minimally invasively) from the decomposition of electromyographic (EMG) signals into motor unit firing activities. For some interfacing and neuro-feedback investigations, EMG decomposition needs to be performed in real time. Here, we introduce an open-source software that performs real-time decoding of motor neurons using a blind-source separation approach for multichannel EMG signal processing. Separation vectors (motor unit filters) are optimised for each motor unit from baseline contractions and then re-applied in real time during test contractions. In this way, the firing activity of multiple motor neurons can be provided through different forms of visual feedback. We provide a complete framework with guidelines and examples of recordings to guide researchers who aim to study movement control at the motor neuron level. We first validated the software with synthetic EMG signals generated during a range of isometric contraction patterns. We then tested the software on data collected using either surface or intramuscular electrode arrays from five lower limb muscles (gastrocnemius lateralis and medialis, vastus lateralis and medialis, and tibialis anterior). We assessed how the muscle or variation of contraction intensity between the baseline contraction and the test contraction impacted the accuracy of the real-time decomposition. This open-source software provides a set of tools for neuroscientists to design experimental paradigms where participants can receive real-time feedback on the output of the spinal cord circuits.