Behavioural and neural signatures of perceptual decision-making are modulated by pupil-linked arousal

  1. Jochem van Kempen  Is a corresponding author
  2. Gerard M Loughnane
  3. Daniel P Newman
  4. Simon P Kelly
  5. Alexander Thiele
  6. Redmond G O'Connell
  7. Mark A Bellgrove
  1. Newcastle University, United Kingdom
  2. Trinity College Dublin, Ireland
  3. Monash University, Australia
  4. University College Dublin, Ireland

Abstract

The timing and accuracy of perceptual decision-making is exquisitely sensitive to fluctuations in arousal. Although extensive research has highlighted the role of various neural processing stages in forming decisions, our understanding of how arousal impacts these processes remains limited. Here we isolated electrophysiological signatures of decision-making alongside signals reflecting target selection, attentional engagement and motor output and examined their modulation as a function of tonic and phasic arousal, indexed by baseline and task-evoked pupil diameter, respectively. Reaction times were shorter on trials with lower tonic, and higher phasic arousal. Additionally, these two pupil measures were predictive of a unique set of EEG signatures that together represent multiple information processing steps of decision-making. Finally, behavioural variability associated with fluctuations in tonic and phasic arousal, indicative of neuromodulators acting on multiple timescales, was mediated by its effects on the EEG markers of attentional engagement, sensory processing and the variability in decision processing.

Data availability

All data have been deposited at https://figshare.com/s/8d6f461834c47180a444, in association with Newman et al (2017).All analysis scripts are publicly available at https://github.com/jochemvankempen/2019_pupil_decisionMaking

Article and author information

Author details

  1. Jochem van Kempen

    Institute of Neuroscience, Newcastle University, Newcastle upon Tyne, United Kingdom
    For correspondence
    jochem.van-kempen@ncl.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0211-9545
  2. Gerard M Loughnane

    School of Engineering, Trinity College Dublin, Dublin, Ireland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1961-5294
  3. Daniel P Newman

    School of Psychological Sciences, Monash University, Melbourne, Australia
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8240-1876
  4. Simon P Kelly

    School of Electrical and Electronic Engineering, University College Dublin, Dublin, Ireland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9983-3595
  5. Alexander Thiele

    Institute of Neuroscience, Newcastle University, Newcastle upon Tyne, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  6. Redmond G O'Connell

    Trinity College Institute of Neuroscience, Trinity College Dublin, Dublin, Ireland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6949-2793
  7. Mark A Bellgrove

    Monash Institute for Cognitive and Clinical Neurosciences, Monash University, Melbourne, Australia
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0186-8349

Funding

Wellcome (93104)

  • Jochem van Kempen
  • Alexander Thiele

Australian Research Council (FT130101488)

  • Mark A Bellgrove

Office of Naval Research Global

  • Alexander Thiele
  • Redmond G O'Connell
  • Mark A Bellgrove

Newcastle University, Monash University

  • Alexander Thiele
  • Mark A Bellgrove

Australian Research Council (DP150100986)

  • Mark A Bellgrove

Australian Research Council (DP180102066)

  • Mark A Bellgrove

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

Reviewing Editor

  1. Eran Eldar, UCL, United Kingdom

Ethics

Human subjects: The experimental protocal was approved by the human research ethics committee from Monash University and Trinity College Dublin, and informed consent was obtained from all participants before testing. Project number Monash University: 3658, Trinity College: SPREC012014-1

Version history

  1. Received: October 3, 2018
  2. Accepted: March 16, 2019
  3. Accepted Manuscript published: March 18, 2019 (version 1)
  4. Version of Record published: April 5, 2019 (version 2)

Copyright

© 2019, van Kempen et al.

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

  • 3,449
    views
  • 549
    downloads
  • 43
    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. Jochem van Kempen
  2. Gerard M Loughnane
  3. Daniel P Newman
  4. Simon P Kelly
  5. Alexander Thiele
  6. Redmond G O'Connell
  7. Mark A Bellgrove
(2019)
Behavioural and neural signatures of perceptual decision-making are modulated by pupil-linked arousal
eLife 8:e42541.
https://doi.org/10.7554/eLife.42541

Share this article

https://doi.org/10.7554/eLife.42541

Further reading

    1. Neuroscience
    Songyao Zhang, Tuo Zhang ... Tianming Liu
    Research Article

    Cortical folding is an important feature of primate brains that plays a crucial role in various cognitive and behavioral processes. Extensive research has revealed both similarities and differences in folding morphology and brain function among primates including macaque and human. The folding morphology is the basis of brain function, making cross-species studies on folding morphology important for understanding brain function and species evolution. However, prior studies on cross-species folding morphology mainly focused on partial regions of the cortex instead of the entire brain. Previously, our research defined a whole-brain landmark based on folding morphology: the gyral peak. It was found to exist stably across individuals and ages in both human and macaque brains. Shared and unique gyral peaks in human and macaque are identified in this study, and their similarities and differences in spatial distribution, anatomical morphology, and functional connectivity were also dicussed.

    1. Neuroscience
    Avani Koparkar, Timothy L Warren ... Lena Veit
    Research Article

    Complex skills like speech and dance are composed of ordered sequences of simpler elements, but the neuronal basis for the syntactic ordering of actions is poorly understood. Birdsong is a learned vocal behavior composed of syntactically ordered syllables, controlled in part by the songbird premotor nucleus HVC (proper name). Here, we test whether one of HVC’s recurrent inputs, mMAN (medial magnocellular nucleus of the anterior nidopallium), contributes to sequencing in adult male Bengalese finches (Lonchura striata domestica). Bengalese finch song includes several patterns: (1) chunks, comprising stereotyped syllable sequences; (2) branch points, where a given syllable can be followed probabilistically by multiple syllables; and (3) repeat phrases, where individual syllables are repeated variable numbers of times. We found that following bilateral lesions of mMAN, acoustic structure of syllables remained largely intact, but sequencing became more variable, as evidenced by ‘breaks’ in previously stereotyped chunks, increased uncertainty at branch points, and increased variability in repeat numbers. Our results show that mMAN contributes to the variable sequencing of vocal elements in Bengalese finch song and demonstrate the influence of recurrent projections to HVC. Furthermore, they highlight the utility of species with complex syntax in investigating neuronal control of ordered sequences.