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Research Article

Regulation of arousal via online neurofeedback improves human performance in a demanding sensory-motor task

Josef Faller, Jennifer Cummings, Sameer Saproo, and View ORCID ProfilePaul Sajda
  1. aDepartment of Biomedical Engineering, Columbia University, New York, NY 10027;
  2. bData Science Institute, Columbia University, New York, NY 10027

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PNAS March 26, 2019 116 (13) 6482-6490; first published March 12, 2019; https://doi.org/10.1073/pnas.1817207116
Josef Faller
aDepartment of Biomedical Engineering, Columbia University, New York, NY 10027;
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  • For correspondence: josef.faller@gmail.com psajda@columbia.edu
Jennifer Cummings
aDepartment of Biomedical Engineering, Columbia University, New York, NY 10027;
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Sameer Saproo
aDepartment of Biomedical Engineering, Columbia University, New York, NY 10027;
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Paul Sajda
aDepartment of Biomedical Engineering, Columbia University, New York, NY 10027;
bData Science Institute, Columbia University, New York, NY 10027
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  • ORCID record for Paul Sajda
  • For correspondence: josef.faller@gmail.com psajda@columbia.edu
  1. Edited by Richard M. Shiffrin, Indiana University, Bloomington, IN, and approved February 19, 2019 (received for review October 6, 2018)

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    Fig. 1.

    Assumptions underlying our hypothesis. (A) If performance decrease during PIO is governed by the Yerkes–Dodson law, then down-regulation of arousal should improve performance. (B) The locus coeruleus–norepinephrine (LC-NE) system is believed to trigger a switch away from model exploitation to stochastic exploration, and thus hypothetically cause PIO, if arousal exceeds a threshold while ACC is in a state reflective of low model performance (17). Lowering arousal should impede this switch to stochastic exploration and thus lower PIO propensity. (C) Subjects typically fail along the way in sufficiently difficult BATs, but impeding PIOs by down-regulating arousal would hypothetically postpone failure and thus improve task performance.

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    Fig. 2.

    Setup of experiment and study protocol. (A) Study participants alternately guided a virtual aircraft through an easy or hard course of red rectangular boundaries (rings). Both courses were a maximum of 90 s long and increased in difficulty over time as ring sizes decreased. Missing a ring ended the flight trial immediately. Every new flight attempt was randomly assigned one of three feedback conditions. In the main condition (a) BCI, audio feedback from an EEG-based decoder was presented to the participant (closed-loop experiment). During the two control conditions (b) sham and (c) silence, partly random or no audio signal was presented, respectively. Participants were instructed to down-regulate their arousal as outlined at the bottom left of the panel. (B) During initial screening in session 1, only novice participants able to repeatedly fly through 66% of course type easy within 40 min were admitted for the main experiment in session 2. Session 2 started with 10 min of EEG collection while participants repeatedly attempted to fly through the easy course. The EEG-based decoder was then trained on these data and subsequently used to generate feedback in the main EEG experiment.

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    Fig. 3.

    Flight performance improved with veridical neurofeedback in the hard but not the easy course. (A) Flight time increased significantly relative to both control conditions sham and silence for course type hard, where sharply elevated levels of arousal are expected. (B) In the hard course, individual flight performance consistently increased with veridical neurofeedback relative to controls for all except three subjects. (C) For the easy course, for which subjects were trained and screened and where no strongly elevated arousal was expected, no significant differences were found between any of the conditions. (D) Individual performance with veridical feedback relative to control conditions in course type easy showed no clear trend for a systematic increase or decrease. Hinges of boxplots represent first and third quartile and whiskers span from smallest to largest value of the data but reach out no further than 1.5 times the interquartile range. Numbers over brackets between boxplots represent uncorrected P values of paired t tests. The pattern of significance does not change after Holm-based correction for six comparisons.

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    Fig. 4.

    Significant changes in pupil size and HRV were observed in condition BCI relative to control conditions during course type hard. (A) For course type hard, HRV was significantly higher in condition BCI relative to both control conditions, while (B) normalized pupil size was significantly lower in condition BCI relative to both control conditions. For course type easy no significant effects were found for (C) HRV or (D) pupil size. Hinges of boxplots represent first and third quartile and whiskers span from smallest to largest value of the data but reach out no further than 1.5 times the interquartile range. Numbers over brackets between boxplots represent uncorrected P values of paired t tests. Holm-based correction for six comparisons does not change the pattern of significance for HRV but elevates the P value of the paired comparison of normalized pupil size between conditions silence and BCI from P = 0.011 to PHolm = 0.057.

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Regulation of arousal via online neurofeedback improves human performance in a demanding sensory-motor task
Josef Faller, Jennifer Cummings, Sameer Saproo, Paul Sajda
Proceedings of the National Academy of Sciences Mar 2019, 116 (13) 6482-6490; DOI: 10.1073/pnas.1817207116

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Regulation of arousal via online neurofeedback improves human performance in a demanding sensory-motor task
Josef Faller, Jennifer Cummings, Sameer Saproo, Paul Sajda
Proceedings of the National Academy of Sciences Mar 2019, 116 (13) 6482-6490; DOI: 10.1073/pnas.1817207116
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Proceedings of the National Academy of Sciences: 116 (13)
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