Local cortical desynchronization and pupil-linked arousal differentially shape brain states for optimal sensory performance
Abstract
Instantaneous brain states have consequences for our sensation, perception, and behaviour. Fluctuations in arousal and neural desynchronization likely pose perceptually relevant states. However, their relationship and their relative impact on perception is unclear. We here show that, at the single-trial level in humans, local desynchronization in sensory cortex (expressed as time-series entropy) versus pupil-linked arousal differentially impact perceptual processing. While we recorded electroencephalography (EEG) and pupillometry data, stimuli of a demanding auditory discrimination task were presented into states of high or low desynchronization of auditory cortex via a real-time closed-loop setup. Desynchronization and arousal distinctly influenced stimulus-evoked activity and shaped behaviour displaying an inverted u-shaped relationship: States of intermediate desynchronization elicited minimal response bias and fastest responses, while states of intermediate arousal gave rise to highest response sensitivity. Our results speak to a model in which independent states of local desynchronization and global arousal jointly optimise sensory processing and performance.
Data availability
EEG data and pupillometry data are publicly available on the Open Science Framework (OSF) https://osf.io/f9kzs/. Custom computer code to reproduce all essential findings are publicly available on the OSF https://osf.io/f9kzs/
Article and author information
Author details
Funding
H2020 European Research Council (646696)
- Jonas Obleser
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Human subjects: Participants gave written informed consent to participate and consent to publish the recorded data in anonymised form. They were financially compensated.The study was approved by the local ethics committee of the University of Lübeck (reference number 15-313) and all experimental procedures were carried out in accordance with the registered protocol.
Reviewing Editor
- Jonathan Erik Peelle, Washington University in St. Louis, United States
Publication history
- Received: August 30, 2019
- Accepted: December 8, 2019
- Accepted Manuscript published: December 10, 2019 (version 1)
- Version of Record published: January 7, 2020 (version 2)
Copyright
© 2019, Waschke 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.
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Temporal synchrony of signals arriving from different neurons or brain regions is essential for proper neural processing. Nevertheless, it is not well understood how such synchrony is achieved and maintained in a complex network of time-delayed neural interactions. Myelin plasticity, accomplished by oligodendrocytes (OLs), has been suggested as an efficient mechanism for controlling timing in brain communications through adaptive changes of axonal conduction velocity and consequently conduction time delays, or latencies; however, local rules and feedback mechanisms that OLs use to achieve synchronization are not known. We propose a mathematical model of oligodendrocyte-mediated myelin plasticity (OMP) in which OLs play an active role in providing such feedback. This is achieved without using arrival times at the synapse or modulatory signaling from astrocytes; instead, it relies on the presence of global and transient OL responses to local action potentials in the axons they myelinate. While inspired by OL morphology, we provide the theoretical underpinnings that motivated the model and explore its performance for a wide range of its parameters. Our results indicate that when the characteristic time of OL’s transient intracellular responses to neural spikes is between 10 and 40 ms and the firing rates in individual axons are relatively low (⪅ 10 Hz), the OMP model efficiently synchronizes correlated and time-locked signals while latencies in axons carrying independent signals are unaffected. This suggests a novel form of selective synchronization in the CNS in which oligodendrocytes play an active role by modulating the conduction delays of correlated spike trains as they traverse to their targets.