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Thalamocortical excitability adjustments guide human perception under uncertainty

View ORCID ProfileJulian Q. Kosciessa, View ORCID ProfileUlman Lindenberger, View ORCID ProfileDouglas D. Garrett
doi: https://doi.org/10.1101/2020.06.22.165118
Julian Q. Kosciessa
1Max Planck UCL Centre for Computational Psychiatry and Ageing Research, Berlin and London
2Center for Lifespan Psychology, Max Planck Institute for Human Development, Lentzeallee 94, 14195 Berlin, Germany
3Department of Psychology, Humboldt-Universität zu Berlin, Berlin, Germany
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  • For correspondence: kosciessa@mpib-berlin.mpg.de garrett@mpib-berlin.mpg.de
Ulman Lindenberger
1Max Planck UCL Centre for Computational Psychiatry and Ageing Research, Berlin and London
2Center for Lifespan Psychology, Max Planck Institute for Human Development, Lentzeallee 94, 14195 Berlin, Germany
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Douglas D. Garrett
1Max Planck UCL Centre for Computational Psychiatry and Ageing Research, Berlin and London
2Center for Lifespan Psychology, Max Planck Institute for Human Development, Lentzeallee 94, 14195 Berlin, Germany
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  • For correspondence: kosciessa@mpib-berlin.mpg.de garrett@mpib-berlin.mpg.de
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Abstract

Adaptive human behavior builds on prior knowledge about stimulus relevance. Some environments cue such knowledge more than others. To behave adaptively, observers need to flexibly adjust sensory processing to the degree of contextual uncertainty. We hypothesize that the neural basis for these perceptual adjustments consists in the ability of the cortical network to switch back and forth between a rhythmic state that serves selective processing, and a state of elevated asynchronous neural activity that boosts sensitivity. To test this hypothesis, we recorded non-invasive EEG and fMRI BOLD dynamics while 47 healthy young adults performed a parametric visual attention task with varying numbers of relevant stimulus features. Drift-diffusion modeling of response behavior and electrophysiological signatures revealed that greater contextual uncertainty lowered the rate of evidence accumulation while increasing thalamocortical engagement, with concomitant increments in cortical excitability and pupil dilation. As predicted, uncertainty-related processing adjustments were expressed as switches between a state of phase-dependent excitability modulation in the alpha band and a state of increased irregularity of brain dynamics. We conclude that humans dynamically adjust sensory excitability according to the processing fidelity afforded by an upcoming choice, and that neuromodulatory processes involving the thalamus play a key role in adjusting excitability in the human brain.

Highlights

  • With increasing contextual uncertainty, human cortical networks shift from a state of phase-dependent excitability modulation in the alpha band into a state of elevated excitatory tone and asynchronous neural activity

  • Evidence based on joint modeling of behavior, EEG, and BOLD suggests that neuromodulatory processes involving the thalamus regulate these shifts

  • Theoretical and empirical considerations suggest contributions of both frequency-specific and aperiodic neural dynamics to human behavior

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC 4.0 International license.
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Posted June 23, 2020.
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Thalamocortical excitability adjustments guide human perception under uncertainty
Julian Q. Kosciessa, Ulman Lindenberger, Douglas D. Garrett
bioRxiv 2020.06.22.165118; doi: https://doi.org/10.1101/2020.06.22.165118
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Thalamocortical excitability adjustments guide human perception under uncertainty
Julian Q. Kosciessa, Ulman Lindenberger, Douglas D. Garrett
bioRxiv 2020.06.22.165118; doi: https://doi.org/10.1101/2020.06.22.165118

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