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Normative Circuit Dynamics Across Human Cortex During Evidence Accumulation in Changing Environments

View ORCID ProfilePeter R Murphy, View ORCID ProfileNiklas Wilming, Diana C Hernandez-Bocanegra, View ORCID ProfileGenis Prat Ortega, View ORCID ProfileTobias H Donner
doi: https://doi.org/10.1101/2020.01.29.924795
Peter R Murphy
1Section Computational Cognitive Neuroscience, Department of Neurophysiology and Pathophysiology, University Medical Center Hamburg-Eppendorf, Martinisrasse 52, Hamburg 20251, Germany
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  • For correspondence: murphyp7@tcd.ie
Niklas Wilming
1Section Computational Cognitive Neuroscience, Department of Neurophysiology and Pathophysiology, University Medical Center Hamburg-Eppendorf, Martinisrasse 52, Hamburg 20251, Germany
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Diana C Hernandez-Bocanegra
1Section Computational Cognitive Neuroscience, Department of Neurophysiology and Pathophysiology, University Medical Center Hamburg-Eppendorf, Martinisrasse 52, Hamburg 20251, Germany
2Interactive Systems Group, Department of Computer Science and Applied Cognitive Science (INKO), University of Duisburg-Essen, Forsthausweg 2, Duisburg 47057, Germany
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Genis Prat Ortega
3Institut D’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Carrer del Rosselló 149, 08036 Barcelona, Spain
4Centre de Recerca Matematica, Campus UAB Edifici C, 08193 Bellaterra, Barcelona
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Tobias H Donner
1Section Computational Cognitive Neuroscience, Department of Neurophysiology and Pathophysiology, University Medical Center Hamburg-Eppendorf, Martinisrasse 52, Hamburg 20251, Germany
5Bernstein Center for Computational Neuroscience, Charité Universitätsmedizin, Haus 6, Philippstraße 13, 10115, Berlin, Germany
6Department of Psychology, University of Amsterdam, Weesperplein 4, 1018 XA, Amsterdam, The Netherlands
7Amsterdam Brain and Cognition, University of Amsterdam, Nieuwe Achtergracht 129, 1018 WS, Amsterdam, The Netherlands
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Abstract

Decision-making under uncertainty commonly entails the accumulation of decision-relevant ‘evidence’ over time. In natural environments, this accumulation process is complicated by the existence of hidden changes in the state of the environment. Optimal behavior in such contexts requires a rapid, non-linear tuning of the evidence accumulation. The neural basis of this adaptive computation has remained elusive. Here, we unraveled the underlying mechanisms across sensory, associative, and motor regions of the human cerebral cortex. We combined a visuo-motor choice task with hidden changes in the evidence source, monitoring of pupil-linked arousal, and model-based analysis of behavior and cortical population activity (assessed with magnetoencephalography). We found that normative, non-linear evidence accumulation results from the interplay of recurrent cortical dynamics and phasic arousal signals from ascending brainstem systems. Our insights forge a strong connection between normative computations for adaptive decision-making and the large-scale neural mechanisms for their implementation.

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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 4.0 International license.
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Posted January 30, 2020.
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Normative Circuit Dynamics Across Human Cortex During Evidence Accumulation in Changing Environments
Peter R Murphy, Niklas Wilming, Diana C Hernandez-Bocanegra, Genis Prat Ortega, Tobias H Donner
bioRxiv 2020.01.29.924795; doi: https://doi.org/10.1101/2020.01.29.924795
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Normative Circuit Dynamics Across Human Cortex During Evidence Accumulation in Changing Environments
Peter R Murphy, Niklas Wilming, Diana C Hernandez-Bocanegra, Genis Prat Ortega, Tobias H Donner
bioRxiv 2020.01.29.924795; doi: https://doi.org/10.1101/2020.01.29.924795

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