Human Anterior Insula Encodes Performance Feedback and Relays Prediction Error to the Medial Prefrontal Cortex

Author:

Billeke Pablo1,Ossandon Tomas23,Perrone-Bertolotti Marcela45,Kahane Philippe6,Bastin Julien7,Jerbi Karim8910,Lachaux Jean-Philippe11,Fuentealba Pablo2

Affiliation:

1. Laboratorio de Neurociencia Social y Neuromodulación, Centro de Investigación en Complejidad Social (neuroCICS), Facultad de Gobierno, Universidad del Desarrollo, Santiago CL 7610658, Chile

2. Departamento de Psiquiatría, Facultad de Medicina y Centro Interdisciplinario de Neurociencia, Pontificia Universidad Católica de Chile, Santiago CL 8330024, Chile

3. Institute of Biological and Medical Engineering, Pontificia Universidad Católica de Chile, Santiago CL 8330024, Chile

4. Université Grenoble Alpes, CNRS, LPNC UMR 5105, Grenoble 38000, France

5. Institut Universitaire de France

6. Université Grenoble Alpes, Inserm, U1216, CHU Grenoble Alpes, Grenoble Institut Neurosciences, Grenoble 38000, France

7. Université Grenoble Alpes, Inserm U1216, Grenoble Institut Neurosciences, Grenoble 38000, France

8. Cognitive & Computational Neuroscience Lab, Psychology Department, University of Montreal, Montreal, QC H3T 1L5, Canada

9. UNIQUE Research Center, QC, Canada

10. MILA (Quebec Artificial Intelligence Institute)

11. INSERM U1028, CNRS UMR5292, Brain Dynamics and Cognition Team, Lyon Neuroscience Research Center, Lyon, Bron 69004, France

Abstract

Abstract Adaptive behavior requires the comparison of outcome predictions with actual outcomes (e.g., performance feedback). This process of performance monitoring is computed by a distributed brain network comprising the medial prefrontal cortex (mPFC) and the anterior insular cortex (AIC). Despite being consistently co-activated during different tasks, the precise neuronal computations of each region and their interactions remain elusive. In order to assess the neural mechanism by which the AIC processes performance feedback, we recorded AIC electrophysiological activity in humans. We found that the AIC beta oscillations amplitude is modulated by the probability of performance feedback valence (positive or negative) given the context (task and condition difficulty). Furthermore, the valence of feedback was encoded by delta waves phase-modulating the power of beta oscillations. Finally, connectivity and causal analysis showed that beta oscillations relay feedback information signals to the mPFC. These results reveal that structured oscillatory activity in the anterior insula encodes performance feedback information, thus coordinating brain circuits related to reward-based learning.

Funder

CONICYT

FONDECYT

Canada Research Chairs

NSERC

New Investigators Award from FQNT

IVADO-Apogée fundamental research project

FRQNT Strategic Clusters Program

Publisher

Oxford University Press (OUP)

Subject

Cellular and Molecular Neuroscience,Cognitive Neuroscience

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