Human Anterior Insula Encodes Performance Feedback and Relays Prediction Error to the Medial Prefrontal Cortex
Journal
Cerebral Cortex
ISSN
1047-3211
1460-2199
Date Issued
2020
Author(s)
Tomas Ossandon
Marcela Perrone-Bertolotti
Philippe Kahane
Julien Bastin
Karim Jerbi
Jean-Philippe Lachaux
Pablo Fuentealba
Type
Resource Types::text::journal::journal article
Abstract
<jats:title>Abstract</jats:title>
<jats:p>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.</jats:p>
<jats:p>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.</jats:p>
Subjects
beta oscillations
;
error monitoring
;
feedback
;
insula
;
intracortical recording
;
adaptation, psychological
;
adolescent
;
adult
;
beta rhythm
;
decision making
;
drug resistant epilepsy
;
electrocorticography
;
feedback, psychological
;
female
;
formative feedback
;
humans
;
insular cortex
;
male
;
memory, short-term
;
middle aged
;
prefrontal cortex
;
reading
;
spatial memory
;
young adult
;
anterior insula
;
article
;
delta rhythm
;
human
;
learning
;
medial prefrontal cortex
;
oscillation
;
prediction
;
probability
;
reward
;
adolescent
;
adult
;
beta rhythm
;
constructive feedback
;
coping behavior
;
decision making
;
drug resistant epilepsy
;
electrocorticography
;
female
;
insula
;
male
;
middle aged
;
physiology
;
prefrontal cortex
;
psychological feedback
;
reading
;
short term memory
;
spatial memory
;
young adult