Anatomical dissociation of intracerebral signals for reward and punishment prediction errors in humans

Maëlle C. M. Gueguen, Alizée Lopez-Persem, Pablo Billeke, Jean-Philippe Lachaux, Sylvain Rheims, Philippe Kahane, Lorella Minotti, Olivier David, Mathias Pessiglione and Julien Bastin ()
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Maëlle C. M. Gueguen: Univ. Grenoble Alpes, Inserm, U1216, Grenoble Institut Neurosciences, GIN
Alizée Lopez-Persem: Frontal Function and Pathology team, Institut du Cerveau, Sorbonne Université, INSERM U 1127, CNRS UMR 7225
Pablo Billeke: División de Neurociencia, Centro de Investigación en Complejidad Social (neuroCICS), Facultad de Gobierno, Universidad del Desarrollo
Jean-Philippe Lachaux: Lyon Neuroscience Research Center, Brain Dynamics and Cognition team, DYCOG INSERM UMRS 1028, CNRS UMR 5292, Université de Lyon
Sylvain Rheims: Hospices Civils de Lyon and University of Lyon
Philippe Kahane: Univ. Grenoble Alpes, Inserm, U1216, CHU Grenoble Alpes, Grenoble Institut Neurosciences, GIN
Lorella Minotti: Univ. Grenoble Alpes, Inserm, U1216, CHU Grenoble Alpes, Grenoble Institut Neurosciences, GIN
Olivier David: Univ. Grenoble Alpes, Inserm, U1216, Grenoble Institut Neurosciences, GIN
Mathias Pessiglione: Institut du Cerveau et de la Moelle épinière, Hôpital de la Pitié-Salpêtrière
Julien Bastin: Univ. Grenoble Alpes, Inserm, U1216, Grenoble Institut Neurosciences, GIN

Nature Communications, 2021, vol. 12, issue 1, 1-12

Abstract: Abstract Whether maximizing rewards and minimizing punishments rely on distinct brain systems remains debated, given inconsistent results coming from human neuroimaging and animal electrophysiology studies. Bridging the gap across techniques, we recorded intracerebral activity from twenty participants while they performed an instrumental learning task. We found that both reward and punishment prediction errors (PE), estimated from computational modeling of choice behavior, correlate positively with broadband gamma activity (BGA) in several brain regions. In all cases, BGA scaled positively with the outcome (reward or punishment versus nothing) and negatively with the expectation (predictability of reward or punishment). However, reward PE were better signaled in some regions (such as the ventromedial prefrontal and lateral orbitofrontal cortex), and punishment PE in other regions (such as the anterior insula and dorsolateral prefrontal cortex). These regions might therefore belong to brain systems that differentially contribute to the repetition of rewarded choices and the avoidance of punished choices.

Date: 2021
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DOI: 10.1038/s41467-021-23704-w

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