Lesions of anterior cingulate cortex disrupt an electrophysiological signature of reward processing in humans

Oerlemans, J.; Alejandro, R. J.; Hemelsoet, D.; Genbrugge, E.; Bouche, K.; Defreyne, L.; De Herdt, V.; Holroyd, C. B.

doi:10.1101/2024.12.04.626789

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bioRxiv · 10.1101/2024.12.04.626789

Lesions of anterior cingulate cortex disrupt an electrophysiological signature of reward processing in humans

Oerlemans, J.·Alejandro, R. J.·Hemelsoet, D.·Genbrugge, E.·Bouche, K.·Defreyne, L.·De Herdt, V.·Holroyd, C. B.

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Abstract

The reward positivity (RewP) is an event-related brain potential (ERP) component associated with feedback and reward processing. Although the component is said to be generated in anterior cingulate cortex (ACC), this inference is disputed because of the inverse problem. Recently, by conducting a current source density analysis of intracranial electroencephalogram (EEG) data recorded from a large cohort of epilepsy patients, we provided direct evidence that the RewP is produced by a circumscribed region in caudal ACC corresponding to Brodmann areas 24c and 32. In the present study we confirm that this brain area is the source of the RewP by examining the effects of damage to frontal cortex on RewP amplitude. We recorded scalp EEG from 68 stroke patients with damage to frontal cortex while they engaged in a trial-and-error guessing task used to elicit a canonical RewP. Application of non-parametric voxel-based lesion-symptom mapping to the lesion data revealed that damage to Brodmann areas 24c and 32 attenuated RewP amplitude, whereas damage to other parts of frontal cortex did not affect it. These results provide causal evidence that the caudal ACC generates the RewP and underscore the contribution of this brain region toward motivating extended behaviours. Significance statementThe reward positivity (RewP) is an event-related brain potential component that reflects reward processing in the brain. Although multiple studies have suggested that anterior cingulate cortex (ACC) is the neural generator of the RewP, this assertion is disputed mainly because of the inverse problem. In this study, we present direct evidence that the RewP is generated in caudal ACC by performing voxel-based lesion-symptom mapping (VLSM) in a cohort of 68 stroke patients with lesions in the frontal lobe. We found that a circumscribed region in right caudal ACC was significantly associated with a reduced RewP, providing the first causal evidence that this region generates the RewP in humans. These fundings elucidate the central role ACC plays in motivating extended behaviours.

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Oerlemans, J., Alejandro, R. J., Hemelsoet, D., Genbrugge, E., Bouche, K., Defreyne, L., De Herdt, V., Holroyd, C. B.. 2024-12-07. Lesions of anterior cingulate cortex disrupt an electrophysiological signature of reward processing in humans. https://doi.org/10.1101/2024.12.04.626789

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