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The Neural Correlates of Cued Reward Omission

Compared to our understanding of positive prediction error signals occurring due to unexpected reward outcomes, less is known about the neural circuitry in humans that drives negative prediction errors during omission of expected rewards. While classical learning theories such as Rescorla–Wagner or...

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Autores principales: Mollick, Jessica A., Chang, Luke J., Krishnan, Anjali, Hazy, Thomas E., Krueger, Kai A., Frank, Guido K. W., Wager, Tor D., O’Reilly, Randall C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7928384/
https://www.ncbi.nlm.nih.gov/pubmed/33679345
http://dx.doi.org/10.3389/fnhum.2021.615313
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author Mollick, Jessica A.
Chang, Luke J.
Krishnan, Anjali
Hazy, Thomas E.
Krueger, Kai A.
Frank, Guido K. W.
Wager, Tor D.
O’Reilly, Randall C.
author_facet Mollick, Jessica A.
Chang, Luke J.
Krishnan, Anjali
Hazy, Thomas E.
Krueger, Kai A.
Frank, Guido K. W.
Wager, Tor D.
O’Reilly, Randall C.
author_sort Mollick, Jessica A.
collection PubMed
description Compared to our understanding of positive prediction error signals occurring due to unexpected reward outcomes, less is known about the neural circuitry in humans that drives negative prediction errors during omission of expected rewards. While classical learning theories such as Rescorla–Wagner or temporal difference learning suggest that both types of prediction errors result from a simple subtraction, there has been recent evidence suggesting that different brain regions provide input to dopamine neurons which contributes to specific components of this prediction error computation. Here, we focus on the brain regions responding to negative prediction error signals, which has been well-established in animal studies to involve a distinct pathway through the lateral habenula. We examine the activity of this pathway in humans, using a conditioned inhibition paradigm with high-resolution functional MRI. First, participants learned to associate a sensory stimulus with reward delivery. Then, reward delivery was omitted whenever this stimulus was presented simultaneously with a different sensory stimulus, the conditioned inhibitor (CI). Both reward presentation and the reward-predictive cue activated midbrain dopamine regions, insula and orbitofrontal cortex. While we found significant activity at an uncorrected threshold for the CI in the habenula, consistent with our predictions, it did not survive correction for multiple comparisons and awaits further replication. Additionally, the pallidum and putamen regions of the basal ganglia showed modulations of activity for the inhibitor that did not survive the corrected threshold.
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spelling pubmed-79283842021-03-04 The Neural Correlates of Cued Reward Omission Mollick, Jessica A. Chang, Luke J. Krishnan, Anjali Hazy, Thomas E. Krueger, Kai A. Frank, Guido K. W. Wager, Tor D. O’Reilly, Randall C. Front Hum Neurosci Neuroscience Compared to our understanding of positive prediction error signals occurring due to unexpected reward outcomes, less is known about the neural circuitry in humans that drives negative prediction errors during omission of expected rewards. While classical learning theories such as Rescorla–Wagner or temporal difference learning suggest that both types of prediction errors result from a simple subtraction, there has been recent evidence suggesting that different brain regions provide input to dopamine neurons which contributes to specific components of this prediction error computation. Here, we focus on the brain regions responding to negative prediction error signals, which has been well-established in animal studies to involve a distinct pathway through the lateral habenula. We examine the activity of this pathway in humans, using a conditioned inhibition paradigm with high-resolution functional MRI. First, participants learned to associate a sensory stimulus with reward delivery. Then, reward delivery was omitted whenever this stimulus was presented simultaneously with a different sensory stimulus, the conditioned inhibitor (CI). Both reward presentation and the reward-predictive cue activated midbrain dopamine regions, insula and orbitofrontal cortex. While we found significant activity at an uncorrected threshold for the CI in the habenula, consistent with our predictions, it did not survive correction for multiple comparisons and awaits further replication. Additionally, the pallidum and putamen regions of the basal ganglia showed modulations of activity for the inhibitor that did not survive the corrected threshold. Frontiers Media S.A. 2021-02-11 /pmc/articles/PMC7928384/ /pubmed/33679345 http://dx.doi.org/10.3389/fnhum.2021.615313 Text en Copyright © 2021 Mollick, Chang, Krishnan, Hazy, Krueger, Frank, Wager and O’Reilly. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Mollick, Jessica A.
Chang, Luke J.
Krishnan, Anjali
Hazy, Thomas E.
Krueger, Kai A.
Frank, Guido K. W.
Wager, Tor D.
O’Reilly, Randall C.
The Neural Correlates of Cued Reward Omission
title The Neural Correlates of Cued Reward Omission
title_full The Neural Correlates of Cued Reward Omission
title_fullStr The Neural Correlates of Cued Reward Omission
title_full_unstemmed The Neural Correlates of Cued Reward Omission
title_short The Neural Correlates of Cued Reward Omission
title_sort neural correlates of cued reward omission
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7928384/
https://www.ncbi.nlm.nih.gov/pubmed/33679345
http://dx.doi.org/10.3389/fnhum.2021.615313
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