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Anterior Prefrontal Cortex Contributes to Action Selection through Tracking of Recent Reward Trends

Kovach, Christopher K. and Daw, Nathaniel D. and Rudrauf, David and Tranel, Daniel and O'Doherty, John P. and Adolphs, Ralph (2012) Anterior Prefrontal Cortex Contributes to Action Selection through Tracking of Recent Reward Trends. Journal of Neuroscience, 32 (25). pp. 8434-8442. ISSN 0270-6474. PMCID PMC3425366. doi:10.1523/JNEUROSCI.5468-11.2012.

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The functions of prefrontal cortex remain enigmatic, especially for its anterior sectors, putatively ranging from planning to self-initiated behavior, social cognition, task switching, and memory. A predominant current theory regarding the most anterior sector, the frontopolar cortex (FPC), is that it is involved in exploring alternative courses of action, but the detailed causal mechanisms remain unknown. Here we investigated this issue using the lesion method, together with a novel model-based analysis. Eight patients with anterior prefrontal brain lesions including the FPC performed a four-armed bandit task known from neuroimaging studies to activate the FPC. Model-based analyses of learning demonstrated a selective deficit in the ability to extrapolate the most recent trend, despite an intact general ability to learn from past rewards. Whereas both brain-damaged and healthy controls used comparisons between the two most recent choice outcomes to infer trends that influenced their decision about the next choice, the group with anterior prefrontal lesions showed a complete absence of this component and instead based their choice entirely on the cumulative reward history. Given that the FPC is thought to be the most evolutionarily recent expansion of primate prefrontal cortex, we suggest that its function may reflect uniquely human adaptations to select and update models of reward contingency in dynamic environments.

Item Type:Article
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URLURL TypeDescription CentralArticle
Kovach, Christopher K.0000-0002-0117-151X
O'Doherty, John P.0000-0003-0016-3531
Adolphs, Ralph0000-0002-8053-9692
Additional Information:© 2012 the authors. Received October 24, 2011. Revision received March 14, 2012. Accepted April 6, 2012. Supported by National Institute of Neurological Disorders and Stroke Grant P50 NS19632 (D.T., R.A.), National Institute on Drug Abuse Grant DA022549 (D.T.), National Institute of Mental Health Grant MH080721 (R.A.), and the Tamagawa University Global Centers of Excellence Program of the Japanese Ministry of Education, Culture, Sports, and Technology (C.K.K., R.A.). N.D.D. was supported by a Scholar Award from the McKnight Foundation and a Scholar Award from the James S. McDonnell Foundation. C.K.K. and N.D.D. contributed equally to this work. The authors declare no competing financial interests. Author contributions: N.D.D., J.P.O., and R.A. designed research; C.K.K. performed research; D.R. and D.T. contributed unpublished reagents/analytic tools; C.K.K., N.D.D., D.R., and D.T. analyzed data; C.K.K., N.D.D., and R.A. wrote the paper.
Funding AgencyGrant Number
NIHP50 NS19632
McKnight FoundationUNSPECIFIED
James S. McDonnell FoundationUNSPECIFIED
Tamagawa UniversityUNSPECIFIED
National Institute of Neurological Disorders and Stroke (NINDS)UNSPECIFIED
National Institute of Mental Health (NIMH)UNSPECIFIED
National Institute on Drug AbuseUNSPECIFIED
Issue or Number:25
PubMed Central ID:PMC3425366
Record Number:CaltechAUTHORS:20120716-085437939
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Official Citation:Christopher K. Kovach, Nathaniel D. Daw, David Rudrauf, Daniel Tranel, John P. O'Doherty, and Ralph Adolphs Anterior Prefrontal Cortex Contributes to Action Selection through Tracking of Recent Reward Trends The Journal of Neuroscience, 20 June 2012, 32(25):8434-8442; doi:10.1523/JNEUROSCI.5468-11.2012
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:32457
Deposited By: Ruth Sustaita
Deposited On:16 Jul 2012 16:45
Last Modified:09 Nov 2021 21:27

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