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  Failing to learn from negative prediction errors: Obesity is associated with alterations in a fundamental neural learning mechanism

Mathar, D., Neumann, J., Villringer, A., & Horstmann, A. (2017). Failing to learn from negative prediction errors: Obesity is associated with alterations in a fundamental neural learning mechanism. Cortex, 95, 222-237. doi:10.1016/j.cortex.2017.08.022.

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Item Permalink: http://hdl.handle.net/11858/00-001M-0000-002D-F4ED-7 Version Permalink: http://hdl.handle.net/21.11116/0000-0003-B452-5
Genre: Journal Article

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 Creators:
Mathar, David1, 2, 3, Author              
Neumann, Jane1, 2, 4, Author              
Villringer, Arno1, 2, 5, 6, Author              
Horstmann, Annette1, 2, Author              
Affiliations:
1Department Neurology, MPI for Human Cognitive and Brain Sciences, Max Planck Society, ou_634549              
2Integrated Research and Treatment Center Adiposity Diseases, University of Leipzig, Germany, ou_persistent22              
3Department of Psychology, University of Cologne, Germany, ou_persistent22              
4Department of Medical Engineering and Biotechnology, University of Applied Sciences, Jena, Germany, ou_persistent22              
5Clinic for Cognitive Neurology, University of Leipzig, Germany, ou_persistent22              
6Berlin School of Mind and Brain, Humboldt University Berlin, Germany, ou_persistent22              

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Free keywords: Procedural stimulus-response learning; Prediction errors; Computational modeling; Obesity; Imaging
 Abstract: Prediction errors (PEs) encode the difference between expected and actual action outcomes in the brain via dopaminergic modulation. Integration of these learning signals ensures efficient behavioral adaptation. Obesity has recently been linked to altered dopaminergic fronto-striatal circuits, thus implying impairments in cognitive domains that rely on its integrity. 28 obese and 30 lean human participants performed an implicit stimulus-response learning paradigm inside an fMRI scanner. Computational modeling and psycho-physiological interaction (PPI) analysis was utilized for assessing PE-related learning and associated functional connectivity. We show that human obesity is associated with insufficient incorporation of negative PEs into behavioral adaptation even in a non-food context, suggesting differences in a fundamental neural learning mechanism. Obese subjects were less efficient in using negative PEs to improve implicit learning performance, despite proper coding of PEs in striatum. We further observed lower functional coupling between ventral striatum and supplementary motor area in obese subjects subsequent to negative PEs. Importantly, strength of functional coupling predicted task performance and negative PE utilization. These findings show that obesity is linked to insufficient behavioral adaptation specifically in response to negative PEs, and to associated alterations in function and connectivity within the fronto-striatal system. Recognition of neural differences as a central characteristic of obesity hopefully paves the way to rethink established intervention strategies: Differential behavioral sensitivity to negative and positive PEs should be considered when designing intervention programs. Measures relying on penalization of unwanted behavior may prove less effective in obese subjects than alternative approaches.

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Language(s): eng - English
 Dates: 2017-06-142017-01-092017-08-172017-08-242017-10
 Publication Status: Published in print
 Pages: -
 Publishing info: -
 Table of Contents: -
 Rev. Method: Peer
 Identifiers: DOI: 10.1016/j.cortex.2017.08.022
PMID: 28917135
Other: Epub 2017
 Degree: -

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Project name : -
Grant ID : 01EO1001
Funding program : -
Funding organization : IFB Adiposity Diseases, German Federal Ministry of Education and Research (BMBF)
Project name : Obesity Mechanisms / SFB 1052
Grant ID : -
Funding program : -
Funding organization : German Research Foundation (DFG)
Project name : -
Grant ID : -
Funding program : -
Funding organization : FAZIT-STIFTUNG
Project name : -
Grant ID : -
Funding program : Landesstipendium
Funding organization : Free State of Saxony

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Title: Cortex
  Other : Cortex
Source Genre: Journal
 Creator(s):
Affiliations:
Publ. Info: Milan [etc.] : Elsevier Masson SAS
Pages: - Volume / Issue: 95 Sequence Number: - Start / End Page: 222 - 237 Identifier: ISSN: 0010-9452
CoNE: https://pure.mpg.de/cone/journals/resource/954925393344