Mathar, David ORCID: 0000-0003-3411-7867, Neumann, Jane, Villringer, Arno and Horstmann, Annette ORCID: 0000-0001-6184-8484 (2017). Failing to learn from negative prediction errors: Obesity is associated with alterations in a fundamental neural learning mechanism. Cortex, 95. S. 222 - 238. MILANO: ELSEVIER MASSON. ISSN 1973-8102

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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. (C) 2017 Elsevier Ltd. All rights reserved.

Item Type: Journal Article
Creators:
CreatorsEmailORCIDORCID Put Code
Mathar, DavidUNSPECIFIEDorcid.org/0000-0003-3411-7867UNSPECIFIED
Neumann, JaneUNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Villringer, ArnoUNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Horstmann, AnnetteUNSPECIFIEDorcid.org/0000-0001-6184-8484UNSPECIFIED
URN: urn:nbn:de:hbz:38-216420
DOI: 10.1016/j.cortex.2017.08.022
Journal or Publication Title: Cortex
Volume: 95
Page Range: S. 222 - 238
Date: 2017
Publisher: ELSEVIER MASSON
Place of Publication: MILANO
ISSN: 1973-8102
Language: English
Faculty: Unspecified
Divisions: Unspecified
Subjects: no entry
Uncontrolled Keywords:
KeywordsLanguage
DIET-INDUCED OBESITY; POSITRON-EMISSION-TOMOGRAPHY; D-2/3 RECEPTOR AVAILABILITY; BASAL GANGLIA; PARKINSONS-DISEASE; NUCLEUS-ACCUMBENS; DOPAMINE RELEASE; D2 DOPAMINE; FUNCTIONAL CONNECTIVITY; INSULIN SENSITIVITYMultiple languages
Behavioral Sciences; Neurosciences; Psychology, ExperimentalMultiple languages
Refereed: Yes
URI: http://kups.ub.uni-koeln.de/id/eprint/21642

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