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

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http://pubman.mpdl.mpg.de/cone/persons/resource/persons22901

Mathar,  David
Department Neurology, MPI for Human Cognitive and Brain Sciences, Max Planck Society;
Integrated Research and Treatment Center Adiposity Diseases, University of Leipzig, Germany;
Department of Psychology, University of Cologne, Germany;

http://pubman.mpdl.mpg.de/cone/persons/resource/persons19887

Neumann,  Jane
Department Neurology, MPI for Human Cognitive and Brain Sciences, Max Planck Society;
Integrated Research and Treatment Center Adiposity Diseases, University of Leipzig, Germany;
Department of Medical Engineering and Biotechnology, University of Applied Sciences, Jena, Germany;

http://pubman.mpdl.mpg.de/cone/persons/resource/persons20065

Villringer,  Arno
Department Neurology, MPI for Human Cognitive and Brain Sciences, Max Planck Society;
Integrated Research and Treatment Center Adiposity Diseases, University of Leipzig, Germany;
Clinic for Cognitive Neurology, University of Leipzig, Germany;
Berlin School of Mind and Brain, Humboldt University Berlin, Germany;

http://pubman.mpdl.mpg.de/cone/persons/resource/persons19734

Horstmann,  Annette
Department Neurology, MPI for Human Cognitive and Brain Sciences, Max Planck Society;
Integrated Research and Treatment Center Adiposity Diseases, University of Leipzig, Germany;

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Citation

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.


Cite as: http://hdl.handle.net/11858/00-001M-0000-002D-F4ED-7
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.