Brain activity, regional gray matter loss, and decision-making in multiple sclerosis

Martin Weygandt; Katharina Wakonig; Janina Behrens; Lil Meyer-Arndt; Eveline Söder; Alexander U Brandt; Judith Bellmann-Strobl; Klemens Ruprecht; Stefan M Gold; John-Dylan Haynes; Friedemann Paul

doi:10.1177/1352458517717089

Brain activity, regional gray matter loss, and decision-making in multiple sclerosis

Mult Scler. 2018 Aug;24(9):1163-1173. doi: 10.1177/1352458517717089. Epub 2017 Jun 28.

Affiliations

¹ Charité - Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health; Excellence Cluster NeuroCure; 10117 Berlin, Germany / Charité - Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health; Berlin Center for Advanced Neuroimaging, Department of Neurology; 10117 Berlin, Germany / Charité - Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health; Bernstein Center for Computational Neuroscience; 10117 Berlin, Germany.
² Charité - Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health; Excellence Cluster NeuroCure; 10117 Berlin, Germany.
³ Charité - Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health; Excellence Cluster NeuroCure; 10117 Berlin, Germany / Charité - Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health; Excellence Cluster NeuroCure; 10117 Berlin, Germany. / Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health; Clinical and Experimental Multiple Sclerosis Research Center, Department of Neurology; 10117 Berlin, Germany.
⁴ Department of Clinical Psychology and Psychotherapy, Institute of Psychology, University of Hamburg, Hamburg, Germany.
⁵ Charité - Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health; Excellence Cluster NeuroCure; 10117 Berlin, Germany / Experimental and Clinical Research Center, Max Delbrueck Center for Molecular Medicine and Charité - Universitätsmedizin Berlin, 13125 Berlin, Germany.
⁶ Charité - Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health; Clinical and Experimental Multiple Sclerosis Research Center, Department of Neurology; 10117 Berlin, Germany.
⁷ Charité - Institute of Neuroimmunology and Multiple Sclerosis (INIMS), Center for Molecular Neurobiology, University Medical Center, 20251 Hamburg, Germany / Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health; Department of Psychiatry and Psychotherapy, Campus Benjamin Franklin; 12203 Berlin, Germany.
⁸ Charité - Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health; Excellence Cluster NeuroCure; 10117 Berlin, Germany / Charité - Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health; Clinical and Experimental Multiple Sclerosis Research Center, Department of Neurology; 10117 Berlin, Germany / Experimental and Clinical Research Center, Max Delbrueck Center for Molecular Medicine and Charité - Universitätsmedizin Berlin, 13125 Berlin, Germany.

PMID: 28657480
DOI: 10.1177/1352458517717089

Abstract

Background: Decision-making (DM) abilities deteriorate with multiple sclerosis (MS) disease progression which impairs everyday life and is thus clinically important.

Objective: To investigate the underlying neurocognitive processes and their relation to regional gray matter (GM) loss induced by MS.

Methods: We used a functional magnetic resonance imaging (fMRI) Iowa Gambling Task to measure DM-related brain activity in 36 MS patients and 21 healthy controls (HC). From this activity, we determined neural parameters of two cognitive stages, a deliberation ("choice") period preceding a choice and a post-choice ("feedback") stage reporting decision outcomes. These measures were related to DM separately in intact and damaged GM areas as determined by a voxel-based morphometry analysis.

Results: Severely affected patients (with high lesion burden) showed worse DM-learning than HC ( t = -1.75, p = 0.045), moderately affected (low lesion burden) did not. Activity in the choice stage in intact insular ( t = 4.60, p_{Family-Wise Error [FWE] corrected} = 0.034), anterior cingulate ( t = 4.50, p_FWE = 0.044), and dorsolateral prefrontal areas ( t = 4.43, p_FWE = 0.049) and in insular areas with GM loss ( t = 3.78, p_FWE = 0.011) was positively linked to DM performance across patients with severe tissue damage and HC. Furthermore, activity in intact orbitofrontal areas was positively linked to DM-learning during the feedback stage across these participants ( t = 4.49, p_FWE = 0.032). During none of the stages, moderately affected patients showed higher activity than HC, which might have indicated preserved DM due to compensatory activity.

Conclusion: We identified dysregulated activity linked to impairment in specific cognitive stages of reward-related DM. The link of brain activity and impaired DM in areas with MS-induced GM loss suggests that this deficit might be tightly coupled to MS neuropathology.

Keywords: Iowa Gambling Task; Multiple sclerosis; brain activity; decision-making; functional magnetic resonance imaging; gray matter loss.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Adult
Decision Making / physiology*
Female
Gray Matter / diagnostic imaging
Gray Matter / pathology*
Humans
Magnetic Resonance Imaging
Male
Middle Aged
Multiple Sclerosis / complications
Multiple Sclerosis / diagnostic imaging
Multiple Sclerosis / pathology*