Altered functional connectivity during performance feedback processing in multiple sclerosis
Effective learning from performance feedback is vital for adaptive behavior regulation necessary for successful cognitive performance. Yet, how this learning operates in clinical groups that experience cognitive dysfunction is not well understood. Multiple sclerosis (MS) is an autoimmune, degenerati...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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Elsevier
2023-01-01
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| Series: | NeuroImage: Clinical |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S2213158222003527 |
| _version_ | 1797869775716614144 |
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| author | Christopher J. Cagna Ahmet O. Ceceli Joshua Sandry Jamil P. Bhanji Elizabeth Tricomi Ekaterina Dobryakova |
| author_facet | Christopher J. Cagna Ahmet O. Ceceli Joshua Sandry Jamil P. Bhanji Elizabeth Tricomi Ekaterina Dobryakova |
| author_sort | Christopher J. Cagna |
| collection | DOAJ |
| description | Effective learning from performance feedback is vital for adaptive behavior regulation necessary for successful cognitive performance. Yet, how this learning operates in clinical groups that experience cognitive dysfunction is not well understood. Multiple sclerosis (MS) is an autoimmune, degenerative disease of the central nervous system characterized by physical and cognitive dysfunction. A highly prevalent impairment in MS is cognitive fatigue (CF). CF is associated with altered functioning within cortico-striatal regions that also facilitate feedback-based learning in neurotypical (NT) individuals. Despite this cortico-striatal overlap, research about feedback-based learning in MS, its associated neural underpinnings, and its sensitivity to CF, are all lacking. The present study investigated feedback-based learning ability in MS, as well as associated cortico-striatal function and connectivity. MS and NT participants completed a functional magnetic resonance imaging (fMRI) paired-word association task during which they received trial-by-trial monetary, non-monetary, and uninformative performance feedback. Despite reporting greater CF throughout the task, MS participants displayed comparable task performance to NTs, suggesting preserved feedback-based learning ability in the MS group. Both groups recruited the ventral striatum (VS), caudate nucleus, and ventromedial prefrontal cortex in response to the receipt of performance feedback, suggesting that people with MS also recruit cortico-striatal regions during feedback-based learning. However, compared to NT participants, MS participants also displayed stronger functional connectivity between the VS and task-relevant regions, including the left angular gyrus and right superior temporal gyrus, in response to feedback receipt. Results indicate that CF may not interfere with feedback-based learning in MS. Nonetheless, people with MS may recruit alternative connections with the striatum to assist with this form of learning. These findings have implications for cognitive rehabilitation treatments that incorporate performance feedback to remediate cognitive dysfunction in clinical populations. |
| first_indexed | 2024-04-10T00:18:08Z |
| format | Article |
| id | doaj.art-ad63708a24ef45d9ba9555fde86ad64e |
| institution | Directory Open Access Journal |
| issn | 2213-1582 |
| language | English |
| last_indexed | 2024-04-10T00:18:08Z |
| publishDate | 2023-01-01 |
| publisher | Elsevier |
| record_format | Article |
| series | NeuroImage: Clinical |
| spelling | doaj.art-ad63708a24ef45d9ba9555fde86ad64e2023-03-16T05:03:54ZengElsevierNeuroImage: Clinical2213-15822023-01-0137103287Altered functional connectivity during performance feedback processing in multiple sclerosisChristopher J. Cagna0Ahmet O. Ceceli1Joshua Sandry2Jamil P. Bhanji3Elizabeth Tricomi4Ekaterina Dobryakova5Department of Psychology, Rutgers University – Newark, 101 Warren Street, Newark, NJ 07102, United States; Corresponding author.Department of Psychiatry, Icahn School of Medicine at Mount Sinai, 1 Gustave L. Levy Place, New York, NY 10029, United StatesDepartment of Psychology, Montclair State University, 1 Normal Avenue, Montclair, NJ 07043, United StatesDepartment of Psychology, Rutgers University – Newark, 101 Warren Street, Newark, NJ 07102, United StatesDepartment of Psychology, Rutgers University – Newark, 101 Warren Street, Newark, NJ 07102, United StatesCenter for Traumatic Brain Injury Research, Kessler Foundation, 120 Eagle Rock Avenue, East Hanover, NJ 07936, United StatesEffective learning from performance feedback is vital for adaptive behavior regulation necessary for successful cognitive performance. Yet, how this learning operates in clinical groups that experience cognitive dysfunction is not well understood. Multiple sclerosis (MS) is an autoimmune, degenerative disease of the central nervous system characterized by physical and cognitive dysfunction. A highly prevalent impairment in MS is cognitive fatigue (CF). CF is associated with altered functioning within cortico-striatal regions that also facilitate feedback-based learning in neurotypical (NT) individuals. Despite this cortico-striatal overlap, research about feedback-based learning in MS, its associated neural underpinnings, and its sensitivity to CF, are all lacking. The present study investigated feedback-based learning ability in MS, as well as associated cortico-striatal function and connectivity. MS and NT participants completed a functional magnetic resonance imaging (fMRI) paired-word association task during which they received trial-by-trial monetary, non-monetary, and uninformative performance feedback. Despite reporting greater CF throughout the task, MS participants displayed comparable task performance to NTs, suggesting preserved feedback-based learning ability in the MS group. Both groups recruited the ventral striatum (VS), caudate nucleus, and ventromedial prefrontal cortex in response to the receipt of performance feedback, suggesting that people with MS also recruit cortico-striatal regions during feedback-based learning. However, compared to NT participants, MS participants also displayed stronger functional connectivity between the VS and task-relevant regions, including the left angular gyrus and right superior temporal gyrus, in response to feedback receipt. Results indicate that CF may not interfere with feedback-based learning in MS. Nonetheless, people with MS may recruit alternative connections with the striatum to assist with this form of learning. These findings have implications for cognitive rehabilitation treatments that incorporate performance feedback to remediate cognitive dysfunction in clinical populations.http://www.sciencedirect.com/science/article/pii/S2213158222003527Multiple sclerosisfMRIFeedbackCognitive fatigueRewardStriatum |
| spellingShingle | Christopher J. Cagna Ahmet O. Ceceli Joshua Sandry Jamil P. Bhanji Elizabeth Tricomi Ekaterina Dobryakova Altered functional connectivity during performance feedback processing in multiple sclerosis NeuroImage: Clinical Multiple sclerosis fMRI Feedback Cognitive fatigue Reward Striatum |
| title | Altered functional connectivity during performance feedback processing in multiple sclerosis |
| title_full | Altered functional connectivity during performance feedback processing in multiple sclerosis |
| title_fullStr | Altered functional connectivity during performance feedback processing in multiple sclerosis |
| title_full_unstemmed | Altered functional connectivity during performance feedback processing in multiple sclerosis |
| title_short | Altered functional connectivity during performance feedback processing in multiple sclerosis |
| title_sort | altered functional connectivity during performance feedback processing in multiple sclerosis |
| topic | Multiple sclerosis fMRI Feedback Cognitive fatigue Reward Striatum |
| url | http://www.sciencedirect.com/science/article/pii/S2213158222003527 |
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