Frequency-specific changes in prefrontal activity associated with maladaptive belief updating in volatile environments in euthymic bipolar disorder
Abstract Bipolar disorder (BD) involves altered reward processing and decision-making, with inconsistencies across studies. Here, we integrated hierarchical Bayesian modelling with magnetoencephalography (MEG) to characterise maladaptive belief updating in this condition. First, we determined if pre...
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Nature Publishing Group
2025-01-01
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| Series: | Translational Psychiatry |
| Online Access: | https://doi.org/10.1038/s41398-025-03225-6 |
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| author | Marina Ivanova Ksenia Germanova Dmitry S. Petelin Aynur Ragimova Grigory Kopytin Beatrice A. Volel Vadim V. Nikulin Maria Herrojo Ruiz |
| author_facet | Marina Ivanova Ksenia Germanova Dmitry S. Petelin Aynur Ragimova Grigory Kopytin Beatrice A. Volel Vadim V. Nikulin Maria Herrojo Ruiz |
| author_sort | Marina Ivanova |
| collection | DOAJ |
| description | Abstract Bipolar disorder (BD) involves altered reward processing and decision-making, with inconsistencies across studies. Here, we integrated hierarchical Bayesian modelling with magnetoencephalography (MEG) to characterise maladaptive belief updating in this condition. First, we determined if previously reported increased learning rates in BD stem from a heightened expectation of environmental changes. Additionally, we examined if this increased expectation speeds up belief updating in decision-making, associated with modulation of rhythmic neural activity within the prefrontal, orbitofrontal, and anterior cingulate cortex (PFC, OFC, ACC). Twenty-two euthymic BD and 27 healthy control (HC) participants completed a reward-based motor decision-making task in a volatile setting. Hierarchical Bayesian modelling revealed BD participants anticipated greater environmental volatility, resulting in a more stochastic mapping from beliefs to actions and paralleled by lower win rates and a reduced tendency to repeat rewarded actions than HC. Despite this, BD individuals adjusted their expectations of action-outcome contingencies more slowly, but both groups invigorated their actions similarly. On a neural level, while healthy individuals exhibited an alpha-beta suppression and gamma increase during belief updating, BD participants showed dampened effects, extending across the PFC, OFC, and ACC regions. This was accompanied by an abnormally increased beta-band directed information flow in BD. Overall, the results suggest euthymic BD individuals anticipate environmental change without adequately learning from it, contributing to maladaptive belief updating. Alterations in frequency-domain amplitude and functional connectivity within the PFC, OFC, and ACC during belief updating underlie the computational effects and could serve as potential indicators for predicting relapse in future research. |
| format | Article |
| id | doaj-art-bd7f1280b781415faf810297aa8d238f |
| institution | Kabale University |
| issn | 2158-3188 |
| language | English |
| publishDate | 2025-01-01 |
| publisher | Nature Publishing Group |
| record_format | Article |
| series | Translational Psychiatry |
| spelling | doaj-art-bd7f1280b781415faf810297aa8d238f2025-01-19T12:39:38ZengNature Publishing GroupTranslational Psychiatry2158-31882025-01-0115111210.1038/s41398-025-03225-6Frequency-specific changes in prefrontal activity associated with maladaptive belief updating in volatile environments in euthymic bipolar disorderMarina Ivanova0Ksenia Germanova1Dmitry S. Petelin2Aynur Ragimova3Grigory Kopytin4Beatrice A. Volel5Vadim V. Nikulin6Maria Herrojo Ruiz7Institute for Cognitive Neuroscience, National Research University Higher School of EconomicsDepartment of Neurology, Max Planck Institute for Human Cognitive and Brain SciencesFirst Moscow State Medical UniversityInstitute for Cognitive Neuroscience, National Research University Higher School of EconomicsInstitute for Cognitive Neuroscience, National Research University Higher School of EconomicsFirst Moscow State Medical UniversityDepartment of Neurology, Max Planck Institute for Human Cognitive and Brain SciencesDepartment of Psychology, Goldsmiths University of LondonAbstract Bipolar disorder (BD) involves altered reward processing and decision-making, with inconsistencies across studies. Here, we integrated hierarchical Bayesian modelling with magnetoencephalography (MEG) to characterise maladaptive belief updating in this condition. First, we determined if previously reported increased learning rates in BD stem from a heightened expectation of environmental changes. Additionally, we examined if this increased expectation speeds up belief updating in decision-making, associated with modulation of rhythmic neural activity within the prefrontal, orbitofrontal, and anterior cingulate cortex (PFC, OFC, ACC). Twenty-two euthymic BD and 27 healthy control (HC) participants completed a reward-based motor decision-making task in a volatile setting. Hierarchical Bayesian modelling revealed BD participants anticipated greater environmental volatility, resulting in a more stochastic mapping from beliefs to actions and paralleled by lower win rates and a reduced tendency to repeat rewarded actions than HC. Despite this, BD individuals adjusted their expectations of action-outcome contingencies more slowly, but both groups invigorated their actions similarly. On a neural level, while healthy individuals exhibited an alpha-beta suppression and gamma increase during belief updating, BD participants showed dampened effects, extending across the PFC, OFC, and ACC regions. This was accompanied by an abnormally increased beta-band directed information flow in BD. Overall, the results suggest euthymic BD individuals anticipate environmental change without adequately learning from it, contributing to maladaptive belief updating. Alterations in frequency-domain amplitude and functional connectivity within the PFC, OFC, and ACC during belief updating underlie the computational effects and could serve as potential indicators for predicting relapse in future research.https://doi.org/10.1038/s41398-025-03225-6 |
| spellingShingle | Marina Ivanova Ksenia Germanova Dmitry S. Petelin Aynur Ragimova Grigory Kopytin Beatrice A. Volel Vadim V. Nikulin Maria Herrojo Ruiz Frequency-specific changes in prefrontal activity associated with maladaptive belief updating in volatile environments in euthymic bipolar disorder Translational Psychiatry |
| title | Frequency-specific changes in prefrontal activity associated with maladaptive belief updating in volatile environments in euthymic bipolar disorder |
| title_full | Frequency-specific changes in prefrontal activity associated with maladaptive belief updating in volatile environments in euthymic bipolar disorder |
| title_fullStr | Frequency-specific changes in prefrontal activity associated with maladaptive belief updating in volatile environments in euthymic bipolar disorder |
| title_full_unstemmed | Frequency-specific changes in prefrontal activity associated with maladaptive belief updating in volatile environments in euthymic bipolar disorder |
| title_short | Frequency-specific changes in prefrontal activity associated with maladaptive belief updating in volatile environments in euthymic bipolar disorder |
| title_sort | frequency specific changes in prefrontal activity associated with maladaptive belief updating in volatile environments in euthymic bipolar disorder |
| url | https://doi.org/10.1038/s41398-025-03225-6 |
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