Frequency-specific Changes in Prefrontal Activity Associated with Maladaptive Belief Updating in Volatile Environments in Euthymic Bipolar Disorder

Overview

Journal Transl Psychiatry

Date 2025 Jan 17

PMID 39824803

Authors

Marina Ivanova

Ksenia Germanova

Dmitry S Petelin

Aynur Ragimova

Grigory Kopytin

Beatrice A Volel

Vadim V Nikulin

Maria Herrojo Ruiz

Affiliations

Soon will be listed here.

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.

References

Ossola P, Garrett N, Sharot T, Marchesi C . Belief updating in bipolar disorder predicts time of recurrence. Elife. 2020; 9. PMC: 7655098. DOI: 10.7554/eLife.58891. View

Hein T, Gong Z, Ivanova M, Fedele T, Nikulin V, Ruiz M . Anterior cingulate and medial prefrontal cortex oscillations underlie learning alterations in trait anxiety in humans. Commun Biol. 2023; 6(1):271. PMC: 10017780. DOI: 10.1038/s42003-023-04628-1. View

de Berker A, Rutledge R, Mathys C, Marshall L, Cross G, Dolan R . Computations of uncertainty mediate acute stress responses in humans. Nat Commun. 2016; 7:10996. PMC: 4820542. DOI: 10.1038/ncomms10996. View

Tecilla M, Grossbach M, Gentile G, Holland P, Sporn S, Antonini A . Modulation of Motor Vigor by Expectation of Reward Probability Trial-by-Trial Is Preserved in Healthy Ageing and Parkinson's Disease Patients. J Neurosci. 2023; 43(10):1757-1777. PMC: 10010462. DOI: 10.1523/JNEUROSCI.1583-22.2022. View

Sedley W, Gander P, Kumar S, Kovach C, Oya H, Kawasaki H . Neural signatures of perceptual inference. Elife. 2016; 5:e11476. PMC: 4841773. DOI: 10.7554/eLife.11476. View

Adida M, Jollant F, Clark L, Guillaume S, Goodwin G, Azorin J . Lithium might be associated with better decision-making performance in euthymic bipolar patients. Eur Neuropsychopharmacol. 2015; 25(6):788-97. DOI: 10.1016/j.euroneuro.2015.03.003. View

Roberts M, Lowet E, Brunet N, Ter Wal M, Tiesinga P, Fries P . Robust gamma coherence between macaque V1 and V2 by dynamic frequency matching. Neuron. 2013; 78(3):523-36. DOI: 10.1016/j.neuron.2013.03.003. View

Acuff H, Versace A, Bertocci M, Ladouceur C, Hanford L, Manelis A . Baseline and follow-up activity and functional connectivity in reward neural circuitries in offspring at risk for bipolar disorder. Neuropsychopharmacology. 2019; 44(9):1570-1578. PMC: 6785101. DOI: 10.1038/s41386-019-0339-2. View

Michalareas G, Vezoli J, van Pelt S, Schoffelen J, Kennedy H, Fries P . Alpha-Beta and Gamma Rhythms Subserve Feedback and Feedforward Influences among Human Visual Cortical Areas. Neuron. 2016; 89(2):384-97. PMC: 4871751. DOI: 10.1016/j.neuron.2015.12.018. View

10.

Rouault M, Drugowitsch J, Koechlin E . Prefrontal mechanisms combining rewards and beliefs in human decision-making. Nat Commun. 2019; 10(1):301. PMC: 6336816. DOI: 10.1038/s41467-018-08121-w. View

11.

Pellegrini F, Delorme A, Nikulin V, Haufe S . Identifying good practices for detecting inter-regional linear functional connectivity from EEG. Neuroimage. 2023; 277:120218. PMC: 10374983. DOI: 10.1016/j.neuroimage.2023.120218. View

12.

Spitzer B, Blankenburg F, Summerfield C . Rhythmic gain control during supramodal integration of approximate number. Neuroimage. 2015; 129:470-479. DOI: 10.1016/j.neuroimage.2015.12.024. View

13.

Clark J, Watson S, Friston K . What is mood? A computational perspective. Psychol Med. 2018; 48(14):2277-2284. PMC: 6340107. DOI: 10.1017/S0033291718000430. View

14.

Taulu S, Hari R . Removal of magnetoencephalographic artifacts with temporal signal-space separation: demonstration with single-trial auditory-evoked responses. Hum Brain Mapp. 2008; 30(5):1524-34. PMC: 6871056. DOI: 10.1002/hbm.20627. View

15.

Gorrindo T, Blair R, Budhani S, Dickstein D, Pine D, Leibenluft E . Deficits on a probabilistic response-reversal task in patients with pediatric bipolar disorder. Am J Psychiatry. 2005; 162(10):1975-7. DOI: 10.1176/appi.ajp.162.10.1975. View

16.

Ethridge L, Hamm J, Shapiro J, Summerfelt A, Keedy S, Stevens M . Neural activations during auditory oddball processing discriminating schizophrenia and psychotic bipolar disorder. Biol Psychiatry. 2012; 72(9):766-74. PMC: 3465513. DOI: 10.1016/j.biopsych.2012.03.034. View

17.

Ozerdem A, Guntekin B, Tunca Z, Basar E . Brain oscillatory responses in patients with bipolar disorder manic episode before and after valproate treatment. Brain Res. 2008; 1235:98-108. DOI: 10.1016/j.brainres.2008.06.101. View

18.

Rolls E, Deco G, Huang C, Feng J . The human orbitofrontal cortex, vmPFC, and anterior cingulate cortex effective connectome: emotion, memory, and action. Cereb Cortex. 2022; 33(2):330-356. DOI: 10.1093/cercor/bhac070. View

19.

Frassle S, Aponte E, Bollmann S, Brodersen K, Do C, Harrison O . TAPAS: An Open-Source Software Package for Translational Neuromodeling and Computational Psychiatry. Front Psychiatry. 2021; 12:680811. PMC: 8206497. DOI: 10.3389/fpsyt.2021.680811. View

20.

Eldar E, Niv Y . Interaction between emotional state and learning underlies mood instability. Nat Commun. 2015; 6:6149. PMC: 5338993. DOI: 10.1038/ncomms7149. View