Neuronal underpinnings of cognitive impairment in bipolar disorder: A large data-driven functional magnetic resonance imaging study.
bipolar disorder
cognition
cognitive impairment
fMRI
neural
pro-cognitive
treatment
Journal
Bipolar disorders
ISSN: 1399-5618
Titre abrégé: Bipolar Disord
Pays: Denmark
ID NLM: 100883596
Informations de publication
Date de publication:
02 2022
02 2022
Historique:
revised:
22
02
2021
received:
19
11
2020
accepted:
27
04
2021
pubmed:
7
5
2021
medline:
20
4
2022
entrez:
6
5
2021
Statut:
ppublish
Résumé
Cognitive impairment occurs in approximately 50% of remitted patients with bipolar disorder (BD). However, there exists no treatment with replicated and robust efficacy on cognition in BD. This is partially due to limited insight into the neuronal underpinnings of cognitive impairment in these patients. This is the first study to investigate neuronal underpinnings of cognitive impairment in a large functional magnetic resonance imaging (fMRI) dataset comparing neural activity patterns between distinct neurocognitive subgroups of partially or fully remitted patients with BD. Patients (n = 153) and healthy controls (HC) (n = 52) underwent neuropsychological assessment and fMRI, during which they performed a verbal N-back working memory (WM) task. Based on hierarchical cluster analysis of neuropsychological test performance, patients were grouped into one of two neurocognitive subgroups (cognitively impaired, n = 91; cognitively normal compared to HC, n = 62) that were compared on WM-related neural activity. Cognitively impaired patients displayed WM-related hypo-activity in left dorsolateral prefrontal cortex and frontal and parietal regions within a cognitive control network (CCN) as well as hyper-activity in the default mode network (DMN) compared to cognitively normal patients. In contrast, cognitively normal patients only exhibited hypo-activity within a small cluster in the superior frontal gyrus relative to HC. Cognitive impairment in BD seems to originate from a failure to recruit key regions in the CCN and to suppress task-irrelevant DMN activity during cognitive performance. These results highlight modulation of aberrant dorsal prefrontal and DMN activity as a putative target for pro-cognitive treatment in BD.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
69-81Informations de copyright
© 2021 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd.
Références
Bourne C, Aydemir Ö, Balanzá-Martínez V, et al. Neuropsychological testing of cognitive impairment in euthymic bipolar disorder: an individual patient data meta-analysis. Acta Psychiatr Scand. 2013;128(3):149-162.
Depp CA, Mausbach BT, Harmell AL, et al. Meta-analysis of the association between cognitive abilities and everyday functioning in bipolar disorder. Bipolar Disord. 2012;14(3):217-226.
Solé B, Vieta E. What else is needed for a full functional recovery in bipolar disorder? Bipolar Disord. 2020;22(4):411-412.
Miskowiak KW, Carvalho AF, Vieta E, Kessing LV. Cognitive enhancement treatments for bipolar disorder: a systematic review and methodological recommendations. Eur Neuropsychopharmacol. 2016;26(10):1541-1561.
Miskowiak KW, Burdick KE, Martinez-Aran A, et al. Methodological recommendations for cognition trials in bipolar disorder by the International Society for Bipolar Disorders Targeting Cognition Task Force. Bipolar Disord. 2017;19(8):614-626.
Miskowiak KW, Petersen CS. Neuronal underpinnings of cognitive impairment and - improvement in mood disorders. CNS Spectr. 2019;24(1):30-53.
Burdick KE, Russo M, Frangou S, et al. Empirical evidence for discrete neurocognitive subgroups in bipolar disorder: clinical implications. Psychol Med. 2014;44(14):3083-3096.
Jensen JH, Knorr U, Vinberg M, Kessing LV, Miskowiak KW. Discrete neurocognitive subgroups in fully or partially remitted bipolar disorder: Associations with functional abilities. J Affect Disord. 2016;205:378-386.
Kjaerstad HL, Eikeseth FF, Vinberg M, Kessing LV, Miskowiak KW. Neurocognitive heterogeneity in patients newly diagnosed with bipolar disorder and their unaffected relatives: Associations with emotional cognition. Psychol Med. 2019;1-12.
Ott CV, Vinberg M, Bowie CR, et al. Effect of action-based cognitive remediation on cognition and neural activity in bipolar disorder: study protocol for a randomized controlled trial. Trials. 2018;19(1):487.
Petersen JZ, Schmidt LS, Vinberg M, et al. Effects of recombinant human erythropoietin on cognition and neural activity in remitted patients with mood disorders and first-degree relatives of patients with psychiatric disorders: a study protocol for a randomized controlled trial. Trials. 2018;19(1):611.
Kessing LV, Munkholm K, Faurholt-Jepsen M, et al. The bipolar illness onset study: research protocol for the BIO cohort study. BMJ Open. 2017;7(6):e015462.
Wing JK, Babor T, Brugha T, et al. SCAN. Schedules for clinical assessment in neuropsychiatry. Arch Gen Psychiatry. 1990;47(6):589-593.
Hamilton M. A rating scale for depression. J Neurol Neurosurg Psychiatry. 1960;23:56-62.
Young RC, Biggs JT, Ziegler VE, Meyer DA. A rating scale for mania: reliability, validity and sensitivity. Br J Psychiatry. 1978;133:429-435.
Battery AIT. Manual of Directions and Scoring. Washington, DC: War Department, Adjutant General’s Office; 1944.
Randolph C, Tierney MC, Mohr E, Chase TN. The repeatable battery for the assessment of neuropsychological status (RBANS): preliminary clinical validity. J Clin Exp Neuropsychol. 1998;20(3):310-319.
Schmidt M. Rey auditory verbal learning test: a handbook (p. 1996). Los Angeles, CA: Western Psychological Services; 1996.
Borkowski J, Benton AL, Spreen O. Word fluency and brain damage. Neuropsychologia. 1967;5:135-140.
Wechsler DWAIS-III. Wechsler adult intelligence scale. Psychological Corporation. 1997.
Nelson HE, O'Connell A. Dementia: the estimation of premorbid intelligence levels using the New Adult Reading Test. Cortex. 1978;14(2):234-244.
Rosa AR, Sánchez-Moreno J, Martínez-Aran A, et al. Validity and reliability of the Functioning Assessment Short Test (FAST) in bipolar disorder. Clinical Practice and Epidemiology in Mental Health. 2007;3(1):5.
Shapiro SS, Wilk MB. An analysis of variance test for normality (complete samples). Biometrika. 1965;52(3/4):591-611.
Grier JB. Nonparametric indexes for sensitivity and bias: computing formulas. Psychol Bull. 1971;75(6):424.
Smith J, Browning M, Conen S, et al. Vortioxetine reduces BOLD signal during performance of the N-back working memory task: a randomised neuroimaging trial in remitted depressed patients and healthy controls. Mol Psychiatry. 2018;23(5):1127-1133.
Owen AM, McMillan KM, Laird AR, Bullmore E. N-back working memory paradigm: a meta-analysis of normative functional neuroimaging studies. Hum Brain Mapp. 2005;25(1):46-59.
Emch M, von Bastian CC, Koch K. Neural correlates of verbal working memory: an fMRI meta-analysis. Front Hum Neurosci. 2019;13:180.
Desikan RS, Ségonne F, Fischl B, et al. An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. NeuroImage. 2006;31(3):968-980.
Woolrich MW, Ripley BD, Brady M, Smith SM. Temporal autocorrelation in univariate linear modeling of FMRI data. NeuroImage. 2001;14(6):1370-1386.
Jenkinson M, Beckmann C, Behrens T, Woolrich M, Smith S. Fsl. NeuroImage [Internet]. 2012;62(2):782-790.
Woolrich MW, Behrens TE, Beckmann CF, Jenkinson M, Smith SM. Multilevel linear modelling for FMRI group analysis using Bayesian inference. NeuroImage. 2004;21(4):1732-1747.
Carvalho AF, Firth J, Vieta E. Bipolar disorder. N Engl J Med. 2020;383(1):58-66.
Fernández-Corcuera P, Salvador R, Monté GC, et al. Bipolar depressed patients show both failure to activate and failure to de-activate during performance of a working memory task. J Affect Disord. 2013;148(2-3):170-178.
Wager TD, Smith EE. Neuroimaging studies of working memory. Cognitive, Affective, & Behavioral Neuroscience. 2003;3(4):255-274.
Ragland JD, Laird AR, Ranganath C, Blumenfeld RS, Gonzales SM, Glahn DC. Prefrontal activation deficits during episodic memory in schizophrenia. Am J Psychiatry. 2009;166(8):863-874.
Barch DM, Braver TS, Nystrom LE, Forman SD, Noll DC, Cohen JD. Dissociating working memory from task difficulty in human prefrontal cortex. Neuropsychologia. 1997;35(10):1373-1380.
Barbey AK, Koenigs M, Grafman J. Dorsolateral prefrontal contributions to human working memory. Cortex. 2013;49(5):1195-1205.
Alonso-Lana S, Goikolea JM, Bonnin CM, et al. Structural and functional brain correlates of cognitive impairment in euthymic patients with bipolar disorder. PLoS One. 2016;11(7).
Fitzgerald PB, Srithiran A, Benitez J, et al. An fMRI study of prefrontal brain activation during multiple tasks in patients with major depressive disorder. Hum Brain Mapp. 2008;29(4):490-501.
Bora E, Hıdıroğlu C, Özerdem A, et al. Executive dysfunction and cognitive subgroups in a large sample of euthymic patients with bipolar disorder. Eur Neuropsychopharmacol. 2016;26(8):1338-1347.
Hamilton JP, Furman DJ, Chang C, Thomason ME, Dennis E, Gotlib IH. Default-mode and task-positive network activity in major depressive disorder: implications for adaptive and maladaptive rumination. Biol Psychiat. 2011;70(4):327-333.
Kessing LV, Forman JL, Andersen PK. Does lithium protect against dementia? Bipolar Disord. 2010;12(1):87-94.
Torrent C, Martinez-Arán A, Daban C, et al. Effects of atypical antipsychotics on neurocognition in euthymic bipolar patients. Compr Psychiatry. 2011;52(6):613-622.
Sabater A, García-Blanco AC, Verdet HM, et al. Comparative neurocognitive effects of lithium and anticonvulsants in long-term stable bipolar patients. J Affect Disord. 2016;190:34-40.
Ramsay IS, MacDonald AW III. Brain correlates of cognitive remediation in schizophrenia: activation likelihood analysis shows preliminary evidence of neural target engagement. Schizophr Bull. 2015;41(6):1276-1284.
Harmer CJ, Cowen PJ, Goodwin GM. Efficacy markers in depression. Journal of Psychopharmacology. 2011;25(9):1148-1158.
Miskowiak KW, Vinberg M, Glerup L, et al. Neural correlates of improved executive function following erythropoietin treatment in mood disorders. Psychol Med. 2016;46(8):1679-1691.
Ott CV, Macoveanu J, Bowie CR, et al. Change in prefrontal activity and executive functions after action-based cognitive remediation in bipolar disorder: a randomized controlled trial. Neuropsychopharmacology. 2020;1-9.
Dias VV, Balanzá-Martinez V, Soeiro-de-Souza MG, et al. Pharmacological approaches in bipolar disorders and the impact on cognition: a critical overview. Acta Psychiatr Scand. 2012;126(5):315-331.