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Opposing Changes in the Functional Architecture of Large-Scale Networks in Bipolar Mania and Depression

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Opposing Changes in the Functional Architecture of Large-Scale Networks in Bipolar Mania and Depression applyparastyle "fig//caption/p[1]" parastyle "FigCapt" applyparastyle "fig" parastyle "Figure" Schizophrenia Bulletin doi:10.1093/schbul/sbaa004 Downloaded from https://academic.oup.com/schizophreniabulletin/advance-article-abstract/doi/10.1093/schbul/sbaa004/5734557 by University of Ottawa user on 03 March 2020 Opposing Changes in the Functional Architecture of Large-Scale Networks in Bipolar Mania and Depression Daniel Russo1,2,10, Matteo Martino3,10, Paola Magioncalda*,1,4,5,10, Matilde Inglese2,6, Mario Amore1,2, and Georg Northoff7–9 1Department of Neuroscience, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health, Section of Psychiatry, University of Genoa, Genoa, Italy; 2Ospedale Policlinico San Martino IRCCS, Genoa, Italy; 3Department of Neurology, Icahn School of Medicine at Mount Sinai, New York, NY; 4Brain and Consciousness Research Center, Taipei Medical University – Shuang Ho Hospital, New Taipei City, Taiwan; 5Graduate Institute of Mind Brain and Consciousness, Taipei Medical University, Taipei, Taiwan; 6Department of Neuroscience, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health, Section of Neurology, University of Genoa, Genoa, Italy; 7University of Ottawa Brain and Mind Research Institute, and Mind Brain Imaging and Neuroethics Royal’s Institute of Mental Health Research, University of Ottawa, Ottawa, ON, Canada; 8Mental Health Centre, Zhejiang University School of Medicine, Hangzhou, Zhejiang Province, China; 9Centre for Cognition and Brain Disorders, Hangzhou Normal University, Hangzhou, China 10These authors contributed equally to this work. *To whom correspondence should be addressed; Graduate Institute of Mind Brain and Consciousness, Taipei Medical University, No. 250 Wuxing Street, 11031 Taipei, Taiwan; tel: 00886-2-2736-1661-8601, fax: 00886-2-8732-5288, e-mail: [email protected] Objective: Manic and depressive phases of bipolar dis- internal thought deficit). Conversely, depression might order (BD) show opposite symptoms in psychomotor, be characterized by a predominance of associative over thought, and affective dimensions. Neuronally, these may sensorimotor networks, possibly driven by a deficit of the depend on distinct patterns of alterations in the func- SMN (reflecting in psychomotor inhibition). tional architecture of brain intrinsic activity. Therefore, the study aimed to characterize the spatial and temporal Key words: bipolar disorder/regional homogeneity/degree changes of resting-state activity in mania and depression, of centrality/default-mode network/sensorimotor network by investigating the regional homogeneity (ReHo) and degree of centrality (DC), in different frequency bands. Introduction Methods: Using resting-state functional magnetic reso- nance imaging (fMRI), voxel-wise ReHo and DC were Background calculated—in the standard frequency band (SFB: 0.01– Episodes of mania and depression are distinctive dis- 0.10 Hz), as well as in Slow5 (0.01–0.027 Hz) and Slow4 ease states of bipolar disorder (BD). These phases (0.027–0.073 Hz)—and compared between manic (n = show very different, often opposite, psychopatho- 36), depressed (n = 43), euthymic (n = 29) patients, and logical features. Mania presents euphoric or irritable healthy controls (n = 112). Finally, clinical correlations mood, externally focused thought, and excited psycho- were investigated. Results: Mania was mainly character- motor behavior.1,2 By contrast, depression is typically ized by decreased ReHo and DC in Slow4 in the medial characterized by depressed mood, internally focused prefrontal cortex (as part of the default-mode network thought, and inhibited psychomotor behavior.1,2 [DMN]), which in turn correlated with manic symptoma- Considering such opposite clinical symptomatology, tology. Conversely, depression was mainly characterized mania and depression could be related to distinct pat- by decreased ReHo in SFB in the primary sensory-motor terns in neuronal activity, which remain to be estab- cortex (as part of the sensorimotor network [SMN]), lished though. which in turn correlated with depressive symptomatology. Physiologically, intrinsic neuronal activity in the low fre- Conclusions: Our data show a functional reconfiguration quencies (<0.1 Hz), as investigated by resting-state func- of the spatiotemporal structure of intrinsic brain activity tional magnetic resonance imaging (fMRI), has shown to occur in BD. Mania might be characterized by a pre- to be organized in a specific functional architecture, so dominance of sensorimotor over associative networks, that temporally coherent fluctuations across distinct spa- possibly driven by a deficit of the DMN (reflecting in tially distributed brain areas originate various large-scale © The Author(s) 2020. Published by Oxford University Press on behalf of the Maryland Psychiatric Research Center. All rights reserved. For permissions, please email: [email protected] Page 1 of 10 D. Russo et al networks, and, in turn, such functional architecture is which is defined as a set of nodes linked by edges. For a fundamental in the expression of different psychological binary graph, DC is the number of edges connecting to Downloaded from https://academic.oup.com/schizophreniabulletin/advance-article-abstract/doi/10.1093/schbul/sbaa004/5734557 by University of Ottawa user on 03 March 2020 and behavioral functions.3–5 As recently demonstrated, a node.24 Thus, high DC in a region might reflect its role these networks show a functional large-scale hierarchy.6 as a central hub in the integration of global resting-state At one end, sensorimotor systems—as organized in the activity (involving both local and distant connections); sensorimotor network (SMN),3,7,8 visual network (VN),3 as DC decreases, centrality becomes lower. Considering dorsal attention network (DAN),9 and salience network that sensorimotor networks show more local connectivity (SN)—have strong recurrent connections and excitatory while associative networks display more global connec- subcortical inputs, consistent with localized processing tivity,3 ReHo may be a relevant measure for networks like of external sensory inputs and motor outputs.6 Thus, the SMN, while DC for networks like the DMN. such networks are involved in externally or environmen- On the other hand, investigating the specific contribu- tally focused thought and behavior. At the opposing end, tion of different frequencies of the resting-state signal the default-mode network (DMN)10–12 has weak recurrent can give information on the temporal organization of connections and excitatory subcortical inputs, consistent intrinsic brain activity. ReHo and DC are usually inves- with associative functions.6 Thus, DMN is involved in in- tigated within the standard frequency band (SFB) of low- ternally focused thought and correspondent internally frequency fluctuations (0.01–0.10 Hz), which are thought driven behavior. Between these 2 poles, the limbic net- to reflect mainly neuronal oscillations.4,25–28 Interestingly, work (LIM) and the central executive network (CEN) SFB was recently subdivided into 2 sub-frequency bands exhibit intermediate features.6 Moreover, such sets of net- that show differential contribution across brain areas and works are frequently organized in balances, as shown, for networks in the healthy brain, ie, Slow5 (0.01–0.027 Hz), instance, by the anticorrelated activity between the DMN which is stronger in the midline structures, and Slow4 and sensorimotor networks.7,13 (0.027–0.073 Hz), which is stronger throughout the senso- The functional architecture of intrinsic brain activity rimotor regions.4,26,27,29–31 Thus, such sub-frequencies could was found to be disrupted in BD.14,15 By investigating the play distinct roles in functional changes at a network level. different phases of illness, we previously detected distinct ReHo has been previously investigated in BD during changes in such functional brain architecture underlying depression (in adults),32–34 while DC has been explored mania and depression. In particular, mania was char- in BD without considering the ongoing episode35,36 or acterized by a tilting of the balance between SMN and during the depressive phase only.37 Therefore, a compre- DMN toward the SMN at the expense of DMN (as meas- hensive characterization of these resting-state metrics, ured by the temporal variability of BOLD signal),16 along also considering the different sub-frequencies, during all with a greater global signal representation in the SMN17 the various phases of BD, needs still to be performed. and reduced functional connectivity (FC) within the DMN.18,19 By contrast, depression was characterized by a tilting in SMN/DMN balance toward the DMN at the Aims of the Study expense of SMN.16 Following this line of evidence on a The aim of this study was to characterize the functional relationship between distinct functional brain alterations architecture of resting-state activity in the different phases and psychopathological states, a further characterization of BD in terms of both local and global connectivity (spa- of the spatiotemporal structure of resting-state activity tial organization) along with the specific contribution of during mania and depression may be highly relevant. the different frequencies of slow signal fluctuations (tem- The spatial organization of intrinsic brain activity can poral organization). For this purpose, ReHo and DC, be investigated both at a local and at a global level, by in SFB and its sub-frequency bands Slow4 and Slow5,
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