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Differences in Resting Corticolimbic Functional Connectivity in Bipolar I Bipolar Disorders 2013 Ó 2013 John Wiley and Sons A/S Published by Blackwell Publishing Ltd. BIPOLAR DISORDERS Original Article Differences in resting corticolimbic functional connectivity in bipolar I euthymia Torrisi S, Moody TD, Vizueta N, Thomason ME, Monti MM, Salvatore Torrisia, Teena D Moodyb, Townsend JD, Bookheimer SY, Altshuler LL. Differences in resting Nathalie Vizuetaa, Moriah E corticolimbic functional connectivity in bipolar I euthymia. Thomasonc, Martin M Montid, Bipolar Disord 2013: 00: 000–000. Ó 2013 John Wiley & Sons A ⁄ S. Jennifer D Townsenda, Susan Y Published by Blackwell Publishing Ltd. Bookheimerb and Lori L Altshulera aDepartment of Psychiatry, Semel Institute for Objective: We examined resting state functional connectivity in the b brain between key emotion regulation regions in bipolar I disorder to Neuroscience and Human Behavior, Center for delineate differences in coupling from healthy subjects. Cognitive Neuroscience, University of California at Los Angeles, Los Angeles, CA, cDepartment of Pediatrics, Wayne State University School of Methods: Euthymic subjects with bipolar I disorder (n = 20) and d matched healthy subjects (n = 20) participated in a resting state Medicine, Detroit, MI, Department of Psychology, functional magnetic resonance imaging scan. Low-frequency fluctuations University of California at Los Angeles, Los in blood oxygen level-dependent (BOLD) signal were correlated in the six Angeles, CA, USA connections between four anatomically defined nodes: left and right amygdala and left and right ventrolateral prefrontal cortex (vlPFC). doi: 10.1111/bdi.12047 Seed-to-voxel connectivity results were probed for commonly coupled regions. Following this, an identified region was included in a mediation Key words: amygdala – bipolar disorder – analysis to determine the potential of mediation. euthymia – functional connectivity – resting state – ventrolateral prefrontal cortex Results: The bipolar I disorder group exhibited significant Received 26 March 2012, revised and accepted for hyperconnectivity between right amygdala and right vlPFC relative to publication 7 November 2012 healthy subjects. The connectivity between these regions in the bipolar I disorder group was partially mediated by activity in the anterior Corresponding author: cingulate cortex (ACC). Dr. Salvatore Torrisi Department of Psychiatry Conclusions: Greater coupling between right amygdala and right UCLA Mood Disorders Research Program vlPFC and their partial mediation by the ACC were found in bipolar I 300 Medical Plaza, Suite 1544 disorder subjects in remission and in the absence of a psychological task. Los Angeles, CA 90095 These findings have implications for a trait-related and clinically USA important imaging biomarker. Fax: 310-794-9915 E-mail: [email protected] Bipolar disorder is a serious psychiatric illness instrumental in the regulation of that response. In thought to involve deficits in the neural substrates healthy subjects, during down-regulation of emo- for emotion regulation because of its characteristic tion, the functional connectivity between these profile of lifetime depressed and manic mood areas has been observed to increase (7, 8). episodes (1, 2). Neuroimaging research in healthy The above-referenced functional magnetic reso- subjects has revealed a number of brain areas nance imaging (fMRI) studies of emotion regula- involved in emotional regulation, including tion involve observation of brain activity while subcortical (e.g., amygdala) and ventrolateral subjects perform a task. Recent studies that have prefrontal cortical (vlPFC) regions (3, 4). Research evaluated subjects while not performing any cog- in both humans and primates has additionally nitive tasks – e.g., resting state studies – have also demonstrated strong anatomical projections be- revealed intrinsic activation patterns in the brain. tween these areas, forming the substrate for which Resting state fMRI provides complementary infor- functional coupling (connectivity) is possible (5, 6). mation to task-based fMRI in that both provide a The amygdala, for example, is functionally respon- platform for examining functional brain networks. sive to emotional stimuli, while the vlPFC is Spatially distributed large-scale brain networks can 1 Torrisi et al. be reliably derived and interrogated by either kind pathophysiology of bipolar disorder, further re- of fMRI experiment (9–11) and one could argue search that investigates common regions in both that both contribute different dimensions to a full hemispheres in single mood states and in single characterization of brain activity. A variety of bipolar disorder subtypes is necessary. methods have been used to analyze such data (12) The goal of the present resting state study was to and have been applied to diverse clinical popula- elucidate differences in intrinsic functional connec- tions in the effort to delineate disease-related tivity that might contribute to mood lability in dysfunctions in connectivity (13). bipolar I disorder. We therefore took a focused While there are a handful of studies that have approach to assessing connectivity in two bilateral investigated functional connectivity in bipolar brain regions strongly implicated in emotion reg- disorder, few are resting state studies (Table 1). ulation (four regions in total: right and left Of these, there is some overlap with the regions amygdalae and right and left vlPFC) in a group used as seeds, such as the medial prefrontal cortex of euthymic bipolar I disorder subjects. We (14, 15) or amygdala (16, 17), but the findings show hypothesized that subjects with bipolar I disorder differences in connectivity in lateralization (left or would demonstrate aberrant functional connectiv- right hemisphere), and in sign (positive or negative ity relative to healthy subjects between amygdalae coupling), and between-group differences (healthy and lateral vlPFC regions that subserve emotion subjects > bipolar disorder or bipolar disor- regulation. Furthermore, observed alterations of der > healthy subjects). Three of these studies brain connectivity during the euthymic state may investigated bipolar mania and ⁄ or depression (14, be considered a potential biomarker of trait aspects 15, 17); however, one combined several mood of the disease. states into its bipolar disorder sample (16) while another combined bipolar I and II disorder Materials and methods subjects (14). This latter issue is particularly problematic as there is evidence to suggest that Participants patterns of activation and connectivity change with Participants provided written informed consent in different mood state and subtype of bipolar disor- accordance with the Institutional Review Boards at der (17–19). For a clearer picture of the underlying Table 1. A selection of functional magnetic resonance imaging (fMRI) connectivity studies in bipolar disorder Study Task ⁄ rest BP mood state Method Seed ⁄ ROI BP > HS HS > BP Foland-Ross et al. Labeling Manic PPI L AMYG Negative FC: ACC Negative FC: LH 2008 (29) emotional (BA 32 and 24) amygdala–bilateral faces and BA 10 vlPFC Pompei et al. Color-word Euthymic PPI R vlPFC Positive FC: Negative FC: 2011 (40) Stroop RH vlPFC–insula RH vlPFC–LH vACC Townsend et al. Explicit emotion Euthymic PPI L AMYG Negative FC: 2013 (30) regulation L AMYG–L vlPFC Versace et al. Labeling sad and Depressed Seed-based omPFC Sad: RH Happy: 2010 (39) happy faces and euthymic FC (BA 11) AMYG–vmOFC LH AMYG–vmOFC and AMYG Anand et al. Rest Manic and Seed-based pgACC LH and RH 2009 (14) depressed FC pgACC–dmTHAL, AMYG, and striatum Chai et al. Rest Manic Seed-based mPFC, AMYG, mPFC–LH insula 2011 (15) FC dlPFC, insula, mPFC–RH BA47 vlPFC Chepenik et al. Rest Rapid cyclers, Seed-based vlPFC, AMYG LH vPFC–RH vPFC Negative FC: 2010 (16) euthymic, FC LH AMYG–vPFC depressed, and mixed Cerullo et al. Steady state Manic and Seed-based L and R AMYG N ⁄ AN⁄ A 2012 (17) depressed FC (longitudinal) – = correlation (coupling); ACC = anterior cingulate cortex; AMYG = amygdala; BA = Brodmann’s Area; BP = bipolar disorder; dlPFC = dorsolateral PFC; dmTHAL = dorsomedial thalamus; FC = functional connectivity; HS = healthy subjects; L = left; LH = left hemisphere; mPFC = medial PFC; N ⁄ A = these direct contrasts were not performed; omPFC = orbitomedial PFC; PFC = prefrontal cortex: vlPFC = ventrolateral PFC; pgACC = pregenual ACC; PPI = psychophysiological interaction; R = right; RH = right hemisphere; ROI = region of interest; vACC = ventral ACC; vmOFC = ventromedial orbitofrontal cortex; vPFC = ventral PFC. 2 Resting corticolimbic functional connectivity the University of California, Los Angeles (UCLA) Image acquisition and the Veterans Affairs (VA) Greater Los Angeles Healthcare System. Subjects with bipolar I disor- Subjects were scanned on a 3T Siemens Trio scanner der were recruited through the outpatient UCLA (Siemens Medical Systems, Erlangen, Germany). Mood Disorders Clinic, the outpatient Bipolar They were asked to rest with their eyes closed Disorders Clinic of the VA Greater Los Angeles during the scan but to not fall asleep. A structural Health Care System, and through local advertising T1 magnetization-prepared rapid gradient echo in the community. Healthy subjects were recruited (MPRAGE) was acquired with parameters of by advertisements in local newspapers and campus repetition time (TR) = 1.9 sec, echo time (TE) = fliers. All participants were first interviewed using 2.26 msec, flip angle = 9°, matrix = 256 · the Structured Clinical Interview (SCID) (20) for 256,
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