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Aberrant intrinsic functional connectivity within and between corticostriatal and temporal–parietal networks in adults and youth with bipolar disorder

Published online by Cambridge University Press:  29 February 2016

J. Stoddard*
Affiliation:
Department of Health and Human Services, Section on Bipolar Spectrum Disorders, Emotion and Development Branch, National Institute of Mental Health, National Institutes of Health, Bethesda, MD, USA
S. J. Gotts
Affiliation:
Department of Health and Human Services, Section on Cognitive Neuropsychology, National Institute of Mental Health, National Institutes of Health, Bethesda, MD, USA
M. A. Brotman
Affiliation:
Department of Health and Human Services, Section on Bipolar Spectrum Disorders, Emotion and Development Branch, National Institute of Mental Health, National Institutes of Health, Bethesda, MD, USA
S. Lever
Affiliation:
Department of Health and Human Services, Section on Bipolar Spectrum Disorders, Emotion and Development Branch, National Institute of Mental Health, National Institutes of Health, Bethesda, MD, USA
D. Hsu
Affiliation:
School of Medicine, Emory University, Atlanta, GA, USA
C. Zarate Jr.
Affiliation:
Department of Health and Human Services, Section on the Neurobiology and Treatment of Mood Disorders, National Institute of Mental Health, National Institutes of Health, Bethesda, MD, USA
M. Ernst
Affiliation:
Department of Health and Human Services, Section on Development and Affective Neuroscience, Emotion and Development Branch, National Institute of Mental Health, National Institutes of Health, Bethesda, MD, USA
D. S. Pine
Affiliation:
Department of Health and Human Services, Section on Development and Affective Neuroscience, Emotion and Development Branch, National Institute of Mental Health, National Institutes of Health, Bethesda, MD, USA
E. Leibenluft
Affiliation:
Department of Health and Human Services, Section on Bipolar Spectrum Disorders, Emotion and Development Branch, National Institute of Mental Health, National Institutes of Health, Bethesda, MD, USA
*
*Address for correspondence: J. Stoddard, Department of Health and Human Services, Section on Bipolar Spectrum Disorders, Emotion and Development Branch, National Institute of Mental Health, National Institutes of Health, 9000 Rockville Pike MSC-2670, Building 15K, Bethesda, MD 20892-2670, USA. (Email: joel.stoddard@nih.gov)

Abstract

Background

Major questions remain regarding the dysfunctional neural circuitry underlying the pathophysiology of bipolar disorder (BD) in both youths and adults. In both age groups, studies implicate abnormal intrinsic functional connectivity among prefrontal, limbic and striatal areas.

Method

We collected resting-state functional magnetic resonance imaging (fMRI) data from youths and adults (ages 10–50 years) with BD (n = 39) and healthy volunteers (HV; n = 78). We identified brain regions with aberrant intrinsic functional connectivity in BD by first comparing voxel-wise mean global connectivity and then conducting correlation analyses. We used k-means clustering and multidimensional scaling to organize all detected regions into networks.

Results

Across the brain, we detected areas of dysconnectivity in both youths and adults with BD relative to HV. There were no significant age-group × diagnosis interactions. When organized by interregional connectivity, the areas of dysconnectivity in patients with BD comprised two networks: one of temporal and parietal areas involved in late stages of visual processing, and one of corticostriatal areas involved in attention, cognitive control and response generation.

Conclusions

These data suggest that two networks show abnormal intrinsic functional connectivity in BD. Regions in these networks have been implicated previously in BD. We observed similar dysconnectivity in youths and adults with BD. These findings provide guidance for refining models of network-based dysfunction in BD.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2016 

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References

Adleman, NE, Kayser, RR, Olsavsky, AK, Bones, BL, Muhrer, EJ, Fromm, SJ, Pine, DS, Zarate, C, Leibenluft, E, Brotman, MA (2013). Abnormal fusiform activation during emotional-face encoding assessed with functional magnetic resonance imaging. Psychiatry Research 212, 161163.CrossRefGoogle ScholarPubMed
Adler, CM, Holland, SK, Schmithorst, V, Tuchfarber, MJ, Strakowski, SM (2004). Changes in neuronal activation in patients with bipolar disorder during performance of a working memory task. Bipolar Disorders 6, 540549.CrossRefGoogle ScholarPubMed
American Psychiatric Association (2000). Diagnostic and Statistical Manual of Mental Disorders, 4th edn. (Text Revised). American Psychiatric Press: Washington, DC.Google Scholar
Anand, A, Li, Y, Wang, Y, Lowe, MJ, Dzemidzic, M (2009). Resting state corticolimbic connectivity abnormalities in unmedicated bipolar disorder and unipolar depression. Psychiatry Research 171, 189198.CrossRefGoogle ScholarPubMed
Anticevic, A, Brumbaugh, MS, Winkler, AM, Lombardo, LE, Barrett, J, Corlett, PR, Kober, H, Gruber, J, Repovs, G, Cole, MW, Krystal, JH, Pearlson, GD, Glahn, DC (2013). Global prefrontal and fronto-amygdala dysconnectivity in bipolar I disorder with psychosis history. Biological Psychiatry 73, 565573.CrossRefGoogle ScholarPubMed
Anticevic, A, Yang, G, Savic, A, Murray, JD, Cole, MW, Repovs, G, Pearlson, GD, Glahn, DC (2014). Mediodorsal and visual thalamic connectivity differ in schizophrenia and bipolar disorder with and without psychosis history. Schizophrenia Bulletin 40, 12271243.CrossRefGoogle ScholarPubMed
Argyelan, M, Ikuta, T, Derosse, P, Braga, RJ, Burdick, KE, John, M, Kingsley, PB, Malhotra, AK, Szeszko, PR (2014). Resting-state fMRI connectivity impairment in schizophrenia and bipolar disorder. Schizophrenia Bulletin 40, 100110.CrossRefGoogle ScholarPubMed
Beckmann, CF, Smith, SM (2004). Probabilistic independent component analysis for functional magnetic resonance imaging. IEEE Transactions on Medical Imaging 23, 137152.CrossRefGoogle ScholarPubMed
Behzadi, Y, Restom, K, Liau, J, Liu, TT (2007). A component based noise correction method (CompCor) for BOLD and perfusion based fMRI. NeuroImage 37, 90101.CrossRefGoogle ScholarPubMed
Birn, RM, Murphy, K, Bandettini, PA (2008). The effect of respiration variations on independent component analysis results of resting state functional connectivity. Human Brain Mapping 29, 740750.CrossRefGoogle ScholarPubMed
Bora, E, Fornito, A, Yücel, M, Pantelis, C (2010). Voxelwise meta-analysis of gray matter abnormalities in bipolar disorder. Biological Psychiatry 67, 10971105.CrossRefGoogle ScholarPubMed
Bora, E, Yucel, M, Pantelis, C (2009). Cognitive endophenotypes of bipolar disorder: a meta-analysis of neuropsychological deficits in euthymic patients and their first-degree relatives. Journal of Affective Disorders 113, 120.CrossRefGoogle ScholarPubMed
Buckner, RL, Sepulcre, J, Talukdar, T, Krienen, FM, Liu, H, Hedden, T, Andrews-Hanna, JR, Sperling, RA, Johnson, KA (2009). Cortical hubs revealed by intrinsic functional connectivity: mapping, assessment of stability, and relation to Alzheimer's disease. Journal of Neuroscience 29, 18601873.CrossRefGoogle ScholarPubMed
Calhoun, BD, Maciejewski, PK, Pearlson, GD, Kiehl, KA (2008). Temporal lobe and “default” hemodynamic brain modes discriminate between schizophrenia and bipolar disorder. Human Brain Mapping 29, 12651275.CrossRefGoogle ScholarPubMed
Chai, XJ, Whitfield-Gabrieli, S, Shinn, AK, Gabrieli, JD, Nieto Castanon, A, McCarthy, JM, Cohen, BM, Ongur, D (2011). Abnormal medial prefrontal cortex resting-state connectivity in bipolar disorder and schizophrenia. Neuropsychopharmacology 36, 20092017.CrossRefGoogle Scholar
Chen, CH, Suckling, J, Lennox, BR, Ooi, C, Bullmore, ET (2011). A quantitative meta-analysis of fMRI studies in bipolar disorder. Bipolar Disorders 13, 115.CrossRefGoogle ScholarPubMed
Chen, G, Adleman, NE, Saad, ZS, Leibenluft, E, Cox, RW (2014). Applications of multivariate modeling to neuroimaging group analysis: a comprehensive alternative to univariate general linear model. NeuroImage 99, 571588.CrossRefGoogle ScholarPubMed
Cox, RW (1996). AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Computers and Biomedical Research, An International Journal 29, 162173.CrossRefGoogle ScholarPubMed
Dickstein, DP, Gorrostieta, C, Ombao, H, Goldberg, LD, Brazel, AC, Gable, CJ, Kelly, C, Gee, DG, Zuo, XN, Castellanos, FX, Milham, MP (2010). Fronto-temporal spontaneous resting state functional connectivity in pediatric bipolar disorder. Biological Psychiatry 68, 839846.CrossRefGoogle ScholarPubMed
Dickstein, DP, Rich, BA, Roberson-Nay, R, Berghorst, L, Vinton, D, Pine, DS, Leibenluft, E (2007). Neural activation during encoding of emotional faces in pediatric bipolar disorder. Bipolar Disorders 9, 679692.CrossRefGoogle ScholarPubMed
Di Martino, A, Yan, CG, Li, Q, Denio, E, Castellanos, FX, Alaerts, K, Anderson, JS, Assaf, M, Bookheimer, SY, Dapretto, M, Deen, B, Delmonte, S, Dinstein, I, Erti-Wagner, B, Fair, DA, Gallagher, L, Kennedy, DP, Keown, CL, Keysers, C, Lainhart, JE, Lord, C, Luna, B, Menon, V, Minshew, NJ, Monk, CS, Mueller, S, Muller, RA, Nebel, MB, Nigg, JT, O'Hearn, K, Pelphrey, KA, Peltier, SJ, Rudie, JD, Sunaert, S, Thioux, M, Tyszka, JM, Uddin, LQ, Verhoeven, JS, Wenderoth, N, Wiggins, JL, Mostofsky, SH, Milham, MP (2014). The autism brain imaging data exchange: towards a large-scale evaluation of the intrinsic brain architecture in autism. Molecular Psychiatry 19, 659667.CrossRefGoogle ScholarPubMed
Du, Y, Pearlson, GD, Liu, J, Sui, J, Yu, Q, He, H, Castro, E, Calhoun, VD (2015). A group ICA based framework for evaluating resting fMRI markers when disease categories are unclear: application to schizophrenia, bipolar, and schizoaffective disorders. NeuroImage 122, 272280.CrossRefGoogle ScholarPubMed
Ellison-Wright, I, Bullmore, E (2010). Anatomy of bipolar disorder and schizophrenia: a meta-analysis. Schizophrenia Research 117, 112.CrossRefGoogle ScholarPubMed
Endicott, J, Spitzer, RL, Fleiss, JL, Cohen, J (1976). The Global Assessment Scale: a procedure for measuring overall severity of psychiatric disturbance. Archives of General Psychiatry 33, 766771.CrossRefGoogle Scholar
Favre, P, Baciu, M, Pichat, C, Bougerol, T, Polosan, M (2014). fMRI evidence for abnormal resting-state functional connectivity in euthymic bipolar patients. Journal of Affective Disorders 165, 182189.CrossRefGoogle ScholarPubMed
Fears, SC, Service, SK, Kremeyer, B, Araya, C, Araya, X, Bejarano, J, Ramirez, M, Castrillon, G, Gomez-Franco, J, Lopez, MC, Montoya, G, Montoya, P, Aldana, I, Teshiba, TM, Abaryan, Z, Al-Sharif, NB, Ericson, M, Jalbrzikowski, M, Luykx, JJ, Navarro, L, Tishler, TA, Altshuler, L, Bartzokis, G, Escobar, J, Glahn, DC, Ospina-Duque, J, Risch, N, Ruiz-Linares, A, Thompson, PM, Cantor, RM, Lopez-Jaramilllo, C, Macava, G, Molina, J, Reus, VI, Sabatti, C, Freimer, NB, Bearden, CE (2014). Multisystem component phenotypes of bipolar disorder for genetic investigations of extended pedigrees. JAMA Psychiatry 71, 375387.CrossRefGoogle ScholarPubMed
First, MB, Spitzer, RL, Miriam, G, Williams, JBW (2002). Structured Clinical Interview for DSM-IV-TR Axis I Disorders, Research Version, Patient Edition With Psychotic Screen (SCID-I/P W/ PSY SCREEN). New York Psychiatric Institute Biometrics Research: New York.Google Scholar
Gao, W, Jiao, Q, Lu, S, Zhong, Y, Qi, R, Lu, D, Xiao, Q, Yang, F, Lu, G, Su, L (2014). Alterations of regional homogeneity in pediatric bipolar depression: a resting-state fMRI study. BMC Psychiatry 14, 222.CrossRefGoogle ScholarPubMed
Glahn, DC, Robinson, JL, Tordesillas-Gutierrez, D, Monkul, ES, Holmes, MK, Green, MJ, Bearden, CE (2010). Fronto-temporal dysregulation in asymptomatic bipolar I patients: a paired associate functional MRI study. Human Brain Mapping 31, 10411051.CrossRefGoogle ScholarPubMed
Glover, GH, Li, TQ, Ress, D (2000). Image-based method for retrospective correction of physiological motion effects in fMRI: RETROICOR. Magnetic Resonance in Medicine 44, 162167.3.0.CO;2-E>CrossRefGoogle ScholarPubMed
Gotts, SJ, Simmons, WK, Milbury, LA, Wallace, GL, Cox, RW, Martin, A (2012). Fractionation of social brain circuits in autism spectrum disorders. Brain 135, 27112725.CrossRefGoogle ScholarPubMed
Jo, HJ, Gotts, SJ, Reynolds, RC, Bandettini, PA, Cox, RW, Saad, ZS (2013). Effective preprocessing procedures virtually eliminate distance-dependent motion artifacts in resting state fMRI. Journal of Applied Mathematics 2013, 10.1155/2013/935154.CrossRefGoogle ScholarPubMed
Jo, HJ, Saad, ZS, Simmons, WK, Milbury, LA, Cox, RW (2010). Mapping sources of correlation in resting state fMRI, with artifact detection and removal. NeuroImage 52, 571582.CrossRefGoogle ScholarPubMed
Jones, TB, Bandettini, PA, Kenworthy, L, Case, LK, Milleville, SC, Martin, A, Birn, RM (2010). Sources of group differences in functional connectivity: an investigation applied to autism spectrum disorder. NeuroImage 49, 401414.CrossRefGoogle ScholarPubMed
Kaufman, J, Birmaher, B, Brent, D, Rao, U, Flynn, C, Moreci, P, Williamson, D, Ryan, N (1997). Schedule for Affective Disorders and Schizophrenia for School-Age Children-Present and Lifetime Version (K-SADS-PL): initial reliability and validity data. Journal of the American Academy of Child and Adolescent Psychiatry 36, 980988.CrossRefGoogle ScholarPubMed
Kupferschmidt, DA, Zakzanis, KK (2011). Toward a functional neuroanatomical signature of bipolar disorder: quantitative evidence from the neuroimaging literature. Psychiatry Research 193, 7179.CrossRefGoogle Scholar
Kurtz, MM, Gerraty, RT (2009). A meta-analytic investigation of neurocognitive deficits in bipolar illness: profile and effects of clinical state. Neuropsychology 23, 551562.CrossRefGoogle ScholarPubMed
Leibenluft, E, Rich, BA, Vinton, DT, Nelson, EE, Fromm, SJ, Berghorst, L, Berghorst, LH, Joshi, P, Robb, A, Schachar, RJ, Dickstein, DP, McClure, EB, Pine, DS (2007). Neural circuitry engaged during unsuccessful motor inhibition in pediatric bipolar disorder. American Journal of Psychiatry 164, 5260.CrossRefGoogle ScholarPubMed
Liu, CH, Li, F, Li, SF, Wang, YJ, Tie, CL, Wu, HY, Zhou, Z, Zhang, D, Dong, J, Yang, Z, Wang, CY (2012). Abnormal baseline brain activity in bipolar depression: a resting state functional magnetic resonance imaging study. Psychiatry Research 203, 175179.CrossRefGoogle ScholarPubMed
Lu, D, Jiao, Q, Zhong, Y, Gao, W, Xiao, Q, Liu, X, Lin, X, Cheng, W, Luo, L, Xu, C, Lu, G, Su, L (2014). Altered baseline brain activity in children with bipolar disorder during mania state: a resting-state study. Neuropsychiatric Disease and Treatment 10, 317323.Google Scholar
Mamah, D, Barch, DM, Repovs, G (2013). Resting state functional connectivity of five neural networks in bipolar disorder and schizophrenia. Journal of Affective Disorders 150, 601609.CrossRefGoogle Scholar
Mazzola-Pomietto, P, Kaladjian, A, Azorin, J-M, Anton, J-L, Jeanningros, R (2009). Bilateral decrease in ventrolateral prefrontal cortex activation during motor response inhibition in mania. Journal of Psychiatric Research 43, 432441.CrossRefGoogle ScholarPubMed
Meda, SA, Gill, A, Stevens, MC, Lorenzoni, RP, Glahn, DC, Calhoun, VD, Sweeny, JA, Tamminga, CA, Keshavan, MS, Thaker, G, Pearlson, GD (2012). Differences in resting-state functional magnetic resonance imaging functional network connectivity between schizophrenia and psychotic bipolar probands and their unaffected first-degree relatives. Biological Psychiatry 71, 881889.CrossRefGoogle ScholarPubMed
Meoded, A, Morrissette, AE, Katipally, R, Schanz, O, Gotts, SJ, Floeter, MK (2014). Cerebro-cerebellar connectivity is increased in primary lateral sclerosis. NeuroImage. Clinical 7, 288296.CrossRefGoogle ScholarPubMed
Monks, PJ, Thompson, JM, Bullmore, ET, Suckling, J, Brammer, MJ, Williams, SC, Simmons, A, Giles, N, Lloyd, AJ, Harrison, CL, Seal, M, Murray, RM, Ferrier, IN, Young, AH, Curtis, VA (2004). A functional MRI study of working memory task in euthymic bipolar disorder: evidence for task-specific function. Bipolar Disorders 6, 550564.CrossRefGoogle Scholar
Niendam, TA, Laird, AR, Ray, KL, Dean, YM, Glahn, DC, Carter, CS (2012). Meta-analytic evidence for a superordinate cognitive control network subserving diverse executive functions. Cognitive, Affective and Behavioral Neuroscience 12, 241268.CrossRefGoogle ScholarPubMed
Nurnberger, JI Jr., Blehar, MC, Kaufmann, CA, York-Cooler, C, Simpson, SG, Harkavy-Friedman, J, Severe, JB, Malaspina, D, Reich, T (1994). Diagnostic interview for genetic studies: rationale, unique features, and training. Archives of General Psychiatry 51, 849859.CrossRefGoogle ScholarPubMed
Passarotti, AM, Sweeney, JA, Pavuluri, MN (2010). Neural correlates of response inhibition in pediatric bipolar disorder and attention deficit hyperactivity disorder. Psychiatry Research 181, 3643.CrossRefGoogle ScholarPubMed
Postuma, RB, Dagher, A (2006). Basal ganglia functional connectivity based on a meta-analysis of 126 positron emission tomography and functional magnetic resonance imaging publications. Cerebral Cortex 16, 15081521.CrossRefGoogle ScholarPubMed
Poznanski, EO, Cook, SC, Carroll, BJ (1979). A depression rating scale for children. Pediatrics 64, 442450.CrossRefGoogle ScholarPubMed
Power, JD, Barnes, KA, Snyder, AZ, Schlaggar, BL, Petersen, SE (2012). Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. NeuroImage 59, 21422154.CrossRefGoogle ScholarPubMed
Power, JD, Mitra, A, Laumann, TO, Snyder, AZ, Schlaggar, BL, Petersen, SE (2014). Methods to detect, characterize, and remove motion artifact in resting state fMRI. NeuroImage 84, 320341.CrossRefGoogle ScholarPubMed
Rashid, B, Damaraju, E, Pearlson, GD, Calhoun, VD (2014). Dynamic connectivity states estimated from resting fMRI Identify differences among schizophrenia, bipolar disorder, and healthy control subjects. Frontiers in Human Neuroscience 8, 897.CrossRefGoogle ScholarPubMed
Reuter, M, Schmansky, NJ, Rosas, HD, Fischl, B (2012). Within-subject template estimation for unbiased longitudinal image analysis. Neuroimage 61, 14021418.CrossRefGoogle ScholarPubMed
Robinson, LJ, Thompson, JM, Gallagher, P, Goswami, U, Young, AH, Ferrier, IN, Moore, PB (2006). A meta-analysis of cognitive deficits in euthymic patients with bipolar disorder. Journal of Affective Disorders 93, 105115.CrossRefGoogle ScholarPubMed
Shaffer, D, Gould, MS, Brasic, J, Ambrosini, P, Fisher, P, Bird, H, Aluwahlia, S (1983). A children's global assessment scale (CGAS). Archives of General Psychiatry 40, 12281231.CrossRefGoogle ScholarPubMed
Shulman, GL, Corbetta, C (2012). Two attentional networks: identification and function within a larger cognitive architecture. In Cognitive Neuroscience of Attention, 2nd edn. (ed. Posner, MI), pp. 113128. Guilford Press: New York.Google Scholar
Smith, SM, Miller, KL, Salimi-Khorshidi, G, Webster, M, Beckmann, CF, Nichols, TE, Ramsey, JD, Woolrich, MW (2011). Network modelling methods for fMRI. NeuroImage 54, 875891.CrossRefGoogle ScholarPubMed
Stoddard, J, Hsu, D, Reynolds, RC, Brotman, MA, Ernst, M, Pine, DS, Leibenluft, E, Dickstein, DP (2014). Aberrent amygdala intrinsic functional connectivity distinguishes youths with bipolar disorder from those with severe mood dysregulation. Psychiatry Research 231, 120125.CrossRefGoogle Scholar
Torrisi, S, Moody, TD, Vizueta, N, Thomason, ME, Monti, MM, Townsend, JD, Bookheimer, SY, Altshuler, LL (2013). Differences in resting corticolimbic functional connectivity in bipolar I euthymia. Bipolar Disorders 15, 156166.CrossRefGoogle ScholarPubMed
Townsend, J, Bookheimer, SY, Foland–Ross, LC, Sugar, CA, Altshuler, LL (2010). fMRI abnormalities in dorsolateral prefrontal cortex during a working memory task in manic, euthymic and depressed bipolar subjects. Psychiatry Research 182, 2229.CrossRefGoogle ScholarPubMed
Tseng, WL, Bones, BL, Kayser, RR, Olsavsky, AK, Fromm, SJ, Pine, DS, Leibenluft, E, Brotman, MA (2015). An fMRI study of emotional face encoding in youth at risk for bipolar disorder. European Psychiatry 30, 9498.CrossRefGoogle ScholarPubMed
Uddin, LQ, Suprekar, K, Menon, V (2010). Typical and atypical development of functional human brain networks: insights from resting-state fMRI. Frontiers in Systems Neuroscience 4, 21.CrossRefGoogle ScholarPubMed
Vargas, C, López-Jaramillo, C, Vieta, E (2013). A systematic literature review of resting state network–functional MRI in bipolar disorder. Journal of Affective Disorders 150, 727735.CrossRefGoogle ScholarPubMed
Wang, Y, Zhong, S, Jia, Y, Zhou, Z, Wang, B, Pan, J, Huang, L (2015). Interhemispheric resting state functional connectivity abnormalities in unipolar depression and bipolar depression. Bipolar Disorders 17, 486495.CrossRefGoogle ScholarPubMed
Williams, JBW, Link, MJ, Rosenthal, NE, Terman, M (1988). Structured Interview Guide for the Hamilton Depression Rating Scale, Seasonal Affective Disorders Version (SIGH-SAD). New York Psychiatric Institute, Biometrics Research: New York.Google Scholar
Wise, T, Radua, J, Nortje, G, Cleare, AJ, Young, AH, Arnone, D (2016). Voxel-based meta-analytical evidence of structural disconnectivity in major depression and bipolar disorder. Biological Psychiatry 79, 293302.CrossRefGoogle ScholarPubMed
Wu, M, Lu, LH, Passarotti, AM, Wegbreit, E, Fitzgerald, J, Pavuluri, MN (2013). Altered affective, executive and sensorimotor resting state networks in patients with pediatric mania. Journal of Psychiatry and Neuroscience 38, 232240.Google ScholarPubMed
Xiao, Q, Zhong, Y, Lu, D, Gao, W, Jiao, Q, Lu, G, Su, L (2013). Altered regional homogeneity in pediatric bipolar disorder during manic state: a resting-state fMRI study. PLOS ONE 8, e57978.Google ScholarPubMed
Yeo, BT, Krienen, FM, Sepulcre, J, Sabuncu, MR, Lashkari, D, Hollinshead, M, Roffman, JL, Smoller, JW, Zollei, L, Polimeni, JR, Fischl, B, Liu, H, Buckner, RL (2011). The organization of the human cerebral cortex estimated by intrinsic functional connectivity. Journal of Neurophysiology 106, 11251165.Google ScholarPubMed
Young, RC, Biggs, JT, Ziegler, VE, Meyer, DA (1978). A rating scale for mania: reliability, validity and sensitivity. British Journal of Psychiatry 133, 429435.CrossRefGoogle ScholarPubMed
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