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Fronto-limbic disconnection in bipolar disorder

Published online by Cambridge University Press:  15 April 2020

D. Radaelli ,
G. Sferrazza Papa ,
B. Vai ,
S. Poletti ,
E. Smeraldi ,
C. Colombo  and
F. Benedetti
D. Radaelli*
Affiliation:
Department of Clinical Neurosciences, Istituto Scientifico Ospedale San Raffaele, San Raffaele Turro, Via Stamira d’Ancona 20, Milan, Italy Centro di Eccellenza Risonanza Magnetica ad Alto Campo (CERMAC) Milano, Italy
G. Sferrazza Papa
Affiliation:
Department of Clinical Neurosciences, Istituto Scientifico Ospedale San Raffaele, San Raffaele Turro, Via Stamira d’Ancona 20, Milan, Italy
B. Vai
Affiliation:
Department of Clinical Neurosciences, Istituto Scientifico Ospedale San Raffaele, San Raffaele Turro, Via Stamira d’Ancona 20, Milan, Italy
S. Poletti
Affiliation:
Department of Clinical Neurosciences, Istituto Scientifico Ospedale San Raffaele, San Raffaele Turro, Via Stamira d’Ancona 20, Milan, Italy Centro di Eccellenza Risonanza Magnetica ad Alto Campo (CERMAC) Milano, Italy
E. Smeraldi
Affiliation:
Department of Clinical Neurosciences, Istituto Scientifico Ospedale San Raffaele, San Raffaele Turro, Via Stamira d’Ancona 20, Milan, Italy Centro di Eccellenza Risonanza Magnetica ad Alto Campo (CERMAC) Milano, Italy
C. Colombo
Affiliation:
Department of Clinical Neurosciences, Istituto Scientifico Ospedale San Raffaele, San Raffaele Turro, Via Stamira d’Ancona 20, Milan, Italy Centro di Eccellenza Risonanza Magnetica ad Alto Campo (CERMAC) Milano, Italy
F. Benedetti
Affiliation:
Department of Clinical Neurosciences, Istituto Scientifico Ospedale San Raffaele, San Raffaele Turro, Via Stamira d’Ancona 20, Milan, Italy Centro di Eccellenza Risonanza Magnetica ad Alto Campo (CERMAC) Milano, Italy
*
*Corresponding author at: Department of Clinical Neurosciences, Istituto Scientifico Ospedale San Raffaele, San Raffaele Turro, Via Stamira d’Ancona 20, Milan, Italy. Tel.: +39 02 26433156; fax: +39 02 26433265. E-mail address: E-mail address:[email protected] (D. Radaelli).
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Abstract

Background:

Bipolar disorder (BD) is a severe, disabling and life-threatening illness. Disturbances in emotion and affective processing are core features of the disorder with affective instability being paralleled by mood-congruent biases in information processing that influence evaluative processes and social judgment. Several lines of evidence, coming from neuropsychological and imaging studies, suggest that disrupted neural connectivity could play a role in the mechanistic explanation of these cognitive and emotional symptoms. The aim of the present study is to investigate the effective connectivity in a sample of bipolar patients.

Methods:

Dynamic causal modeling (DCM) technique was used to study 52 inpatients affected by bipolar disorders consecutively admitted to San Raffaele hospital in Milano and forty healthy subjects. A face-matching task was used as activation paradigm.

Results:

Patients with BD showed a significantly reduced endogenous connectivity in the DLPFC to Amy connection. There was no significant group effect upon the endogenous connection from Amy to ACC, from ACC to Amy and from DLPFC to ACC.

Conclusions:

Both DLPFC and ACC are part of a network implicated in emotion regulation and share strong reciprocal connections with the amygdale. The pattern of abnormal or reduced connectivity between DLPFC and amygdala may reflect abnormal modulation of mood and emotion typical of bipolar patients.

Keywords

Bipolar disorderNeuroimagingDynamic causal modelingDepressionfMRIAffective disorders
Type
Original article
Information
European Psychiatry , Volume 30 , Issue 1 , January 2015 , pp. 82 - 88
Copyright
Copyright © Elsevier Masson SAS 2015

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References

Adler, CM, DelBello, MP, Strakowski, SM. Brain network dysfunction in bipolar disorder. CNS Spectr 2006; 11: 312–320. [quiz 23–4].CrossRefGoogle ScholarPubMed
Almeida, JR, Mechelli, A, Hassel, S, Versace, A, Kupfer, DJ, Phillips, ML. Abnormally increased effective connectivity between parahippocampal gyrus and ventromedial prefrontal regions during emotion labeling in bipolar disorder. Psychiatry Res 2009; 174: 195–201CrossRefGoogle ScholarPubMed
Almeida, JR, Versace, A, Mechelli, A, Hassel, S, Quevedo, K, Kupfer, DJ, et al.Abnormal amygdala-prefrontal effective connectivity to happy faces differentiates bipolar from major depression. Biol Psychiatry 2009; 66: 451–459.CrossRefGoogle ScholarPubMed
Anand, A, Li, Y, Wang, Y, Lowe, MJ, Dzemidzic, M. Resting state corticolimbic connectivity abnormalities in unmedicated bipolar disorder and unipolar depression. Psychiatry Res 2009; 171: 189–198.CrossRefGoogle ScholarPubMed
Anticevic, A, Brumbaugh, MS, Winkler, AM, Lombardo, LE, Barrett, J, Corlett, PR, et al.Global prefrontal and fronto-amygdala dysconnectivity in bipolar I disorder with psychosis history. Biol Psychiatry 2012; 73: 565–573.CrossRefGoogle ScholarPubMed
Barbas, H. Anatomic basis of cognitive-emotional interactions in the primate prefrontal cortex. Neurosci Biobehav Rev 1995; 19: 499–510.CrossRefGoogle ScholarPubMed
Benedetti, FRecent findings on the role of white matter pathology in Bipolar Disorder. Harv Rev Psychiatry 2013 [in press].Google Scholar
Benedetti, F, Absinta, M, Rocca, MA, Radaelli, D, Poletti, S, Bernasconi, A, et al.Tract-specific white matter structural disruption in patients with bipolar disorder. Bipolar Disord 2011; 13: 414–424.CrossRefGoogle ScholarPubMed
Benedetti, F, Bernasconi, A, Blasi, V, Cadioli, M, Colombo, C, Falini, A, et al.Neural and genetic correlates of antidepressant response to sleep deprivation: a fMRI study of moral valence decision in bipolar depression. Arch Gen Psychiatry 2007; 64: 179–187.CrossRefGoogle ScholarPubMed
Benedetti, F, Yeh, PH, Bellani, M, Radaelli, D, Nicoletti, MA, Poletti, S, et al.Disruption of white matter integrity in bipolar depression as a possible structural marker of illness. Biol Psychiatry 2011; 69: 309–317.CrossRefGoogle Scholar
Craig, AD. Significance of the insula for the evolution of human awareness of feelings from the body. Ann N Y Acad Sci 2011; 1225: 72–82.CrossRefGoogle ScholarPubMed
Daunizeau, J, Stephan, KE, Friston, KJ. Stochastic dynamic causal modelling of fMRI data: should we care about neural noise?. Neuroimage 2012; 62: 464–481.CrossRefGoogle ScholarPubMed
Dickstein, DP, Gorrostieta, C, Ombao, H, Goldberg, LD, Brazel, AC, Gable, CJ, et al.Fronto-temporal spontaneous resting state functional connectivity in pediatric bipolar disorder. Biol Psychiatry 2010; 68: 839–846.CrossRefGoogle ScholarPubMed
Friston, KJ, Harrison, L, Penny, W. Dynamic causal modelling. Neuroimage 2003; 19: 1273–1302.CrossRefGoogle ScholarPubMed
Ghashghaei, HT, Hilgetag, CC, Barbas, H. Sequence of information processing for emotions based on the anatomic dialogue between prefrontal cortex and amygdala. Neuroimage 2007; 34: 905–923.CrossRefGoogle ScholarPubMed
Goodwin, F, Jamison, KManic-depressive illness 2nd ed.New York: Oxford University Press; 2007.Google Scholar
Hamann, S. Blue genes: wiring the brain for depression. Nat Neurosci 2005; 8: 701–703.CrossRefGoogle ScholarPubMed
Hamilton, M. A rating scale for depression. J Neurol Neurosurg Psychiatry 1960; 23: 56–62.CrossRefGoogle ScholarPubMed
Hamilton, M. Development of a rating scale for primary depressive illness. Br J Soc Clin Psychol 1967; 6: 278–296.CrossRefGoogle ScholarPubMed
Hariri, AR, Bookheimer, SY, Mazziotta, JC. Modulating emotional responses: effects of a neocortical network on the limbic system. Neuroreport 2000; 11: 43–48.CrossRefGoogle ScholarPubMed
Hariri, AR, Mattay, VS, Tessitore, A, Kolachana, B, Fera, F, Goldman, D, et al.Serotonin transporter genetic variation and the response of the human amygdala. Science 2002; 297: 400–403.CrossRefGoogle ScholarPubMed
Jollant, F, Lawrence, NL, Olie, E, Guillaume, S, Courtet, P. The suicidal mind and brain: a review of neuropsychological and neuroimaging studies. World J Biol Psychiatry 2011; 12: 319–339.CrossRefGoogle ScholarPubMed
Kotter, R. Online retrieval, processing, and visualization of primate connectivity data from the CoCoMac database. Neuroinformatics 2004; 2: 127–144.CrossRefGoogle ScholarPubMed
Ladouceur, CD, Diwadkar, VA, White, R, Bass, J, Birmaher, B, Axelson, DA, et al.Fronto-limbic function in unaffected offspring at familial risk for bipolar disorder during an emotional working memory paradigm. Dev Cogn Neurosci 5C 2013 185196.CrossRefGoogle Scholar
LeDoux, JEThe emotional brain: the mysterious underpinnings of emotional life New York: Simon & Schuster; 1996.Google Scholar
Levesque, J, Eugene, F, Joanette, Y, Paquette, V, Mensour, B, Beaudoin, G, et al.Neural circuitry underlying voluntary suppression of sadness. Biol Psychiatry 2003; 53: 502–510.CrossRefGoogle ScholarPubMed
Li, B, Daunizeau, J, Stephan, KE, Penny, W, Hu, D, Friston, KGeneralised filtering and stochastic DCM for fMRI. Neuroimage 2011; 58: 442–457.CrossRefGoogle ScholarPubMed
Lin, F, Weng, S, Xie, B, Wu, G, Lei, HAbnormal frontal cortex white matter connections in bipolar disorder: a DTI tractography study. J Affect Disord 2011; 131: 299–306.CrossRefGoogle ScholarPubMed
Liu, H, Tang, Y, Womer, F, Fan, G, Lu, T, Driesen, N, et al.Differentiating patterns of amygdala-frontal functional connectivity in schizophrenia and bipolar disorder. Schizophr Bull 4022014 469477.CrossRefGoogle ScholarPubMed
Mayberg, HS, Liotti, M, Brannan, SK, McGinnis, S, Mahurin, RK, Jerabek, PA, et al.Reciprocal limbic-cortical function and negative mood: converging PET findings in depression and normal sadness. Am J Psychiatry 1999; 156: 675–682.Google ScholarPubMed
Murphy, FC, Sahakian, BJNeuropsychology of bipolar disorder. Br J Psychiatry Suppl 2001; 41: s120–s127.CrossRefGoogle ScholarPubMed
Murphy, FC, Sahakian, BJ, Rubinsztein, JS, Michael, A, Rogers, RD, Robbins, TW, et al.Emotional bias and inhibitory control processes in mania and depression. Psychol Med 1999; 29: 1307–1321.CrossRefGoogle ScholarPubMed
Ongur, D, Ferry, AT, Price, JLArchitectonic subdivision of the human orbital and medial prefrontal cortex. J Comp Neurol 2003; 460: 425–449.CrossRefGoogle ScholarPubMed
Pan, LA, Hassel, S, Segreti, AM, Nau, SA, Brent, DA, Phillips, MLDifferential patterns of activity and functional connectivity in emotion processing neural circuitry to angry and happy faces in adolescents with and without suicide attempt. Psychol Med 2013; 43(10): 1–14.CrossRefGoogle ScholarPubMed
Penny, WD, Stephan, KE, Daunizeau, J, Rosa, MJ, Friston, KJ, Schofield, TM, et al.Comparing families of dynamic causal models. PLoS Comput Biol 2010; 6: e1000709.CrossRefGoogle ScholarPubMed
Petrides, M, Pandya, DNEfferent association pathways from the rostral prefrontal cortex in the macaque monkey. J Neurosci 2007; 27: 11573–11586.CrossRefGoogle ScholarPubMed
Pezawas, L, Meyer-Lindenberg, A, Drabant, EM, Verchinski, BA, Munoz, KE, Kolachana, BS, et al.5-HTTLPR polymorphism impacts human cingulate-amygdala interactions: a genetic susceptibility mechanism for depression. Nat Neurosci 2005; 8: 828–834.CrossRefGoogle ScholarPubMed
Phelps, EA, LeDoux, JEContributions of the amygdala to emotion processing: from animal models to human behavior. Neuron 2005; 48: 175–187.CrossRefGoogle ScholarPubMed
Phillips, ML, Ladouceur, CD, Drevets, WCA neural model of voluntary and automatic emotion regulation: implications for understanding the pathophysiology and neurodevelopment of bipolar disorder. Mol Psychiatry 2008; 13: 829[33–57]CrossRefGoogle ScholarPubMed
Price, JL, Drevets, WCNeurocircuitry of mood disorders. Neuropsychopharmacology 2010; 35: 192–216.CrossRefGoogle ScholarPubMed
Rich, BA, Fromm, SJ, Berghorst, LH, Dickstein, DP, Brotman, MA, Pine, DS, et al.Neural connectivity in children with bipolar disorder: impairment in the face emotion processing circuit. J Child Psychol Psychiatry 2008; 49: 88–96.CrossRefGoogle ScholarPubMed
Rubinsztein, JS, Michael, A, Paykel, ES, Sahakian, BJCognitive impairment in remission in bipolar affective disorder. Psychol Med 2000; 30: 1025–1036.CrossRefGoogle ScholarPubMed
Scharinger, C, Rabl, U, Sitte, HH, Pezawas, LImaging genetics of mood disorders. Neuroimage 2010; 53: 810–821.CrossRefGoogle ScholarPubMed
Seghier, ML, Zeidman, P, Neufeld, NH, Leff, AP, Price, CJIdentifying abnormal connectivity in patients using dynamic causal modeling of FMRI responses. Front Syst Neurosci 2010; 4: 1–14.Google ScholarPubMed
Sole, B, Bonnin, CM, Torrent, C, Martinez-Aran, A, Popovic, D, Tabares-Seisdedos, R, et al.Neurocognitive impairment across the bipolar spectrum. CNS Neurosci Ther 2012; 18: 194–200.CrossRefGoogle ScholarPubMed
Sonty, SP, Mesulam, MM, Weintraub, S, Johnson, NA, Parrish, TB, Gitelman, DRAltered effective connectivity within the language network in primary progressive aphasia. J Neurosci 2007; 27: 1334–1345.CrossRefGoogle ScholarPubMed
Stein, JL, Wiedholz, LM, Bassett, DS, Weinberger, DR, Zink, CF, Mattay, VS, et al.A validated network of effective amygdala connectivity. Neuroimage 2007; 36: 736–745.CrossRefGoogle ScholarPubMed
Stephan, KE, Weiskopf, N, Drysdale, PM, Robinson, PA, Friston, KJComparing hemodynamic models with DCM. Neuroimage 2007; 38: 387–401.CrossRefGoogle ScholarPubMed
Stephan, KE, Penny, WD, Moran, RJ, den Ouden, HE, Daunizeau, J, Friston, KJTen simple rules for dynamic causal modeling. Neuroimage 2010; 49: 3099–3109.CrossRefGoogle ScholarPubMed
Sui, J, Pearlson, G, Caprihan, A, Adali, T, Kiehl, KA, Liu, J, et al.Discriminating schizophrenia and bipolar disorder by fusing fMRI and DTI in a multimodal CCA+ joint ICA model. Neuroimage 2011; 57: 839–855.CrossRefGoogle Scholar
Sussmann, JE, Lymer, GK, McKirdy, J, Moorhead, TW, Munoz Maniega, S, Job, D, et al.White matter abnormalities in bipolar disorder and schizophrenia detected using diffusion tensor magnetic resonance imaging. Bipolar Disord 2009; 11: 11–18.CrossRefGoogle ScholarPubMed
Townsend, JD, Torrisi, SJ, Lieberman, MD, Sugar, CA, Bookheimer, SY, Altshuler, LLFrontal-amygdala connectivity alterations during emotion downregulation in bipolar I disorder. Biol Psychiatry 2013; 73: 127–135.CrossRefGoogle ScholarPubMed
Versace, A, Almeida, JR, Quevedo, K, Thompson, WK, Terwilliger, RA, Hassel, S, et al.Right orbitofrontal corticolimbic and left corticocortical white matter connectivity differentiate bipolar and unipolar depression. Biol Psychiatry 2010; 68: 560–567.CrossRefGoogle ScholarPubMed
Versace, A, Almeida, JR, Hassel, S, Walsh, ND, Novelli, M, Klein, CR, et al.Elevated left and reduced right orbitomedial prefrontal fractional anisotropy in adults with bipolar disorder revealed by tract-based spatial statistics. Arch Gen Psychiatry 2008; 65: 1041–1052.CrossRefGoogle ScholarPubMed
Vizueta, N, Rudie, JD, Townsend, JD, Torrisi, S, Moody, TD, Bookheimer, SY, et al.Regional fMRI hypoactivation and altered functional connectivity during emotion processing in nonmedicated depressed patients with bipolar II disorder. Am J Psychiatry 2012; 169: 831–840.CrossRefGoogle ScholarPubMed
Wagner, G, Schultz, CC, Koch, K, Schachtzabel, C, Sauer, H, Schlosser, RGPrefrontal cortical thickness in depressed patients with high risk for suicidal behavior. J Psychiatr Res 2012; 46: 1449–1455.CrossRefGoogle ScholarPubMed
Wessa, M, Kanske, P, Linke, JBipolar disorder: a neural network perspective on a disorder of emotion and motivation. Restor Neurol Neurosci 3212014 5162.Google ScholarPubMed
Zarate, CA Jr., Mathews, DC, Furey, MLHuman biomarkers of rapid antidepressant effects. Biol Psychiatry 2013; 73: 1142–1155.CrossRefGoogle ScholarPubMed
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