Hostname: page-component-8448b6f56d-dnltx Total loading time: 0 Render date: 2024-04-15T11:53:51.927Z Has data issue: false hasContentIssue false

Decoupling of the amygdala to other salience network regions in adolescent-onset recurrent major depressive disorder

Published online by Cambridge University Press:  20 January 2016

R. H. Jacobs
Affiliation:
Department of Psychiatry, University of Illinois at Chicago, Chicago, IL, USA
A. Barba
Affiliation:
Department of Psychiatry, University of Illinois at Chicago, Chicago, IL, USA
J. R. Gowins
Affiliation:
Department of Psychiatry, University of Illinois at Chicago, Chicago, IL, USA
H. Klumpp
Affiliation:
Department of Psychiatry, University of Illinois at Chicago, Chicago, IL, USA
L. M. Jenkins
Affiliation:
Department of Psychiatry, University of Illinois at Chicago, Chicago, IL, USA
B. J. Mickey
Affiliation:
Department of Psychiatry, University of Michigan, Ann Arbor, MI, USA
O. Ajilore
Affiliation:
Department of Psychiatry, University of Illinois at Chicago, Chicago, IL, USA
M. Peciña
Affiliation:
Department of Psychiatry, University of Michigan, Ann Arbor, MI, USA
M. Sikora
Affiliation:
Department of Psychiatry, University of Michigan, Ann Arbor, MI, USA
K. A. Ryan
Affiliation:
Department of Psychiatry, University of Michigan, Ann Arbor, MI, USA
D. T. Hsu
Affiliation:
Department of Psychiatry, University of Michigan, Ann Arbor, MI, USA Department of Psychiatry, Stony Brook University, Stony Brook, NY, USA
R. C. Welsh
Affiliation:
Department of Psychiatry, University of Michigan, Ann Arbor, MI, USA Department of Radiology, Molecular and Behavioral Neuroscience Institute, Ann Arbor, MI, USA
J.-K. Zubieta
Affiliation:
Department of Psychiatry, University of Michigan, Ann Arbor, MI, USA Department of Radiology, Molecular and Behavioral Neuroscience Institute, Ann Arbor, MI, USA
K. L. Phan
Affiliation:
Department of Psychiatry, University of Illinois at Chicago, Chicago, IL, USA Mental Health Service Line, Jesse Brown VA Medical Center, Chicago, IL, USA
S. A. Langenecker*
Affiliation:
Department of Psychiatry, University of Illinois at Chicago, Chicago, IL, USA
*
*Address for correspondence: S. A. Langenecker, Ph.D., Department of Psychiatry, University of Illinois at Chicago, 1601 W. Taylor Street, M/C 912, Chicago, IL 60612, USA. (Email: slangenecker@psych.uic.edu)

Abstract

Background

Recent meta-analyses of resting-state networks in major depressive disorder (MDD) implicate network disruptions underlying cognitive and affective features of illness. Heterogeneity of findings to date may stem from the relative lack of data parsing clinical features of MDD such as phase of illness and the burden of multiple episodes.

Method

Resting-state functional magnetic resonance imaging data were collected from 17 active MDD and 34 remitted MDD patients, and 26 healthy controls (HCs) across two sites. Participants were medication-free and further subdivided into those with single v. multiple episodes to examine disease burden. Seed-based connectivity using the posterior cingulate cortex (PCC) seed to probe the default mode network as well as the amygdala and subgenual anterior cingulate cortex (sgACC) seeds to probe the salience network (SN) were conducted.

Results

Young adults with remitted MDD demonstrated hyperconnectivity of the left PCC to the left inferior frontal gyrus and of the left sgACC to the right ventromedial prefrontal cortex (PFC) and left hippocampus compared with HCs. Episode-independent effects were observed between the left PCC and the right dorsolateral PFC, as well as between the left amygdala and right insula and caudate, whereas the burden of multiple episodes was associated with hypoconnectivity of the left PCC to multiple cognitive control regions as well as hypoconnectivity of the amygdala to large portions of the SN.

Conclusions

This is the first study of a homogeneous sample of unmedicated young adults with a history of adolescent-onset MDD illustrating brain-based episodic features of illness.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alexopoulos, GS, Hoptman, MJ, Kanellopoulos, D, Murphy, CF, Lim, KO, Gunning, FM (2012). Functional connectivity in the cognitive control network and the default mode network in late-life depression. Journal of Affective Disorders 139, 5665.CrossRefGoogle ScholarPubMed
Aron, AR, Durston, S, Eagle, DM, Logan, GD, Stinear, CM, Stuphorn, V (2007). Converging evidence for a fronto-basal-ganglia network for inhibitory control of action and cognition. Journal of Neuroscience 27, 1186011864.CrossRefGoogle Scholar
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
Bluhm, RL, Clark, CR, McFarlane, AC, Moores, KA, Shaw, ME, Lanius, RA (2011). Default network connectivity during a working memory task. Human Brain Mapping 32, 10291035.CrossRefGoogle ScholarPubMed
Bressler, SL, Menon, V (2010). Large-scale brain networks in cognition: emerging methods and principles. Trends in Cognitive Sciences 14, 277290.CrossRefGoogle ScholarPubMed
Briceño, EM, Weisenbach, SL, Rapport, LJ, Hazlett, KE, Bieliauskas, LA, Haase, BD, Ransom, MT, Brinkman, ML, Pecina, M, Schteingart, DE, Starkman, MN, Giordani, B, Welsh, RC, Noll, DC, Zubieta, J-K, Langenecker, SA (2013). Shifted inferior frontal laterality in women with major depressive disorder is related to emotion-processing deficits. Psychological Medicine 43, 14331445.CrossRefGoogle ScholarPubMed
Crowther, A, Smoski, MJ, Minkel, J, Moore, T, Gibbs, D, Petty, C, Bizzell, J, Schiller, CE, Sideris, J, Carl, H, Dichter, GS (2015). Resting-state connectivity predictors of response to psychotherapy in major depressive disorder. Neuropsychopharmacology 40, 16591673.CrossRefGoogle ScholarPubMed
de Kwaasteniet, BP, Rive, MM, Ruhé, HG, Schene, AH, Veltman, DJ, Fellinger, L, van Wingen, GA, Denys, D (2015). Decreased resting-state connectivity between neurocognitive networks in treatment resistant depression. Frontiers in Psychiatry 6, 28.CrossRefGoogle ScholarPubMed
Dichter, GS, Gibbs, D, Smoski, MJ (2015). A systematic review of relations between resting-state functional-MRI and treatment response in major depressive disorder. Journal of Affective Disorders 172, 817.CrossRefGoogle ScholarPubMed
Drevets, WC, Price, JL, Furey, ML (2008). Brain structural and functional abnormalities in mood disorders: implications for neurocircuitry models of depression. Brain Structure and Function 213, 93118.CrossRefGoogle ScholarPubMed
Fox, MD, Snyder, AZ, Vincent, JL, Corbetta, M, Van Essen, DC, Raichle, ME (2005). The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proceedings of the National Academy of Sciences USA 102, 96739678.CrossRefGoogle ScholarPubMed
Fox, MD, Zhang, D, Snyder, AZ, Raichle, ME (2009). The global signal and observed anticorrelated resting state brain networks. Journal of Neurophysiology 101, 32703283.CrossRefGoogle ScholarPubMed
Gabbay, V, Ely, BA, Qingyang, L, Bangaru, SD, Panzer, AM, Alonso, CM, Castellanos, FX, Milham, MP (2013). Striatum-based circuitry of adolescent depression and anhedonia. Journal of the American Academy of Child and Adolescent Psychiatry 52, 628641.CrossRefGoogle ScholarPubMed
Hamilton, JP, Etkin, A, Furman, DJ, Lemus, MG, Johnson, RF, Gotlib, IH (2012). Functional neuroimaging of major depressive disorder: a meta-analysis and new integration of base line activation and neural response data. American Journal of Psychiatry 169, 693703.CrossRefGoogle ScholarPubMed
Hamilton, JP, Farmer, M, Fogelman, P, Gotlib, IH (2015). Depressive rumination, the default-mode network, and the dark matter of clinical science. Biological Psychiatry 78, 224230.CrossRefGoogle Scholar
Hamilton, M (1960). A rating scale for depression. Journal of Neurology, Neurosurgery and Psychiatry 23, 5662.CrossRefGoogle ScholarPubMed
Harrison, BJ, Pujol, J, Ortiz, H, Fornito, A, Pantelis, C, Yücel, M (2008). Modulation of brain resting-state networks by sad mood induction. PLoS ONE 3, e1794.CrossRefGoogle ScholarPubMed
Jacobs, RH, Jenkins, LM, Gabriel, LB, Barba, A, Ryan, KA, Weisenbach, SL, Verges, A, Baker, AM, Peters, AT, Crane, NA, Gotlib, IH, Zubieta, J-K, Phan, KL, Langenecker, SA (2014). Increased coupling of intrinsic networks in remitted depressed youth predicts rumination and cognitive control. PLOS ONE 9, e104366.CrossRefGoogle ScholarPubMed
Jo, HJ, Gotts, SJ, Reynolds, RC, Bandettini, PA, Martin, A, 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
Kaiser, RH, Andrews-Hanna, JR, Wager, TD, Pizzagalli, DA (2015). Large-scale network dysfunction in major depressive disorder: a meta-analysis of resting-state functional connectivity. JAMA Psychiatry 72, 603611.CrossRefGoogle ScholarPubMed
Keller, MB, Trivedi, MH, Thase, ME, Shelton, RC, Kornstein, SG, Nemeroff, CB, Friedman, ES, Gelenberg, AJ, Kocsis, JH, Dunner, DL, Hirschfeld, RM, Rothschild, AJ, Ferguson, JM, Schatzberg, AF, Zajecka, JM, Pedersen, RD, Yan, B, Ahmed, S, Musgnung, J, Ninan, PT (2007). The Prevention of Recurrent Episodes of Depression with Venlafaxine for Two Years (PREVENT) Study: outcomes from the 2-year and combined maintenance phases. Journal of Clinical Psychiatry 68, 12461256.CrossRefGoogle ScholarPubMed
Kelly, AMC, Di Martino, A, Uddin, LQ, Shehzad, Z, Gee, DG, Reiss, PT, Margulies, DS, Castellanos, FX, Milham, MP (2009). Development of anterior cingulate functional connectivity from late childhood to early adulthood. Cerebral Cortex 19, 640657.CrossRefGoogle ScholarPubMed
Kerestes, R, Bhagwagar, Z, Nathan, PJ, Meda, SA, Ladouceur, CD, Maloney, K, Matuskey, D, Ruf, B, Saricicek, A, Wang, F, Pearlson, GD, Phillips, ML, Blumberg, HP (2012). Prefrontal cortical response to emotional faces in individuals with major depressive disorder in remission. Psychiatry Research 202, 3037.CrossRefGoogle ScholarPubMed
Langenecker, SA, Briceño, EM, Hamid, NM, Nielson, KA (2007). An evaluation of distinct volumetric and functional MRI contributions toward understanding age and task performance: a study in the basal ganglia. Brain Research 1135, 5868.CrossRefGoogle ScholarPubMed
Lee, RSC, Hermens, DF, Porter, MA, Redoblado-Hodge, A (2012). A meta-analysis of cognitive deficits in first-episode major depressive disorder. Journal of Affective Disorders 140, 113124.CrossRefGoogle ScholarPubMed
Majer, M, Nater, UM, Lin, JM, Capuron, L, Reeves, WC (2010). Association of childhood trauma with cognitive function in healthy adults: a pilot study. BMC Neurology 10, 61.CrossRefGoogle ScholarPubMed
Margulies, DS, Kelly, AMC, Uddin, LQ, Biswal, BB, Castellanos, FX, Milham, MP (2007). Mapping the functional connectivity of anterior cingulate cortex. NeuroImage 37, 579588.CrossRefGoogle ScholarPubMed
Mayberg, HS, Liotti, M, Brannan, SK, McGinnis, S, Mahurin, RK, Jerabek, PA, Silva, JA, Tekell, JL, Martin, CC, Lancaster, JL, Fox, PT (1999). Reciprocal limbic-cortical function and negative mood: converging PET findings in depression and normal sadness. American Journal of Psychiatry 156, 675682.CrossRefGoogle ScholarPubMed
McCabe, C, Mishor, Z (2011). Antidepressant medications reduce subcortical-cortical resting-state functional connectivity in healthy volunteers. NeuroImage 57, 13171323.CrossRefGoogle ScholarPubMed
Menon, V (2011). Large-scale brain networks and psychopathology: a unifying triple network model. Trends in Cognitive Sciences 15, 483506.CrossRefGoogle ScholarPubMed
Menon, V, Uddin, LQ (2010). Saliency, switching, attention and control: a network model of insula function. Brain Structure and Function 214, 655667.CrossRefGoogle ScholarPubMed
Pannekoek, JN, Veer, IM, van Tol, MJ, van der Werff, SJA, Demenescu, LR, Aleman, A, Veltman, DJ, Zitman, FG, Rombouts, SARB, van der Wee, NJA (2013). Aberrant limbic and salience network resting-state functional connectivity in panic disorder without comorbidity. Journal of Affective Disorders 145, 2935.CrossRefGoogle ScholarPubMed
Perlman, SB, Almeida, JRC, Kronhaus, DM, Versace, A, LaBarbara, EJ, Klein, CR, Phillips, ML (2012). Amygdala activity and prefrontal cortex-amygdala effective connectivity to emerging emotional faces distinguish remitted and depressed mood states in bipolar disorder. Bipolar Disorders 14, 162174.CrossRefGoogle ScholarPubMed
Pizzagalli, D (2011). Frontocingulate dysfunction in depression: toward biomarkers of treatment response. Neuropsychopharmacology 36, 183206.CrossRefGoogle ScholarPubMed
Price, JL, Drevets, WC (2010). Neurocircuitry of mood disorders. Neuropsychopharmacology 35, 192216.CrossRefGoogle ScholarPubMed
Rogosch, FA, Cicchetti, D, Aber, JL (1995). The role of child maltreatment in early deviations in cognitive and affective processing abilities and later peer relationship problems. Development and Psychopathology 7, 591609.CrossRefGoogle Scholar
Seeley, WW, Menon, V, Schatzberg, AF, Keller, J, Glover, GH, Kenna, H, Reiss, AL, Greicius, MD (2007). Dissociable intrinsic connectivity networks for salience processing and executive control. Journal of Neuroscience 27, 23492356.CrossRefGoogle ScholarPubMed
Sheline, YI, Barch, DM, Price, JL, Rundle, MM, Vaishnavi, SN, Snyder, AZ, Mintun, MA, Wang, S, Coalson, RS, Raichle, ME (2009). The default mode network and self-referential processes in depression. Proceedings of the National Academy of Sciences USA 106, 19421947.CrossRefGoogle ScholarPubMed
Sheline, YI, Price, JL, Yan, Z, Mintun, MA (2010). Resting-state functional MRI in depression unmasks increased connectivity between networks via the dorsal nexus. Proceedings of the National Academy of Sciences USA 107, 1102011025.CrossRefGoogle ScholarPubMed
Spann, MN, Mayes, LC, Kalmar, JH, Guiney, J, Womer, FY, Pittman, B, Mazure, CM, Sinha, R, Blumberg, HP (2012). Childhood abuse and neglect and cognitive flexibility in adolescents. Child Neuropsychology 18, 182189.CrossRefGoogle ScholarPubMed
Sundermann, B, Beverborg, MOL, Pfleiderer, B (2014). Toward literature-based feature selection for diagnostic classification: a meta-analysis of resting-state fMRI in depression. Frontiers in Human Neuroscience 8, 692.CrossRefGoogle ScholarPubMed
Versace, A, Ladouceur, CD, Romero, S, Birmaher, B, Axelson, DA, Kupfer, DJ, Phillips, ML (2010). Altered development of white matter in youth at high familial risk for bipolar disorder: a diffusion tensor imaging study. Journal of the American Academy of Child and Adolescent Psychiatry 49, 12491259.Google ScholarPubMed
Weisenbach, SL, Kassel, MT, Rao, J, Weldon, AL, Avery, ET, Briceño, EM, Ajilore, O, Mann, M, Kales, HC, Welsh, RC, Zubieta, J-K, Langenecker, SA (2014). Differential prefrontal and subcortical circuitry engagement during encoding of semantically related words in patients with late-life depression. International Journal of Geriatric Psychiatry 29, 11041115.CrossRefGoogle ScholarPubMed
Whitfield-Gabrieli, S, Ford, JM (2012). Default mode network activity and connectivity in psychopathology. Annual Review of Clinical Psychology 8, 4976.CrossRefGoogle ScholarPubMed
Supplementary material: File

Jacobs supplementary material

Jacobs supplementary material 1

Download Jacobs supplementary material(File)
File 454.1 KB