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Distinct neurobiological signatures of brain connectivity in depression subtypes during natural viewing of emotionally salient films

Published online by Cambridge University Press:  18 February 2016

C. C. Guo ,
M. P. Hyett ,
V. T. Nguyen ,
G. B. Parker  and
M. J. Breakspear
C. C. Guo*
Affiliation:
QIMR Berghofer Medical Research Institute, Herston, QLD, Australia
M. P. Hyett
Affiliation:
QIMR Berghofer Medical Research Institute, Herston, QLD, Australia School of Psychiatry, University of New South Wales, Sydney, Australia
V. T. Nguyen
Affiliation:
QIMR Berghofer Medical Research Institute, Herston, QLD, Australia
G. B. Parker
Affiliation:
School of Psychiatry, University of New South Wales, Sydney, Australia Black Dog Institute, Sydney, Australia
M. J. Breakspear
Affiliation:
QIMR Berghofer Medical Research Institute, Herston, QLD, Australia Black Dog Institute, Sydney, Australia
*
*Address for correspondence: C. C. Guo, Ph.D., QIMR Berghofer Medical Research Institute, Locked Bag 2000, Royal Brisbane Hospital, Herston, QLD 4029, Australia. (Email: christine.cong@gmail.com)
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Abstract

Background

Establishing an evidence-based diagnostic system informed by the biological (dys)function of the nervous system is a major priority in psychiatry. This objective, however, is often challenged by difficulties in identifying homogeneous clinical populations. Melancholia, a biological and endogenous subtype for major depressive disorder, presents a canonical test case in the search of biological nosology.

Method

We employed a unique combination of naturalistic functional magnetic resonance imaging (fMRI) paradigms – resting state and free viewing of emotionally salient films – to search for neurobiological signatures of depression subtypes. fMRI data were acquired from 57 participants; 17 patients with melancholia, 17 patients with (non-melancholic) major depression and 23 matched healthy controls.

Results

Patients with melancholia showed a prominent loss of functional connectivity in hub regions [including ventral medial prefrontal cortex, anterior cingulate cortex (ACC) and superior temporal gyrus] during natural viewing, and in the posterior cingulate cortex while at rest. Of note, the default mode network showed diminished reactivity to external stimuli in melancholia, which correlated with the severity of anhedonia. Intriguingly, the subgenual ACC, a potential target for treating depression with deep brain stimulation (DBS), showed divergent changes between the two depression subtypes, with increased connectivity in the non-melancholic and decreased connectivity in the melancholic subsets.

Conclusion

These findings reveal neurobiological changes specific to depression subtypes during ecologically valid behavioural conditions, underscoring the critical need to respect differing neurobiological processes underpinning depressive subtypes.

Keywords

Depressionemotionfunctional connectivitynatural viewing
Type
Original Articles
Information
Psychological Medicine , Volume 46 , Issue 7 , May 2016 , pp. 1535 - 1545
Copyright
Copyright © Cambridge University Press 2016 

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References

Anand, A, Li, Y, Wang, Y, Wu, J, Gao, S, Bukhari, L, Mathews, VP, Kalnin, A, Lowe, MJ (2005). Activity and connectivity of brain mood regulating circuit in depression: a functional magnetic resonance study. Biological Psychiatry 57, 1079–1088.CrossRefGoogle ScholarPubMed
Anticevic, A, Cole, MW, Murray, JD, Corlett, PR, Wang, X-J, Krystal, JH (2012). The role of default network deactivation in cognition and disease. Trends in Cognitive Sciences 16, 584–592.CrossRefGoogle ScholarPubMed
Betti, V, Della Penna, S, de Pasquale, F, Mantini, D, Marzetti, L, Romani, GL, Corbetta, M (2013). Natural scenes viewing alters the dynamics of functional connectivity in the human brain. Neuron 79, 782–797.Google Scholar
Bluhm, R, Williamson, P, Lanius, R, Théberge, J, Densmore, M, Bartha, R, Neufeld, R, Osuch, E (2009). Resting state default-mode network connectivity in early depression using a seed region-of-interest analysis: decreased connectivity with caudate nucleus. Psychiatry and Clinical Neurosciences 63, 754–761.Google Scholar
Casanova, R, Srikanth, R, Baer, A, Laurienti, PJ, Burdette, JH, Hayasaka, S, Flowers, L, Wood, F, Maldjian, JA (2007). Biological parametric mapping: a statistical toolbox for multimodality brain image analysis. NeuroImage 34, 137–143.Google Scholar
Craig, AD (2009). How do you feel – now? The anterior insula and human awareness. Nature Reviews Neuroscience 10, 59–70.CrossRefGoogle Scholar
Cullen, KR, Gee, DG, Klimes-Dougan, B, Gabbay, V, Hulvershorn, L, Mueller, BA, Camchong, J, Bell, CJ, Houri, A, Kumra, S, Lim, KO, Castellanos, FX, Milham, MP (2009). A preliminary study of functional connectivity in comorbid adolescent depression. Neuroscience Letters 460, 227–231.CrossRefGoogle ScholarPubMed
Cuthbert, BN, Insel, TR (2013). Toward the future of psychiatric diagnosis: the seven pillars of RDoC. BMC Medicine 11, 126.Google Scholar
Day, CCVA, Williams, LML (2012). Finding a biosignature for melancholic depression. Expert Review of Neurotherapeutics 12, 835–847.CrossRefGoogle ScholarPubMed
Drevets, W, Price, J, Simpson, J, Todd, R (1997). Subgenual prefrontal cortex abnormalities in mood disorders. Nature 386, 824–827.Google Scholar
Drevets, WC, Price, JL, Furey, ML (2008 a). Brain structural and functional abnormalities in mood disorders: implications for neurocircuitry models of depression. Brain Structure & Function 213, 93–118.Google Scholar
Drevets, WC, Savitz, J, Trimble, M (2008 b). The subgenual anterior cingulate cortex in mood disorders. CNS Spectrums 13, 663–681.CrossRefGoogle ScholarPubMed
Friston, KJ, Holmes, AP, Worsley, KJ, Poline, J-P, Frith, CD, Frackowiak, RSJ (1994). Statistical parametric maps in functional imaging: a general linear approach. Human Brain Mapping 2, 189–210.CrossRefGoogle Scholar
Greicius, MD, Flores, BH, Menon, V, Glover, GH, Solvason, HB, Kenna, H, Reiss, AL, Schatzberg, AF (2007). Resting-state functional connectivity in major depression: abnormally increased contributions from subgenual cingulate cortex and thalamus. Biological Psychiatry 62, 429–437.Google Scholar
Gross, JJ, Levenson, RW (1995). Emotion elicitation using films. Cognition & Emotion 9, 87–108.Google Scholar
Guo, CC, Gorno-Tempini, ML, Gesierich, B, Henry, M, Trujillo, A, Shany-Ur, T, Jovicich, J, Robinson, SD, Kramer, JH, Rankin, KP, Miller, BL, Seeley, WW (2013). Anterior temporal lobe degeneration produces widespread network-driven dysfunction. Brain 136, 2979–2991.Google Scholar
Hasson, U, Malach, R, Heeger, DJ (2010). Reliability of cortical activity during natural stimulation. Trends in Cognitive Sciences 14, 40–48.CrossRefGoogle ScholarPubMed
Horn, DI, Yu, C, Steiner, J, Buchmann, J, Kaufmann, J, Osoba, A, Eckert, U, Zierhut, KC, Schiltz, K, He, H, Biswal, B, Bogerts, B, Walter, M (2010). Glutamatergic and resting-state functional connectivity correlates of severity in major depression – the role of pregenual anterior cingulate cortex and anterior insula. Frontiers in Systems Neuroscience 4, 1–10.Google Scholar
Kross, E, Davidson, M, Weber, J, Ochsner, K (2009). Coping with emotions past: the neural bases of regulating affect associated with negative autobiographical memories. Society of Biological Psychiatry Biological Psychiatry 65, 361–366.CrossRefGoogle ScholarPubMed
Kumfor, F, Sapey-Triomphe, L-A, Leyton, CE, Burrell, JR, Hodges, JR, Piguet, O (2014). Degradation of emotion processing ability in corticobasal syndrome and Alzheimer's disease. Brain 137, 3061–3072.Google Scholar
Liao, X-H, Xia, M-R, Xu, T, Dai, Z-J, Cao, X-Y, Niu, H-J, Zuo, X-N, Zang, Y-F, He, Y (2013). Functional brain hubs and their test-retest reliability: a multiband resting-state functional MRI study. NeuroImage 83, 969–982.Google Scholar
Lui, S, Wu, Q, Qiu, L, Yang, X, Kuang, W, Chan, RCK, Huang, X, Kemp, GJ, Mechelli, A, Gong, Q (2011). Resting-state functional connectivity in treatment-resistant depression. American Journal of Psychiatry 168, 642–648.Google Scholar
Menon, V (2011). Large-scale brain networks and psychopathology: a unifying triple network model. Trends in Cognitive Sciences 15, 483–506.Google Scholar
Myers-Schulz, B, Koenigs, M (2012). Functional anatomy of ventromedial prefrontal cortex: implications for mood and anxiety disorders. Molecular Psychiatry 17, 132–141.Google Scholar
Nemeroff, CB (2007). The burden of severe depression: a review of diagnostic challenges and treatment alternatives. Journal of Psychiatric Research 41, 189–206.Google Scholar
Nguyen, VT, Breakspear, M, Hu, X, Guo, CC (2015). The integration of the internal and external milieu in the insula during dynamic emotional experiences. NeuroImage 124, 455–463.CrossRefGoogle ScholarPubMed
Nummenmaa, L, Glerean, E, Viinikainen, M, Jääskeläinen, IP, Hari, R, Sams, M (2012). Emotions promote social interaction by synchronizing brain activity across individuals. Proceedings of the National Academy of Sciences USA 109, 9599–9604.Google Scholar
Osuch, EA, Ketter, TA, Kimbrell, TA, George, MS, Benson, BE, Herscovitch, MWW, Post, RM (2000). Regional cerebral metabolism associated with anxiety symptoms in affective disorder patients. Biological Psychiatry 48, 1020–1023.CrossRefGoogle ScholarPubMed
Parker, G, Fink, M, Shorter, E, Taylor, MA, Akiskal, H, Berrios, G, Bolwig, T, Brown, WA, Carroll, B, Healy, D, Klein, DF, Koukopoulos, A, Michels, R, Paris, J, Rubin, RT, Spitzer, R, Swartz, C (2010). Issues for DSM-5: whither melancholia? The case for its classification as a distinct mood disorder. American Journal of Psychiatry 167, 745–747.CrossRefGoogle ScholarPubMed
Parker, G, Fletcher, K, Hyett, M, Hadzi-Pavlovic, D, Barrett, M, Synnott, H (2009). Measuring melancholia: the utility of a prototypic symptom approach. Psychological Medicine 39, 989–998.Google Scholar
Parker, G, Hadzi-Pavlovic, D, Wilhelm, K, Hickie, I, Brodaty, H, Boyce, P, Mitchell, P, Eyers, K (1994). Defining melancholia: properties of a refined sign-based measure. British Journal of Psychiatry 164, 316–326.Google Scholar
Rush, AJ, Trivedi, MH, Ibrahim, HM, Carmody, TJ, Arnow, B, Klein, DN, Markowitz, JC, Ninan, PT, Kornstein, S, Manber, R, Thase, ME, Kocsis, JH, Keller, MB (2003). The 16-item quick inventory of depressive symptomatology (QIDS), clinician rating (QIDS-C), and self-report (QIDS-SR): a psychometric evaluation in patients with chronic major depression. Biological Psychiatry 54, 573–583.Google 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, 2349–2356.Google Scholar
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, 11020–11025.Google Scholar
Sliz, D, Hayley, S (2012). Major depressive disorder and alterations in insular cortical activity: a review of current functional magnetic imaging research. Frontiers Frontiers in Human Neuroscience 6, 323.CrossRefGoogle ScholarPubMed
Smith, SM, Nichols, TE (2009). Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. NeuroImage 44, 83–98.Google Scholar
Stanley, ML, Moussa, MN, Paolini, BM, Lyday, RG, Burdette, JH, Laurienti, PJ (2013). Defining nodes in complex brain networks. Frontiers in Computational Neuroscience 7, 169.Google Scholar
van Tol, M-J, Li, M, Metzger, CD, Hailla, N, Horn, DI, Li, W, Heinze, HJ, Bogerts, B, Steiner, J, He, H, Walter, M (2014). Local cortical thinning links to resting-state disconnectivity in major depressive disorder. Cambridge University Press Psychological Medicine 44, 2053–2065.Google Scholar
Veer, IM, Beckmann, CF, van Tol, M-J, Ferrarini, L, Milles, J, Veltman, DJ, Aleman, A, van Buchem, MA, van der Wee, NJ, Rombouts, SARB (2010). Whole brain resting-state analysis reveals decreased functional connectivity in major depression. Frontiers in Systems Neuroscience 4, 1–10.Google Scholar
Walter, M, Henning, A, Grimm, S, Schulte, RF, Beck, J, Dydak, U, Schnepf, B, Boeker, H, Boesiger, P, Northoff, G (2009). The relationship between aberrant neuronal activation in the pregenual anterior cingulate, altered glutamatergic metabolism, and anhedonia in major depression. Archives of General Psychiatry 66, 478–486.Google Scholar
Zald, DH, Mattson, DL, Pardo, JV (2002). Brain activity in ventromedial prefrontal cortex correlates with individual differences in negative affect. Proceedings of the National Academy of Sciences USA 99, 2450–2454.Google Scholar
Zhang, B, Li, M, Qin, W, Demenescu, LR, Metzger, CD, Bogerts, B, Yu, C, Walter, M ((in press). Altered functional connectivity density in major depressive disorder at rest. Springer Berlin Heidelberg European Archives of Psychiatry and Clinical Neuroscience.Google Scholar
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