Aberrant intrinsic connectivity of hippocampus and amygdala overlap in the fronto-insular and dorsomedial-prefrontal cortex in major depressive disorder

Frontiers in Human Neuroscience

Volumn , Issue OCT, 2013, Pages

  Tahmasian, Masoud ^a,b   Knight, David C ^c   Manoliu, Andrei ^a   Schwerthöffer, Dirk ^a   Scherr, Martin ^a,d   Meng, Chun ^a,e   Shao, Junming ^a   Peters, Henning ^a   Doll, Anselm ^a,e   Khazaie, Habibolah ^b   Drzezga, Alexander ^a,f   Bäuml, Josef ^a   Zimmer, Claus ^a   Förstl, Hans ^a   Wohlschläger, Afra M ^a   Riedl, Valentin ^a   Sorg, Christian ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b KERMANSHAH UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^d PARACELSUS MEDICAL UNIVERSITY   (Austria)

^e UNIVERSITY OF MUNICH   (Germany)

^f UNIVERSITY HOSPITAL OF COLOGNE   (Germany)

Author keywords

Amygdala; Dorsomedial prefrontal cortex; Fronto insular operculum; Hippocampus; Intrinsic functional connectivity; Major depressive disorder; Resting state fMRI

Indexed keywords

ADULT; AMYGDALOID NUCLEUS; ARTICLE; BOLD SIGNAL; BRAIN REGION; BRAIN SIZE; CLINICAL ARTICLE; CONTROLLED STUDY; DORSOMEDIAL PREFRONTAL CORTEX; FEMALE; FRONTAL OPERCULUM; FRONTO INSULAR PREFRONTAL CORTEX; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GRAY MATTER; HIPPOCAMPUS; HUMAN; MAJOR DEPRESSION; MALE; NEUROPATHOLOGY; PATHOLOGICAL ANATOMY; PREFRONTAL CORTEX; RESTING STATE NETWORK;

EID: 84886379239     PISSN: 16625161     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnhum.2013.00639     Document Type: Article

References (61)

1. Aggleton, J. P. (2012). Multiple anatomical systems embedded within the primate medial temporal lobe: implications for hippocampal function. Neurosci. Biobehav. Rev. 36, 1579-1596. doi:10.1016/j. neubiorev.2011.09.005
2. American Psychiatric Association. (2000). Diagnostic and Statistical Manual of Mental Disorders (DSMIV-TR), 4th Edn. Washington, DC: American Psychiatric Association.
3. Anand, A., Li, Y., Wang, Y., Wu, J., Gao, S., Bukhari, L., et al. (2005). Activity and connectivity of brain mood regulating circuit in depression: a functional magnetic resonance study. Biol. Psychiatry 57, 1079-1088. doi: 10.1016/j.biopsych.2005.02.021
4. Ashburner, J., and Friston, K. J. (2005). Unified segmentation. Neuroimage 26, 839-851. doi:10.1016/j. neuroimage.2005.02.018
5. Beck, A. T., Ward, C. H., Mendelson, M., Mock, J., and Erbaugh, J. (1961). An inventory for measuring depression. Arch. Gen. Psychiatry 4, 561-571. doi:10.1001/archpsyc.1961.01710120031004
6. Bruhl, A. B., Kaffenberger, T., and Herwig, U. (2010). Serotonergic and noradrenergic modulation of emotion processing by single dose antidepressants. Neuropsychopharmacology 35, 521-533. doi:10.1038/npp.2009.159
7. Cao, X., Liu, Z., Xu, C., Li, J., Gao, Q., Sun, N., et al. (2012). Disrupted resting-state functional connectivity of the hippocampus in medicationnaive patients with major depressive disorder. J. Affect. Disord. 141, 194-203. doi:10.1016/j.jad.2012.03.002
8. Chai, X. J., Castanon, A. N., Ongur, D., and Whitfield-Gabrieli, S. (2012). Anticorrelations in resting state networks without global signal regression. Neuroimage 59, 1420-1428. doi:10.1016/j. neuroimage.2011.08.048
9. Chang, C., and Glover, G. H. (2009). Effects of model-based physiological noise correction on default mode network anti-correlations and correlations. Neuroimage 47, 1448-1459. doi:10.1016/j.neuroimage.2009.05. 012
10. Delaveau, P., Jabourian, M., Lemogne, C., Guionnet, S., Bergouignan, L., and Fossati, P. (2011). Brain effects of antidepressants in major depression: a meta-analysis of emotional processing studies. J. Affect. Disord. 130, 66-74. doi:10.1016/j.jad.2010.09.032
11. Dosenbach, N. U., Fair, D. A., Miezin, F. M., Cohen, A. L., Wenger, K. K., Dosenbach, R. A., et al. (2007). Distinct brain networks for adaptive and stable task control in humans. Proc. Natl. Acad. Sci. U.S.A. 104, 11073-11078. doi:10. 1073/pnas.0704320104
12. Drevets, W. C., Price, J. L., and Furey, M. L. (2008). Brain structural and functional abnormalities in mood disorders: implications for neurocircuitry models of depression. Brain Struct. Funct. 213, 93-118. doi:10. 1007/s00429-008-0189-x
13. Endicott, J., Spitzer, R. L., Fleiss, J. L., and Cohen, J. (1976). The global assessment scale. A procedure for measuring overall severity of psychiatric disturbance. Arch. Gen. Psychiatry 33, 766-771. doi:10.1001/archpsyc. 1976.01770060086012
14. Etkin, A., Prater, K. E., Schatzberg, A. F., Menon, V., and Greicius, M. D. (2009). Disrupted amygdalar subregion functional connectivity and evidence of a compensatory network in generalized anxiety disorder. Arch. Gen. Psychiatry 66, 1361-1372. doi:10.1001/ archgenpsychiatry.2009.104
15. First, M. B., Spitzer, R. L., Gibbon, M., and Williams, J. B. W. (1996). Structured Clinical Interview for DSMIV Axis I Disorders: Clinician Version (SCID-CV). Washington, DC: American Psychiatric Press, Inc.
16. Fox, M. D., and Raichle, M. E. (2007). Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat. Rev. Neurosci. 8, 700-711. doi:10. 1038/nrn2201
17. Fox, M. D., Snyder, A. Z., Vincent, J. L., Corbetta, M., Van Essen, D. C., and Raichle, M. E. (2005). The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc. Natl. Acad. Sci. U.S.A. 102, 9673-9678. doi:10.1073/pnas.0504136102
18. Fox, M. D., Zhang, D., Snyder, A. Z., and Raichle, M. E. (2009). The global signal and observed anticorrelated resting state brain networks. J. Neurophysiol. 101, 3270-3283. doi:10. 1152/jn.90777.2008
19. Frodl, T., Jager, M., Smajstrlova, I., Born, C., Bottlender, R., Palladino, T., et al. (2008a). Effect of hippocampal and amygdala volumes on clinical outcomes in major depression: a 3year prospective magnetic resonance imaging study. J. PsychiatryNeurosci. 33, 423-430.
20. Frodl, T. S., Koutsouleris, N., Bottlender, R., Born, C., Jager, M., Scupin, I., et al. (2008b). Depressionrelated variation in brain morphology over 3 years: effects of stress? Arch. Gen. Psychiatry 65,1156-1165. doi:10.1001/archpsyc.65.10.1156
21. Frodl, T., Meisenzahl, E. M., Zetzsche, T., Born, C., Jager, M., Groll, C., et al. (2003). Larger amygdala volumes in first depressive episode as compared to recurrent major depression and healthy control subjects. Biol. Psychiatry 53,338-344. doi: 10.1016/ S0006-3223(02)01474-9
22. Fu, C. H., Williams, S. C., Brammer, M. J., Suckling, J., Kim, J., Cleare, A. J., et al. (2007). Neural responses to happy facial expressions in major depression following antidepressant treatment. Am. J. Psychiatry 164, 599-607. doi:10.1176/appi.ajp.164. 4.599
23. Greicius, M. D., Flores, B. H., Menon, V., Glover, G. H., Solvason, H. B., Kenna, H., et al. (2007). Resting-state functional connectivity in major depression: abnormally increased contributions from subgenual cingulate cortex and thalamus. Biol. Psychiatry 62, 429-437. doi:10.1016/j.biopsych. 2006.09.020
24. Hamilton, J. P., Chen, M. C., and Gotlib, I. H. (2013). Neural systems approaches to understanding major depressive disorder: an intrinsic functional organization perspective. Neurobiol. Dis. 52,4-11. doi:10. 1016/j.nbd.2012.01.015
25. Hamilton, J. P., Etkin, A., Furman, D. J., Lemus, M. G., Johnson, R. F., and Gotlib, I. H. (2012). Functional neuroimaging of major depressive disorder: a meta-analysis and new integration of base line activation and neural response data. Am. J. Psychiatry 169, 693-703. doi:10.1176/appi. ajp.2012.11071105
26. Hamilton, J. P., Furman, D. J., Chang, C., Thomason, M. E., Dennis, E., and Gotlib, I. H. (2011). Defaultmode and task-positive network activity in major depressive disorder: implications for adaptive and maladaptive rumination. Biol. Psychiatry 70, 327-333. doi:10.1016/j.biopsych.2011.02.003
27. Hamilton, J. P., and Gotlib, I. H. (2008). Neuralsubstratesofincreasedmemory sensitivity for negative stimuli in major depression. Biol. Psychiatry 63, 1155-1162. doi:10.1016/j.biopsych.2007.12.015
28. Hamilton, M. (1960). A rating scale for depression. J. Neurol. Neurosurg. Psychiatr. 23, 56-62. doi: 10.1136/jnnp.23.1.56
29. Heller, A. S., Johnstone, T., Light, S. N., Peterson, M. J., Kolden, G. G., Kalin, N. H., et al. (2013). Relationships between changes in sustained fronto-striatal connectivity and positive affect in major depression resulting from antidepressant treatment. Am. J. Psychiatry 170, 197-206. doi:10.1176/appi.ajp.2012. 12010014
30. Kahn, I., Andrews-Hanna, J. R., Vincent, J. L., Snyder, A. Z., and Buckner, R. L. (2008). Distinct cortical anatomy linked to subregions of the medial temporal lobe revealed by intrinsic functional connectivity. J. Neurophysiol. 100, 129-139. doi: 10.1152/jn.00077.2008
31. Kalisch, R. (2009). The functional neuroanatomy of reappraisal: time matters. Neurosci. Biobehav. Rev. 33, 1215-1226. doi:10.1016/j.neubiorev.2009.06.003
32. Kempton, M. J., Salvador, Z., Munafo, M. R., Geddes, J. R., Simmons, A., Frangou, S., et al. (2011). Structural neuroimaging studies in major depressive disorder. Metaanalysis and comparison with bipolar disorder. Arch. Gen. Psychiatry 68, 675-690. doi:10.1001/archgenpsychiatry.2011.60
33. Kendler, K. S., Thornton, L. M., and Gardner, C. O. (2001). Genetic risk, number of previous depressive episodes, and stressful life events in predicting onset of major depression. Am. J. Psychiatry 158, 582-586. doi:10.1176/appi.ajp.158.4.582
34. Kessler, R. C., Berglund, P., Demler, O., Jin, R., Koretz, D., Merikangas, K. R., et al. (2003). The epidemiology of major depressive disorder: results from the National Comorbidity Survey Replication (NCS-R). JAMA 289, 3095-3105. doi:10.1001/ jama.289.23.3095
35. Kronmuller, K. T., Pantel, J., Gotz, B., Kohler, S., Victor, D., Mundt, C., et al. (2008). Life events and hippocampal volume in first-episode major depression. J. Affect. Disord. 110, 241-247. doi:10.1016/j.jad.2008.01.022
36. LaBar, K. S., and Cabeza, R. (2006). Cognitive neuroscience of emotional memory. Nat. Rev. Neurosci. 7, 54-64. doi:10.1038/nrn1825
37. LeDoux, J. (2007). The amygdala. Curr. Biol. 17, R868-R874. doi:10.1016/j. cub.2007.08.005
38. Liang, Z., King, J., and Zhang, N. (2012). Anticorrelated resting-state functional connectivity in awake rat brain. Neuroimage 59, 1190-1199. doi:10.1016/j.neuroimage.2011.08.009
39. MacQueen, G., and Frodl, T. (2011). The hippocampus in major depression: evidence for the convergence of the bench and bedside in psychiatric research? Mol. Psychiatry 16, 252-264. doi:10.1038/mp.2010.80
40. Menon, V. (2011). Large-scale brain networks and psychopathology: a unifying triple network model. Trends Cogn. Sci. (Regul. Ed.) 15, 483-506. doi:10.1016/j.tics.2011.08.003
41. Murphy, K., Bodurka, J., and Bandettini, P. A. (2007). How long to scan? The relationship between fMRI temporal signal to noise ratio and necessary scan duration. Neuroimage 34, 565-574. doi:10.1016/j.neuroimage.2006.09.032
42. Murray, E. A., Wise, S. P., and Drevets, W. C. (2011). Localization of dysfunction in major depressive disorder: prefrontal cortex and amygdala. Biol. Psychiatry 69, e43-e54. doi:10.1016/j.biopsych.2010.09.041
43. Ochsner, K. N., and Gross, J. J. (2005). The cognitive control of emotion. Trends Cogn. Sci. (Regul. Ed.) 9, 242-249. doi:10.1016/j.tics.2005.03.010
44. Perlman, G., Simmons, A. N., Wu, J., Hahn, K. S., Tapert, S. F., Max, J. D., et al. (2012). Amygdala response and functional connectivity during emotion regulation: a study of 14 depressed adolescents. J. Affect. Disord. 139, 75-84. doi:10.1016/j.jad.2012.01.044
45. Rigucci, S., Serafini, G., Pompili, M., Kotzalidis, G. D., and Tatarelli, R. (2010). Anatomical and functional correlates in major depressive disorder: the contribution of neuroimagingstudies. WorldJ. Biol. Psychiatry 11, 165-180. doi:10.1080/15622970903131571
46. Robinson, O. J., and Sahakian, B. J. (2008). Recurrence in major depressive disorder: a neurocognitive perspective. Psychol. Med. 38, 315-318. doi:10.1017/S0033291707001249
47. Roy, A. K., Shehzad, Z., Margulies, D. S., Kelly, A. M., Uddin, L. Q., Gotimer, K., et al. (2009). Functional connectivity of the human amygdala using resting state fMRI. Neuroimage 45, 614-626. doi:10.1016/j.neuroimage.2008.11.030
48. Scheidegger, M., Walter, M., Lehmann, M., Metzger, C., Grimm, S., Boeker, H., et al. (2012). Ketamine decreases resting state functional network connectivity in healthy subjects: implications for antidepressant drug action. PLoS ONE 7:e44799. doi:10. 1371/journal.pone.0044799
49. Seeley, W. W., Menon, V., Schatzberg, A. F., Keller, J., Glover, G. H., Kenna, H., et al. (2007). Dissociable intrinsic connectivity networks for salience processing and executive control. J. Neurosci. 27, 2349-2356. doi:10. 1523/JNEUROSCI.5587-06.2007
50. Segal, Z. V., Williams, J. M., Teas-dale, J. D., and Gemar, M. (1996). A cognitive science perspective on kindling and episode sensitization in recurrent affective disorder. Psychol. Med. 26, 371-380. doi:10.1017/ S0033291700034760
51. Sheline, Y. I., Barch, D. M., Price, J. L., Rundle, M. M., Vaishnavi, S. N., Snyder, A. Z., et al. (2009). The default mode network and self-referential processes in depression. Proc. Natl. Acad. Sci. U.S.A. 106, 1942-1947. doi:10.1073/pnas.0812686106
52. Sheline, Y. I., Price, J. L., Yan, Z., and Mintun, M. A. (2010). Restingstate functional MRI in depression unmasks increased connectivity between networks via the dorsal nexus. Proc. Natl. Acad. Sci. U.S.A. 107, 11020-11025. doi:10. 1073/pnas.1000446107
53. Sheline, Y. I., Wang, P. W., Gado, M. H., Csernansky, J. G., and Vannier, M. W. (1996). Hippocampal atrophy in recurrent major depression. Proc. Natl. Acad. Sci. U.S.A. 93, 3908-3913. doi:10.1073/pnas.93.9.3908
54. Sorg, C., Manoliu, A., Neufang, S., Myers, N., Peters, H., Schwerthoffer, D., et al. (2012). Increased intrinsic brain activityin the striatum reflects symptom dimensions in schizophrenia. Schizophr. Bull. 39, 387-395. doi:10.1093/schbul/sbr184
55. Squire, L. R., Stark, C. E., and Clark, R. E. (2004). The medial temporal lobe. Annu. Rev. Neurosci. 27, 279-306. doi:10.1146/annurev.neuro.27.070203.144130
56. Tang, Y., Kong, L., Wu, F., Womer, E., Jiang, W., Cao, Y., et al. (2012). Decreased functional connectivity between the amygdala and the left ventral prefrontal cortex in treatment-naive patients with major depressive disorder: a resting-state functional magnetic resonance imaging study. Psychol. Med. 43, 1921-1927. doi:10.1017/S0033291712002759
57. Van Dijk, K. R., Sabuncu, M. R., and Buckner, R. L. (2012). The influence of head motion on intrinsic functional connectivity MRI. Neuroimage 59, 431-438. doi: 10.1016/j. neuroimage.2011.07.044
58. Veer, I. M., Beckmann, C. F., van Tol, M. J., Ferrarini, L., Milles, J., Veltman, D. J., et al. (2010).Whole brain restingstate analysis reveals decreased functional connectivityin major depression. Front. Syst. Neurosci. 4:41. doi: 10.3389/fnsys.2010.00041
59. Winecoff, A., Labar, K. S., Madden, D. J., Cabeza, R., and Huettel, S. A. (2011). Cognitive and neural contributors to emotion regulation in aging. Soc. Cogn. Affect. Neurosci. 6, 165-176. doi:10.1093/scan/nsq030
60. Wong, C. W., Olafsson, V., Tal, O., and Liu, T. T. (2012). Anti-correlated networks, global signal regression, and the effects of caffeine in resting-state functional MRI. Neuroimage 63, 356-364. doi:10.1016/j. neuroimage.2012.06.035
61. Wood, K. H., Ver Hoef, L. W., and Knight, D. C. (2012). Neural mechanisms underlying the conditioned diminution of the unconditioned fear response. Neuroimage 60, 787-799. doi:10.1016/j.neuroimage.2011.12.048