Imbalanced spontaneous brain activity in orbitofrontal-insular circuits in individuals with cognitive vulnerability to depression

Journal of Affective Disorders

Volumn 198, Issue , 2016, Pages 56-63

  Zhang, Xiaocui ^a   Di, Xin ^b   Lei, Hui ^c   Yang, Juan ^d   Xiao, Jing ^e   Wang, Xiang ^a   Yao, Shuqiao ^a   Rao, Hengyi ^f,g  

^a CENTRAL SOUTH UNIVERSITY   (China)

^b NEW JERSEY INSTITUTE OF TECHNOLOGY   (United States)

^c HUNAN AGRICULTURAL UNIVERSITY   (China)

^d HAINAN MEDICAL UNIVERSITY   (China)

^e CAPITAL NORMAL UNIVERSITY   (China)

^f SHANGHAI INTERNATIONAL STUDIES UNIVERSITY   (China)

^g UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Amplitude of low frequency fluctuation; fMRI; Hopelessness theory; Major depression disorder; Resting state; Trait depression

Indexed keywords

ADULT; AMPLITUDE OF LOW FREQUENCY FLUCTUATION; ARTICLE; CENTER FOR EPIDEMIOLOGICAL STUDIES DEPRESSION SCALE; COGNITIVE STYLE QUESTIONNAIRE; COGNITIVE VULNERABILITY TO DEPRESSION; CONTROLLED STUDY; CORRELATION ANALYSIS; ELECTROENCEPHALOGRAM; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUSIFORM GYRUS; HOPELESSNESS; HUMAN; INSULA; MAJOR CLINICAL STUDY; MAJOR DEPRESSION; MALE; ORBITAL CORTEX; PRIORITY JOURNAL; PSYCHOMETRY; QUESTIONNAIRE; ADOLESCENT; BRAIN CORTEX; CASE CONTROL STUDY; COGNITION; CROSS-SECTIONAL STUDY; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PHYSIOLOGY; PREFRONTAL CORTEX; TEMPORAL LOBE; YOUNG ADULT;

ADOLESCENT; CASE-CONTROL STUDIES; CEREBRAL CORTEX; COGNITION; CROSS-SECTIONAL STUDIES; DEPRESSIVE DISORDER, MAJOR; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; NEUROIMAGING; PREFRONTAL CORTEX; TEMPORAL LOBE; YOUNG ADULT;

EID: 84978985854     PISSN: 01650327     EISSN: 15732517     Source Type: Journal    
DOI: 10.1016/j.jad.2016.03.001     Document Type: Article

References (75)

1. Abela, J.R., Stolow, D., Mineka, S., Yao, S., Zhu, X.Z., Hankin, B.L., Cognitive vulnerability to depressive symptoms in adolescents in urban and rural Hunan, China: a multiwave longitudinal study. J. Abnorm. Psychol. 120 (2011), 765–778.
2. Abela, J.R.Z., Sarin, S., Cognitive vulnerability to hopelessness depression: a chain is only as strong as its weakest link. Cognit. Ther. Res. 26 (2002), 811–829.
3. Abramson, L.Y.M.G.A.L., Hopelessness depression: a theory-based subtype of depression. Psychol. Rev. 96 (1989), 358–372.
4. Abramson, L.Y., Alloy, L.B., Hankin, B.L., Haeffel, G.J., MacCoon, D.G., Gibb, B.E., Cognitive vulnerability-stress models of depression in a self-regulatory and psychobiological context. Gotlib, I.H., Hammen, C.L., (eds.) Handbook of Depression, 2002, 2002, The Guilford Press, NY, 268–294.
5. Abramson, L.Y., Metalsky, G.I., 1986. The Cognitive Style Questionnaire: Measurement of Negative Cognitive Styles about Self and Consequences. Unpublished manuscript.
6. Alloy, L.B., Abramson, L.Y., Whitehouse, W.G., Hogan, M.E., Panzarella, C., Rose, D.T., Prospective incidence of first onsets and recurrences of depression in individuals at high and low cognitive risk for depression. J. Abnorm. Psychol. 115 (2006), 145–156.
7. Augustine, J.R., Circuitry and functional aspects of the insular lobe in primates including humans. Brain Res. Rev. 22 (1996), 229–244.
8. Barnhofer, T., Duggan, D., Crane, C., Hepburn, S., Fennell, M.J., Williams, J.M., Effects of meditation on frontal alpha-asymmetry in previously suicidal individuals. Neuroreport 18 (2007), 709–712.
9. Beauregard, M., Paquette, V., Levesque, J., Dysfunction in the neural circuitry of emotional self-regulation in major depressive disorder. Neuroreport 17 (2006), 843–846.
10. Beck, A.T., Cognitive models of depression. J. Cogn. Psychother. 1 (1987), 5–37.
11. Biswal, B., Yetkin, F.Z., Haughton, V.M., Hyde, J.S., Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn. Reson. Med. 34 (1995), 537–541.
12. Chen, S., Li, L., Xu, B., Liu, J., Insular cortex involvement in declarative memory deficits in patients with post-traumatic stress disorder. BMC Psychiatry, 9, 2009, 39.
13. Craig, A.D., How do you feel? Interoception: the sense of the physiological condition of the body. Nat. Rev. Neurosci. 3 (2002), 655–666.
14. Craig, A.D., Interoception: the sense of the physiological condition of the body. Curr. Opin. Neurobiol. 13 (2003), 500–505.
15. Craig, A.D., Forebrain emotional asymmetry: a neuroanatomical basis?. Trends Cogn. Sci. 9 (2005), 566–571.
16. De Brito, S.A., Viding, E., Sebastian, C.L., Kelly, P.A., Mechelli, A., Maris, H., McCrory, E.J., Reduced orbitofrontal and temporal grey matter in a community sample of maltreated children. J. Child. Psychol. Psychiatry 54 (2013), 105–112.
17. First, M.B., Spitzer, R.L., Gibbon, M., Williams, J.B., Structured Clinical Interview for DSM-IV Axis I Disorders: Patient Edition (February 1996 Final), SCID-I/P. 1998, Biometrics Research Department, New York State Psychiatric Institute, New York.
18. Galynker, I.I., Cai, J., Ongseng, F., Finestone, H., Dutta, E., Serseni, D., Hypofrontality and negative symptoms in major depressive disorder. J. Nucl. Med. 39 (1998), 608–612.
19. Goldin, P.R., Manber, T., Hakimi, S., Canli, T., Gross, J.J., Neural bases of social anxiety disorder: emotional reactivity and cognitive regulation during social and physical threat. Arch. Gen. Psychiatry 66 (2009), 170–180.
20. Goncalves, S.I., de Munck, J.C., Pouwels, P.J., Schoonhoven, R., Kuijer, J.P., Maurits, N.M., Hoogduin, J.M., Van Someren, E.J., Heethaar, R.M., Lopes, D.S.F., Correlating the alpha rhythm to BOLD using simultaneous EEG/fMRI: inter-subject variability. Neuroimage 30 (2006), 203–213.
21. Gotlib, I.H., Hamilton, J.P., Cooney, R.E., Singh, M.K., Henry, M.L., Joormann, J., Neural processing of reward and loss in girls at risk for major depression. Arch. Gen. Psychiatry 67 (2010), 380–387.
22. Grafman, J., Schwab, K., Warden, D., Pridgen, A., Brown, H.R., Salazar, A.M., Frontal lobe injuries, violence, and aggression: a report of the Vietnam head injury study. Neurology 46 (1996), 1231–1238.
23. Haeffel, G.J., Gibb, B.E., Metalsky, G.I., Alloy, L.B., Abramson, L.Y., Hankin, B.L., Joiner, T.J., Swendsen, J.D., Measuring cognitive vulnerability to depression: development and validation of the cognitive style questionnaire. Clin. Psychol. Rev. 28 (2008), 824–836.
24. Iacoviello, B.M., Alloy, L.B., Abramson, L.Y., Whitehouse, W.G., Hogan, M.E., The course of depression in individuals at high and low cognitive risk for depression: a prospective study. J. Affect. Disord. 93 (2006), 61–69.
25. Jakab, A., Molnar, P.P., Bogner, P., Beres, M., Berenyi, E.L., Connectivity-based parcellation reveals interhemispheric differences in the insula. Brain Topogr. 25 (2012), 264–271.
26. Janig, W., Habler, H.J., Physiology and pathophysiology of visceral pain. Schmerz 16 (2002), 429–446.
27. Jarnum, H., Eskildsen, S.F., Steffensen, E.G., Lundbye-Christensen, S., Simonsen, C.W., Thomsen, I.S., Frund, E.T., Theberge, J., Larsson, E.M., Longitudinal MRI study of cortical thickness, perfusion, and metabolite levels in major depressive disorder. Acta Psychiatr. Scand. 124 (2011), 435–446.
28. Jiao, Q., Ding, J., Lu, G., Su, L., Zhang, Z., Wang, Z., Zhong, Y., Li, K., Ding, M., Liu, Y., Increased activity imbalance in fronto-subcortical circuits in adolescents with major depression. PLoS One, 6, 2011, e25159, 10.1371/journal.pone.0025159.
29. Johnstone, T., van Reekum, C.M., Urry, H.L., Kalin, N.H., Davidson, R.J., Failure to regulate: counterproductive recruitment of top-down prefrontal-subcortical circuitry in major depression. J. Neurosci. 27 (2007), 8877–8884.
30. Joormann, J., Gilbert, K., Gotlib, I.H., Emotion identification in girls at high risk for depression. J. Child. Psychol. Psychiatry 51 (2010), 575–582.
31. Keune, P.M., Bostanov, V., Hautzinger, M., Kotchoubey, B., Mindfulness-based cognitive therapy (MBCT), cognitive style, and the temporal dynamics of frontal EEG alpha asymmetry in recurrently depressed patients. Biol. Psychol. 88 (2011), 243–252.
32. Kong, J., White, N.S., Kwong, K.K., Vangel, M.G., Rosman, I.S., Gracely, R.H., Gollub, R.L., Using fMRI to dissociate sensory encoding from cognitive evaluation of heat pain intensity. Hum. Brain Mapp. 27 (2006), 715–721.
33. Kong, L., Chen, K., Tang, Y., Wu, F., Driesen, N., Womer, F., Fan, G., Ren, L., Jiang, W., Cao, Y., Blumberg, H.P., Xu, K., Wang, F., Functional connectivity between the amygdala and prefrontal cortex in medication-naive individuals with major depressive disorder. J. Psychiatry Neurosci. 38 (2013), 417–422.
34. Lacerda, A.L., Keshavan, M.S., Hardan, A.Y., Yorbik, O., Brambilla, P., Sassi, R.B., Nicoletti, M., Mallinger, A.G., Frank, E., Kupfer, D.J., Soares, J.C., Anatomic evaluation of the orbitofrontal cortex in major depressive disorder. Biol. Psychiatry 55 (2004), 353–358.
35. Levesque, J., Joanette, Y., Mensour, B., Beaudoin, G., Leroux, J.M., Bourgouin, P., Beauregard, M., Neural correlates of sad feelings in healthy girls. Neuroscience 121 (2003), 545–551.
36. Li, H.J., Cao, X.H., Zhu, X.T., Zhang, A.X., Hou, X.H., Xu, Y., Zuo, X.N., Zhang, K.R., Surface-based regional homogeneity in first-episode, drug-naive major depression: a resting-state FMRI study. Biomed. Res. Int., 2014, 2014, 374828.
37. Liu, J., Ren, L., Womer, F.Y., Wang, J., Fan, G., Jiang, W., Blumberg, H.P., Tang, Y., Xu, K., Wang, F., Alterations in amplitude of low frequency fluctuation in treatment-naive major depressive disorder measured with resting-state fMRI. Hum. Brain Mapp. 35 (2014), 4979–4988.
38. Liu, Z., Xu, C., Xu, Y., Wang, Y., Zhao, B., Lv, Y., Cao, X., Zhang, K., Du, C., Decreased regional homogeneity in insula and cerebellum: a resting-state fMRI study in patients with major depression and subjects at high risk for major depression. Psychiatry Res. 182 (2010), 211–215.
39. Ma, Z., Li, R., Yu, J., He, Y., Li, J., Alterations in regional homogeneity of spontaneous brain activity in late-life subthreshold depression. PLoS One, 8, 2013, e53148, 10.1371/journal.pone.0053148.
40. Marcus, M., Yasamy, M.T., van Ommeren, M., Chisholm, D., Saxena, S., Depression: A Global public Health Concern. 2012, World Health Organization, Geneva (Switzerland) 1-2-2013.
41. McCabe, C., Woffindale, C., Harmer, C.J., Cowen, P.J., Neural processing of reward and punishment in young people at increased familial risk of depression. Biol. Psychiatry 72 (2012), 588–594.
42. Mesulam, M.M., Mufson, E.J., Insula of the old world monkey. I. Architectonics in the insulo-orbito-temporal component of the paralimbic brain. J. Comp. Neurol. 212 (1982), 1–22.
43. Monkul, E.S., Silva, L.A., Narayana, S., Peluso, M.A., Zamarripa, F., Nery, F.G., Najt, P., Li, J., Lancaster, J.L., Fox, P.T., Lafer, B., Soares, J.C., Abnormal resting state corticolimbic blood flow in depressed unmedicated patients with major depression: a (15)O-H(2)O PET study. Hum. Brain Mapp. 33 (2012), 272–279.
44. Nagafusa, Y., Okamoto, N., Sakamoto, K., Yamashita, F., Kawaguchi, A., Higuchi, T., Matsuda, H., Assessment of cerebral blood flow findings using 99mTc-ECD single-photon emission computed tomography in patients diagnosed with major depressive disorder. J. Affect. Disord. 140 (2012), 296–299.
45. Nusslock, R., Shackman, A.J., Harmon-Jones, E., Alloy, L.B., Coan, J.A., Abramson, L.Y., Cognitive vulnerability and frontal brain asymmetry: common predictors of first prospective depressive episode. J. Abnorm. Psychol. 120 (2011), 497–503.
46. O'Donnell, M.L., Creamer, M., Pattison, P., Posttraumatic stress disorder and depression following trauma: understanding comorbidity. Am. J. Psychiatry 161 (2004), 1390–1396.
47. Oldfield, R.C., The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9 (1971), 97–113.
48. Petrovic, P., Ingvar, M., Imaging cognitive modulation of pain processing. Pain 95 (2002), 1–5.
49. Phan, K.L., Fitzgerald, D.A., Nathan, P.J., Moore, G.J., Uhde, T.W., Tancer, M.E., Neural substrates for voluntary suppression of negative affect: a functional magnetic resonance imaging study. Biol. Psychiatry 57 (2005), 210–219.
50. Phan, K.L., Wager, T., Taylor, S.F., Liberzon, I., Functional neuroanatomy of emotion: a meta-analysis of emotion activation studies in PET and fMRI. Neuroimage 16 (2002), 331–348.
51. Ploran, E.J., Nelson, S.M., Velanova, K., Donaldson, D.I., Petersen, S.E., Wheeler, M.E., Evidence accumulation and the moment of recognition: dissociating perceptual recognition processes using fMRI. J. Neurosci. 27 (2007), 11912–11924.
52. Radloff, L.S., The CES-D scale a self-report depression scale for research in the general population. Appl. Psychol. Meas. 1 (1977), 385–401.
53. Raichle, M.E., MacLeod, A.M., Snyder, A.Z., Powers, W.J., Gusnard, D.A., Shulman, G.L., A default mode of brain function. Proc. Natl. Acad. Sci. USA 98 (2001), 676–682.
54. Rajkowska, G., Postmortem studies in mood disorders indicate altered numbers of neurons and glial cells. Biol. Psychiatry 48 (2000), 766–777.
55. Rajkowska, G., Miguel-Hidalgo, J.J., Wei, J., Dilley, G., Pittman, S.D., Meltzer, H.Y., Overholser, J.C., Roth, B.L., Stockmeier, C.A., Morphometric evidence for neuronal and glial prefrontal cell pathology in major depression. Biol. Psychiatry 45 (1999), 1085–1098.
56. Scheuerecker, J., Meisenzahl, E.M., Koutsouleris, N., Roesner, M., Schopf, V., Linn, J., Wiesmann, M., Bruckmann, H., Moller, H.J., Frodl, T., Orbitofrontal volume reductions during emotion recognition in patients with major depression. J. Psychiatry Neurosci. 35 (2010), 311–320.
57. Shimamura, A.P., The role of the prefrontal cortex in dynamic filtering. Psychobiology 28 (2000), 207–218.
58. Shmuel, A., Leopold, D.A., Neuronal correlates of spontaneous fluctuations in fMRI signals in monkey visual cortex: Implications for functional connectivity at rest. Hum. Brain Mapp. 29 (2008), 751–761.
59. So, E., Kam, I., Leung, C.M., Chung, D., Liu, Z., Fong, S., The Chinese-bilingual SCID-I/P project: stage 1-reliability for mood disorders and schizophrenia. Hong. Kong J. Psychiatry 13 (2003), 7–18.
60. Sprengelmeyer, R., Steele, J.D., Mwangi, B., Kumar, P., Christmas, D., Milders, M., Matthews, K., The insular cortex and the neuroanatomy of major depression. J. Affect. Disord. 133 (2011), 120–127.
61. Starrs, C.J., Abela, J.R.Z., Shih, J.H., Cohen, J.R., Yao, S., Zhu, X., Hammen, C.L., Stress Generation and Vulnerability in Adolescents in Mainland China. Int. J. Cogn. Ther. 3 (2010), 345–357.
62. Surguladze, S.A., El-Hage, W., Dalgleish, T., Radua, J., Gohier, B., Phillips, M.L., Depression is associated with increased sensitivity to signals of disgust: a functional magnetic resonance imaging study. J. Psychiatr. Res. 44 (2010), 894–902.
63. Takahashi, T., Yucel, M., Lorenzetti, V., Tanino, R., Whittle, S., Suzuki, M., Walterfang, M., Pantelis, C., Allen, N.B., Volumetric MRI study of the insular cortex in individuals with current and past major depression. J. Affect. Disord. 121 (2010), 231–238.
64. Taylor, K.S., Seminowicz, D.A., Davis, K.D., Two systems of resting state connectivity between the insula and cingulate cortex. Hum. Brain Mapp. 30 (2009), 2731–2745.
65. Wang, L., Dai, W., Su, Y., Wang, G., Tan, Y., Jin, Z., Zeng, Y., Yu, X., Chen, W., Wang, X., Si, T., Amplitude of low-frequency oscillations in first-episode, treatment-naive patients with major depressive disorder: a resting-state functional MRI study. PLoS One, 7, 2012, e48658, 10.1371/journal.pone.0048658.
66. Wang, M., Armour, C., Wu, Y., Ren, F., Zhu, X., Yao, S., Factor structure of the CES-D and measurement invariance across gender in Mainland Chinese adolescents. J. Clin. Psychol. 69 (2013), 966–979.
67. Xiao, J., He, Y., McWhinnie, C.M., Yao, S., Altered white matter integrity in individuals with cognitive vulnerability to depression: a tract-based spatial statistics study. Sci. Rep., 5, 2015, 9738, 10.1038/srep09738.
68. Xiao, J., Qiu, Y., He, Y., Cui, L., Auerbach, R.P., McWhinnie, C.M., Yao, S., 'Weakest link’ as a cognitive vulnerability within the hopelessness theory of depression in chinese university students. Stress Health, 2014, 10.1002/smi.2571.
69. Yang, J., Yao, S., Zhu, X., Zhang, C., Ling, Y., Abela, J.R., Esseling, P.G., McWhinnie, C., The impact of stress on depressive symptoms is moderated by social support in Chinese adolescents with subthreshold depression: a multi-wave longitudinal study. J. Affect. Disord. 127 (2010), 113–121.
70. Zang, Y.F., He, Y., Zhu, C.Z., Cao, Q.J., Sui, M.Q., Liang, M., Tian, L.X., Jiang, T.Z., Wang, Y.F., Altered baseline brain activity in children with ADHD revealed by resting-state functional MRI. Brain Dev. 29 (2007), 83–91.
71. Zhang, X., Yao, S., Zhu, X., Wang, X., Zhu, X., Zhong, M., Gray matter volume abnormalities in individuals with cognitive vulnerability to depression: a voxel-based morphometry study. J. Affect. Disord. 136 (2012), 443–452.
72. Zhang, X., Zhu, X., Wang, X., Zhu, X., Zhong, M., Yi, J., Rao, H., Yao, S., First-episode medication-naive major depressive disorder is associated with altered resting brain function in the affective network. PLoS One, 9, 2014, e85241.
73. Zhang, Y.Q., Tang, J.S., Yuan, B., Jia, H., Inhibitory effects of electrically evoked activation of ventrolateral orbital cortex on the tail-flick reflex are mediated by periaqueductal gray in rats. Pain 72 (1997), 127–135.
74. Zhong, M., Wang, X., Xiao, J., Yi, J., Zhu, X., Liao, J., Wang, W., Yao, S., Amygdala hyperactivation and prefrontal hypoactivation in subjects with cognitive vulnerability to depression. Biol. Psychol. 88 (2011), 233–242.
75. Zuo, X.N., Xing, X.X., Test-retest reliabilities of resting-state FMRI measurements in human brain functional connectomics: a systems neuroscience perspective. Neurosci. Biobehav. Rev. 45 (2014), 100–118.