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Differential functional connectivity within an emotion regulation neural network among individuals resilient and susceptible to the depressogenic effects of early life stress

Published online by Cambridge University Press:  10 July 2012

J. M. Cisler ,
G. A. James ,
S. Tripathi ,
T. Mletzko ,
C. Heim ,
X. P. Hu ,
H. S. Mayberg ,
C. B. Nemeroff  and
C. D. Kilts
J. M. Cisler*
Affiliation:
Brain Imaging Research Center, Psychiatric Research Institute, University of Arkansas for Medical Sciences, Little Rock, AR, USA
G. A. James
Affiliation:
Brain Imaging Research Center, Psychiatric Research Institute, University of Arkansas for Medical Sciences, Little Rock, AR, USA
S. Tripathi
Affiliation:
Brain Imaging Research Center, Psychiatric Research Institute, University of Arkansas for Medical Sciences, Little Rock, AR, USA
T. Mletzko
Affiliation:
Department of Psychiatry and Behavioral Sciences, Emory University, Atlanta, GA, USA
C. Heim
Affiliation:
Department of Psychiatry and Behavioral Sciences, Emory University, Atlanta, GA, USA
X. P. Hu
Affiliation:
Biomedical Imaging Technology Center, Emory University, Atlanta, GA, USA
H. S. Mayberg
Affiliation:
Department of Psychiatry and Behavioral Sciences, Emory University, Atlanta, GA, USA
C. B. Nemeroff
Affiliation:
Department of Psychiatry and Behavioral Sciences, University of Miami Miller School of Medicine, Miami, FA, USA
C. D. Kilts
Affiliation:
Brain Imaging Research Center, Psychiatric Research Institute, University of Arkansas for Medical Sciences, Little Rock, AR, USA
*
*Address for correspondence: J. M. Cisler, Ph.D., Brain Imaging Research Center, Psychiatric Research Institute, University of Arkansas for Medical Sciences, 4301 West Markham St, Mail Slot 554, Little Rock, AR 72205, USA. (Email: [email protected])
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Abstract

Background

Early life stress (ELS) is a significant risk factor for depression. The effects of ELS exposure on neural network organization have not been differentiated from the effect of depression. Furthermore, many individuals exposed to ELS do not develop depression, yet the network organization patterns differentiating resiliency versus susceptibility to the depressogenic effects of ELS are not clear.

Method

Women aged 18–44 years with either a history of ELS and no history of depression (n = 7), a history of ELS and current or past depression (n = 19), or a history of neither ELS nor depression (n = 12) underwent a resting-state 3-T functional magnetic resonance imaging (fMRI) scan. An emotion regulation brain network consisting of 21 nodes was described using graph analyses and compared between groups.

Results

Group differences in network topology involved decreased global connectivity and hub-like properties for the right ventrolateral prefrontal cortex (vlPFC) and decreased local network connectivity for the dorsal anterior cingulate cortex (dACC) among resilient individuals. Decreased local connectivity and increased hub-like properties of the left amygdala, decreased hub-like properties of the dACC and decreased local connectivity of the left vlPFC were observed among susceptible individuals. Regression analyses suggested that the severity of ELS (measured by self-report) correlated negatively with global connectivity and hub-like qualities for the left dorsolateral PFC (dlPFC).

Conclusions

These preliminary results suggest functional neural connectivity patterns specific to ELS exposure and resiliency versus susceptibility to the depressogenic effects of ELS exposure.

Keywords

Depressionearly life traumaemotion regulationgraph theoryresting-state fMRI
Type
Original Articles
Information
Psychological Medicine , Volume 43 , Issue 3 , March 2013 , pp. 507 - 518
Copyright
Copyright © Cambridge University Press 2012

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References

Albert, R, Jeong, H, Barabasi, AL (2000). Error and attack tolerance of complex networks. Nature 406, 378–382.CrossRefGoogle ScholarPubMed
Alstott, J, Breakspear, M, Hagmann, P, Cammoun, L, Sporns, O (2009). Modeling the impact of lesions in the human brain. PLoS Computational Biology 5, e1000408.CrossRefGoogle ScholarPubMed
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
Aron, AR, Behrens, TE, Smith, S, Frank, MJ, Poldrack, RA (2007). Triangulating a cognitive control network using diffusion-weighted magnetic resonance imaging (MRI) and functional MRI. Journal of Neuroscience 27, 3743–3752.CrossRefGoogle ScholarPubMed
Aron, AR, Poldrack, RA (2006). Cortical and subcortical contributions to Stop signal response inhibition: role of the subthalamic nucleus. Journal of Neuroscience 26, 2424–2433.CrossRefGoogle ScholarPubMed
Aron, AR, Robbins, TW, Poldrack, RA (2004). Inhibition and the right inferior frontal cortex. Trends in Cognitive Sciences 8, 170–177.CrossRefGoogle ScholarPubMed
Bernstein, DP, Fink, L, Handelsman, L, Foote, J, Lovejoy, M, Wenzel, K, Sapareto, E, Ruggiero, J (1994). Initial reliability and validity of a new retrospective measure of child abuse and neglect. American Journal of Psychiatry 151, 1132–1136.Google ScholarPubMed
Bremner, JD, Narayan, M, Anderson, ER, Staib, LH, Miller, HL, Charney, DS (2000 a). Hippocampal volume reduction in major depression. American Journal of Psychiatry 157, 115–118.CrossRefGoogle ScholarPubMed
Bremner, JD, Vermetten, E, Mazure, CM (2000 b). Development and preliminary psychometric properties of an instrument for the measurement of childhood trauma: the Early Trauma Inventory. Depression and Anxiety 12, 1–12.3.0.CO;2-W>CrossRefGoogle ScholarPubMed
Bullmore, E, Sporns, O (2009). Complex brain networks: graph theoretical analysis of structural and functional systems. Nature Reviews Neuroscience 10, 186–198.CrossRefGoogle ScholarPubMed
Bullmore, ET, Bassett, DS (2011). Brain graphs: graphical models of the human brain connectome. Annual Review of Clinical Psychology 7, 113–140.CrossRefGoogle ScholarPubMed
Carpenter, LL, Gawuga, CE, Tyrka, AR, Lee, JK, Anderson, GM, Price, LH (2010). Association between plasma IL-6 response to acute stress and early-life adversity in healthy adults. Neuropsychopharmacology 35, 2617–2623.CrossRefGoogle ScholarPubMed
Craddock, RC, Holtzheimer, PE 3rd, Hu, XP, Mayberg, HS (2009). Disease state prediction from resting state functional connectivity. Magnetic Resonance in Medicine 62, 1619–1628.CrossRefGoogle ScholarPubMed
Craig, AD (2002). How do you feel? Interoception: the sense of the physiological condition of the body. Nature Reviews Neuroscience 3, 655–666.CrossRefGoogle Scholar
Critchley, HD, Wiens, S, Rotshtein, P, Ohman, A, Dolan, RJ (2004). Neural systems supporting interoceptive awareness. Nature Neuroscience 7, 189–195.CrossRefGoogle ScholarPubMed
Davidson, RJ, Irwin, W, Anderle, MJ, Kalin, NH (2003). The neural substrates of affective processing in depressed patients treated with venlafaxine. American Journal of Psychiatry 160, 64–75.CrossRefGoogle ScholarPubMed
Davis, M, Whalen, PJ (2001). The amygdala: vigilance and emotion. Molecular Psychiatry 6, 13–34.CrossRefGoogle ScholarPubMed
Deco, G, Jirsa, VK, McIntosh, AR (2011). Emerging concepts for the dynamical organization of resting-state activity in the brain. Nature Reviews Neuroscience 12, 43–56.CrossRefGoogle ScholarPubMed
Elliott, R, Zahn, R, Deakin, JF, Anderson, IM (2011). Affective cognition and its disruption in mood disorders. Neuropsychopharmacology 36, 153–182.CrossRefGoogle ScholarPubMed
Erk, S, Mikschl, A, Stier, S, Ciaramidaro, A, Gapp, V, Weber, B, Walter, H (2010). Acute and sustained effects of cognitive emotion regulation in major depression. Journal of Neuroscience 30, 15726–15734.CrossRefGoogle ScholarPubMed
First, MB, Spitzer Robert, L, Gibbon, M, Williams, JBW (2002). Structured Clinical Interview for DSM-IV-TR Axis I Disorders, Research Version, Non-Patient Edition. Biometrics Research, New York State Psychiatric Institute: New York.Google Scholar
Franco, A, Shin, J, Choi, KS, Craddock, R, Mayberg, H, Hu, X (2011). Increased intra-slice functional correlation: problem and solution. Poster presented at the annual Organization for Human Brain Mapping Conference. Quebec City, Canada.Google Scholar
Gillespie, CF, Nemeroff, CB (2007). Corticotropin-releasing factor and the psychobiology of early-life stress. Current Directions in Psychological Science 16, 85–89.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.CrossRefGoogle ScholarPubMed
Hamilton, M (1960). A rating scale for depression. Journal of Neurology, Neurosurgery, and Psychiatry 23, 56–62.CrossRefGoogle ScholarPubMed
Hanson, JL, Chung, MK, Avants, BB, Shirtcliff, EA, Gee, JC, Davidson, RJ, Pollak, SD (2010). Early stress is associated with alterations in the orbitofrontal cortex: a tensor-based morphometry investigation of brain structure and behavioral risk. Journal of Neuroscience 30, 7466–7472.CrossRefGoogle ScholarPubMed
Heberlein, KA, Hu, X (2004). Simultaneous acquisition of gradient-echo and asymmetric spin-echo for single-shot z-shim: Z-SAGA. Magnetic Resonance in Medicine 51, 212–216.CrossRefGoogle ScholarPubMed
Heim, C, Newport, DJ, Heit, S, Graham, YP, Wilcox, M, Bonsall, R, Miller, AH, Nemeroff, CB (2000). Pituitary-adrenal and autonomic responses to stress in women after sexual and physical abuse in childhood. Journal of the American Medical Association 284, 592–597.CrossRefGoogle ScholarPubMed
Heim, C, Plotsky, PM, Nemeroff, CB (2004). Importance of studying the contributions of early adverse experience to neurobiological findings in depression. Neuropsychopharmacology 29, 641–648.CrossRefGoogle ScholarPubMed
James, GA, Kelley, ME, Craddock, RC, Holtzheimer, PE, Dunlop, BW, Nemeroff, CB, Mayberg, HS, Hu, XP (2009). Exploratory structural equation modeling of resting-state fMRI: applicability of group models to individual subjects. NeuroImage 45, 778–787.CrossRefGoogle ScholarPubMed
Johnstone, T, Van Reekum, CM, Urry, HL, Kalin, NH, Davidson, RJ (2007). Failure to regulate: counterproductive recruitment of top-down prefrontal-subcortical circuitry in major depression. Journal of Neuroscience 27, 8877–8884.CrossRefGoogle ScholarPubMed
Kessler, RC, Davis, CG, Kendler, KS (1997). Childhood adversity and adult psychiatric disorder in the US National Comorbidity Survey. Psychological Medicine 27, 1101–1119.CrossRefGoogle ScholarPubMed
Kilpatrick, DG, Ruggiero, KJ, Acierno, R, Saunders, BE, Resnick, HS, Best, CL (2003). Violence and risk of PTSD, major depression, substance abuse/dependence, and comorbidity: results from the National Survey of Adolescents. Journal of Consulting and Clinical Psychology 71, 692–700.CrossRefGoogle ScholarPubMed
LeDoux, JE (2000). Emotion circuits in the brain. Annual Review of Neuroscience 23, 155–184.CrossRefGoogle ScholarPubMed
Lee, BT, Seok, JH, Lee, BC, Cho, SW, Yoon, BJ, Lee, KU, Chae, JH, Choi, IG, Ham, BJ (2008). Neural correlates of affective processing in response to sad and angry facial stimuli in patients with major depressive disorder. Progress in Neuropsychopharmacology and Biological Psychiatry 32, 778–785.CrossRefGoogle ScholarPubMed
Lynall, ME, Bassett, DS, Kerwin, R, McKenna, PJ, Kitzbichler, M, Muller, U, Bullmore, E (2010). Functional connectivity and brain networks in schizophrenia. Progress in Neuropsychopharmacology and Biological Psychiatry 30, 9477–9487.Google ScholarPubMed
Matthews, SC, Strigo, IA, Simmons, AN, Yang, TT, Paulus, MP (2008). Decreased functional coupling of the amygdala and supragenual cingulate is related to increased depression in unmedicated individuals with current major depressive disorder. Journal of Affective Disorders 111, 13–20.CrossRefGoogle ScholarPubMed
Matz, K, Junghofer, M, Elbert, T, Weber, K, Wienbruch, C, Rockstroh, B (2010). Adverse experiences in childhood influence brain responses to emotional stimuli in adult psychiatric patients. International Journal of Psychophysiology 75, 277–286.CrossRefGoogle ScholarPubMed
McCauley, J, Kern, DE, Kolodner, K, Dill, L, Schroeder, AF, Dechant, HK, Ryden, J, Derogatis, LR, Bass, EB (1997). Clinical characteristics of women with a history of childhood abuse: unhealed wounds. Journal of the American Medical Association 277, 1362–1368.CrossRefGoogle ScholarPubMed
McRae, K, Hughes, B, Chopra, S, Gabrieli, JD, Gross, JJ, Ochsner, KN (2010). The neural bases of distraction and reappraisal. Journal of Cognitive Neuroscience 22, 248–262.CrossRefGoogle ScholarPubMed
Mueller, SC, Maheu, FS, Dozier, M, Peloso, E, Mandell, D, Leibenluft, E, Pine, DS, Ernst, M (2010). Early-life stress is associated with impairment in cognitive control in adolescence: an fMRI study. Neuropsychologia 48, 3037–3044.CrossRefGoogle ScholarPubMed
Ochsner, KN, Bunge, SA, Gross, JJ, Gabrieli, JD (2002). Rethinking feelings: an fMRI study of the cognitive regulation of emotion. Journal of Cognitive Neuroscience 14, 1215–1229.CrossRefGoogle ScholarPubMed
Ochsner, KN, Ray, RD, Cooper, JC, Robertson, ER, Chopra, S, Gabrieli, JD, Gross, JJ (2004). For better or for worse: neural systems supporting the cognitive down- and up-regulation of negative emotion. NeuroImage 23, 483–499.CrossRefGoogle ScholarPubMed
Price, JL, Drevets, WC (2010). Neurocircuitry of mood disorders. Neuropsychopharmacology 35, 192–216.CrossRefGoogle ScholarPubMed
Resnick, HS, Kilpatrick, DG, Dansky, BS, Saunders, BE, Best, CL (1993). Prevalence of civilian trauma and posttraumatic stress disorder in a representative national sample of women. Journal of Consulting and Clinical Psychology 61, 984–991.CrossRefGoogle Scholar
Rubinov, M, Sporns, O (2010). Complex network measures of brain connectivity: uses and interpretations. NeuroImage 52, 1059–1069.CrossRefGoogle ScholarPubMed
Seminowicz, DA, Mayberg, HS, McIntosh, AR, Goldapple, K, Kennedy, S, Segal, Z, Rafi-Tari, S (2004). Limbic-frontal circuitry in major depression: a path modeling metanalysis. NeuroImage 22, 409–418.CrossRefGoogle ScholarPubMed
Taylor, SE, Eisenberger, NI, Saxbe, D, Lehman, BJ, Lieberman, MD (2006). Neural responses to emotional stimuli are associated with childhood family stress. Biological Psychiatry 60, 296–301.CrossRefGoogle ScholarPubMed
van den Heuvel, MP, Mandl, RC, Kahn, RS, Hulshoff Pol, HE (2009). Functionally linked resting-state networks reflect the underlying structural connectivity architecture of the human brain. Human Brain Mapping 30, 3127–3141.CrossRefGoogle ScholarPubMed
van Wijk, BC, Stam, CJ, Daffertshofer, A (2010). Comparing brain networks of different size and connectivity density using graph theory. PLoS ONE 5, e13701.CrossRefGoogle ScholarPubMed
Vasic, N, Walter, H, Sambataro, F, Wolf, RC (2009). Aberrant functional connectivity of dorsolateral prefrontal and cingulate networks in patients with major depression during working memory processing. Psychological Medicine 39, 977–987.CrossRefGoogle ScholarPubMed
Victor, TA, Furey, ML, Fromm, SJ, Ohman, A, Drevets, WC (2010). Relationship between amygdala responses to masked faces and mood state and treatment in major depressive disorder. Archives of General Psychiatry 67, 1128–1138.CrossRefGoogle ScholarPubMed
Vythilingam, M, Heim, C, Newport, J, Miller, AH, Anderson, E, Bronen, R, Brummer, M, Staib, L, Vermetten, E, Charney, DS, Nemeroff, CB, Bremner, JD (2002). Childhood trauma associated with smaller hippocampal volume in women with major depression. American Journal of Psychiatry 159, 2072–2080.CrossRefGoogle ScholarPubMed
Wager, TD, Davidson, ML, Hughes, BL, Lindquist, MA, Ochsner, KN (2008). Prefrontal-subcortical pathways mediating successful emotion regulation. Neuron 59, 1037–1050.CrossRefGoogle ScholarPubMed
Weber, K, Miller, GA, Schupp, HT, Borgelt, J, Awiszus, B, Popov, T, Elbert, T, Rockstroh, B (2009). Early life stress and psychiatric disorder modulate cortical responses to affective stimuli. Psychophysiology 46, 1234–1243.CrossRefGoogle ScholarPubMed
Williams, LM, Gatt, JM, Schofield, PR, Olivieri, G, Peduto, A, Gordon, E (2009). ‘Negativity bias’ in risk for depression and anxiety: brain-body fear circuitry correlates, 5-HTT-LPR and early life stress. NeuroImage 47, 804–814.CrossRefGoogle ScholarPubMed