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Resting-state functional connectivity in adults with childhood emotional maltreatment

Published online by Cambridge University Press:  20 December 2012

S. J. A. van der Werff ,
J. N. Pannekoek ,
I. M. Veer ,
M.-J. van Tol ,
A. Aleman ,
D. J. Veltman ,
F. G. Zitman ,
S. A. R. B. Rombouts ,
B. M. Elzinga  and
N. J. A. van der Wee
S. J. A. van der Werff*
Affiliation:
Department of Psychiatry, Leiden University Medical Center, The Netherlands Leiden Institute for Brain and Cognition (LIBC), Leiden University, The Netherlands National Initiative Brain and Cognition, The Netherlands
J. N. Pannekoek
Affiliation:
Department of Psychiatry, Leiden University Medical Center, The Netherlands Leiden Institute for Brain and Cognition (LIBC), Leiden University, The Netherlands
I. M. Veer
Affiliation:
Leiden Institute for Brain and Cognition (LIBC), Leiden University, The Netherlands Department of Radiology, Leiden University Medical Center, The Netherlands Institute of Psychology, Leiden University, The Netherlands
M.-J. van Tol
Affiliation:
BCN Neuroimaging Center, University of Groningen, The Netherlands
A. Aleman
Affiliation:
BCN Neuroimaging Center, University of Groningen, The Netherlands
D. J. Veltman
Affiliation:
Department of Psychiatry, VU Medical Center, Amsterdam, The Netherlands
F. G. Zitman
Affiliation:
Department of Psychiatry, Leiden University Medical Center, The Netherlands
S. A. R. B. Rombouts
Affiliation:
Leiden Institute for Brain and Cognition (LIBC), Leiden University, The Netherlands Department of Radiology, Leiden University Medical Center, The Netherlands Institute of Psychology, Leiden University, The Netherlands
B. M. Elzinga
Affiliation:
Leiden Institute for Brain and Cognition (LIBC), Leiden University, The Netherlands Institute of Psychology, Leiden University, The Netherlands
N. J. A. van der Wee
Affiliation:
Department of Psychiatry, Leiden University Medical Center, The Netherlands Leiden Institute for Brain and Cognition (LIBC), Leiden University, The Netherlands National Initiative Brain and Cognition, The Netherlands
*
*Address for correspondence: Mr S. J. A. van der Werff, Leiden University Medical Center, Department of Psychiatry, B1-P, PO Box 9600, 2300 RC Leiden, The Netherlands. (Email: S.J.A.van_der_Werff@lumc.nl)
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Abstract

Background

Childhood emotional maltreatment (CEM) has been associated with disturbances in emotional and behavioral functioning, and with changes in regional brain morphology. However, whether CEM has any effect on the intrinsic organization of the brain is not known. In this study, we investigated the effects of CEM on resting-state functional connectivity (RSFC) using seeds in the limbic network, the default-mode network (DMN) and the salience network, and the left dorsomedial prefrontal cortex (dmPFC).

Method

Using 3-T magnetic resonance imaging (MRI), resting-state functional MRI (RS-fMRI) scans were obtained. We defined seeds in the bilateral amygdala, the dorsal anterior cingulate cortex (dACC), the posterior cingulate cortex (PCC) and the left dmPFC, and used these to examine whether individuals reporting CEM (n=44) differed from individuals reporting no CEM (n=44) in RSFC with other brain regions. The two groups were matched for age, gender, handedness and the presence of psychopathology.

Results

CEM was associated with decreased RSFC between the right amygdala and the bilateral precuneus and a cluster extending from the left insula to the hippocampus and putamen. In addition, CEM was associated with decreased RSFC between the dACC and the precuneus and also frontal regions of the brain.

Conclusions

We found that CEM has a profound effect on RSFC in the limbic network and the salience network. Regions that show aberrant connectivity are related to episodic memory encoding, retrieval and self-processing operations.

Keywords

Amygdalachildhood emotional maltreatmentdefault mode networkprecuneusresting-state functional connectivitysalience network
Type
Original Articles
Information
Psychological Medicine , Volume 43 , Issue 9 , September 2013 , pp. 1825 - 1836
Copyright
Copyright © Cambridge University Press 2012 

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References

Beck, AT, Epstein, N, Brown, G, Steer, RA (1988). An inventory for measuring clinical anxiety: psychometric properties. Journal of Consulting and Clinical Psychology 56, 893–897.Google Scholar
Bennett, MR (2011). The prefrontal-limbic network in depression: modulation by hypothalamus, basal ganglia and midbrain. Progress in Neurobiology 93, 468–487.CrossRefGoogle ScholarPubMed
Binggeli, NJ, Hart, SN, Brassard, MR (2001). Psychological Maltreatment of Children. The APSAC Study Guides, Vol. 4. Sage: Thousand Oaks, CA.Google Scholar
Birn, RM, Diamond, JB, Smith, MA, Bandettini, PA (2006). Separating respiratory-variation-related fluctuations from neuronal-activity-related fluctuations in fMRI. NeuroImage 31, 1536–1548.CrossRefGoogle ScholarPubMed
Biswal, B, Yetkin, FZ, Haughton, VM, Hyde, JS (1995). Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magnetic Resonance in Medicine 34, 537–541.CrossRefGoogle ScholarPubMed
Biswal, BB, Mennes, M, Zuo, XN, Gohel, S, Kelly, C, Smith, SM, Beckmann, CF, Adelstein, JS, Buckner, RL, Colcombe, S, Dogonowski, AM, Ernst, M, Fair, D, Hampson, M, Hoptman, MJ, Hyde, JS, Kiviniemi, VJ, Kotter, R, Li, SJ, Lin, CP, Lowe, MJ, Mackay, C, Madden, DJ, Madsen, KH, Margulies, DS, Mayberg, HS, McMahon, K, Monk, CS, Mostofsky, SH, Nagel, BJ, Pekar, JJ, Peltier, SJ, Petersen, SE, Riedl, V, Rombouts, SA, Rypma, B, Schlaggar, BL, Schmidt, S, Seidler, RD, Siegle, GJ, Sorg, C, Teng, GJ, Veijola, J, Villringer, A, Walter, M, Wang, L, Weng, XC, Whitfield-Gabrieli, S, Williamson, P, Windischberger, C, Zang, YF, Zhang, HY, Castellanos, FX, Milham, MP (2010). Toward discovery science of human brain function. Proceedings of the National Academy of Sciences USA 107, 4734–4739.CrossRefGoogle ScholarPubMed
Bremner, JD (2007 a). Functional neuroimaging in post-traumatic stress disorder. Expert Review of Neurotherapeutics 7, 393–405.CrossRefGoogle ScholarPubMed
Bremner, JD (2007 b). Neuroimaging in posttraumatic stress disorder and other stress-related disorders. Neuroimaging Clinics of North America 17, 523–538, ix.CrossRefGoogle ScholarPubMed
Broyd, SJ, Demanuele, C, Debener, S, Helps, SK, James, CJ, Sonuga-Barke, EJ (2009). Default-mode brain dysfunction in mental disorders: a systematic review. Neuroscience and Biobehavioral Reviews 33, 279–296.CrossRefGoogle ScholarPubMed
Buckner, RL, Andrews-Hanna, JR, Schacter, DL (2008). The brain's default network: anatomy, function, and relevance to disease. Annals of the New York Academy of Sciences 1124, 1–38.CrossRefGoogle ScholarPubMed
Cavanna, AE, Trimble, MR (2006). The precuneus: a review of its functional anatomy and behavioural correlates. Brain 129, 564–583.CrossRefGoogle ScholarPubMed
Costa, PT Jr., McCrea, RR (1992). Manual for the Revised NEO Personality Inventory (NEO-PIR) and NEO Five-Factor Inventory (NEO-FFI). Psychological Assessment Resources: Odessa.Google Scholar
Damoiseaux, JS, Rombouts, SA, Barkhof, F, Scheltens, P, Stam, CJ, Smith, SM, Beckmann, CF (2006). Consistent resting-state networks across healthy subjects. Proceedings of the National Academy of Sciences USA 103, 13848–13853.CrossRefGoogle ScholarPubMed
Danese, A, McEwen, BS (2012). Adverse childhood experiences, allostasis, allostatic load, and age-related disease. Physiology and Behavior 106, 29–39.CrossRefGoogle ScholarPubMed
De Graaf, R, Bijl, RV, Smit, F, Vollebergh, WA, Spijker, J (2002). Risk factors for 12-month comorbidity of mood, anxiety, and substance use disorders: findings from the Netherlands Mental Health Survey and Incidence Study. American Journal of Psychiatry 159, 620–629.CrossRefGoogle ScholarPubMed
Egeland, B (2009). Taking stock: childhood emotional maltreatment and developmental psychopathology. Child Abuse and Neglect 33, 22–26.CrossRefGoogle ScholarPubMed
Fabricius, K, Wortwein, G, Pakkenberg, B (2008). The impact of maternal separation on adult mouse behaviour and on the total neuron number in the mouse hippocampus. Brain Structure and Function 212, 403–416.CrossRefGoogle ScholarPubMed
Finzi, R, Cohen, O, Sapir, Y, Weizman, A (2000). Attachment styles in maltreated children: a comparative study. Child Psychiatry and Human Development 31, 113–128.CrossRefGoogle ScholarPubMed
Fletcher, PC, Frith, CD, Baker, SC, Shallice, T, Frackowiak, RS, Dolan, RJ (1995). The mind's eye – precuneus activation in memory-related imagery. NeuroImage 2, 195–200.CrossRefGoogle ScholarPubMed
Fox, MD, Raichle, ME (2007). Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nature Reviews. Neuroscience 8, 700–711.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, 9673–9678.CrossRefGoogle ScholarPubMed
Frings, L, Wagner, K, Quiske, A, Schwarzwald, R, Spreer, J, Halsband, U, Schulze-Bonhage, A (2006). Precuneus is involved in allocentric spatial location encoding and recognition. Experimental Brain Research 173, 661–672.CrossRefGoogle ScholarPubMed
Gibb, BE (2002). Childhood maltreatment and negative cognitive styles. A quantitative and qualitative review. Clinical Psychology Review 22, 223–246.CrossRefGoogle Scholar
Gibb, BE, Chelminski, I, Zimmerman, M (2007). Childhood emotional, physical, and sexual abuse, and diagnoses of depressive and anxiety disorders in adult psychiatric outpatients. Depression and Anxiety 24, 256–263.CrossRefGoogle ScholarPubMed
Gilbert, R, Widom, CS, Browne, K, Fergusson, D, Webb, E, Janson, S (2009). Burden and consequences of child maltreatment in high-income countries. Lancet 373, 68–81.CrossRefGoogle ScholarPubMed
Greicius, M (2008). Resting-state functional connectivity in neuropsychiatric disorders. Current Opinion in Neurology 21, 424–430.CrossRefGoogle ScholarPubMed
Greicius, MD, Krasnow, B, Reiss, AL, Menon, V (2003). Functional connectivity in the resting brain: a network analysis of the default mode hypothesis. Proceedings of the National Academy of Sciences USA 100, 253–258.CrossRefGoogle Scholar
Guyer, AE, Kaufman, J, Hodgdon, HB, Masten, CL, Jazbec, S, Pine, DS, Ernst, M (2006). Behavioral alterations in reward system function: the role of childhood maltreatment and psychopathology. Journal of the American Academy of Child and Adolescent Psychiatry 45, 1059–1067.CrossRefGoogle ScholarPubMed
Joels, M, Krugers, H, Karst, H (2008). Stress-induced changes in hippocampal function. Progress in Brain Research 167, 3–15.CrossRefGoogle ScholarPubMed
Kahnt, T, Grueschow, M, Speck, O, Haynes, JD (2011). Perceptual learning and decision-making in human medial frontal cortex. Neuron 70, 549–559.CrossRefGoogle ScholarPubMed
Kim, H (2012). A dual-subsystem model of the brain's default network: self-referential processing, memory retrieval processes, and autobiographical memory retrieval. NeuroImage 61, 966–977.CrossRefGoogle ScholarPubMed
Kircher, TT, Senior, C, Phillips, ML, Benson, PJ, Bullmore, ET, Brammer, M, Simmons, A, Williams, SC, Bartels, M, David, AS (2000). Towards a functional neuroanatomy of self processing: effects of faces and words. Brain Research. Cognitive Brain Research 10, 133–144.CrossRefGoogle ScholarPubMed
Kjaer, TW, Nowak, M, Lou, HC (2002). Reflective self-awareness and conscious states: PET evidence for a common midline parietofrontal core. NeuroImage 17, 1080–1086.CrossRefGoogle ScholarPubMed
Koechlin, E (2011). Frontal pole function: what is specifically human? Trends in Cognitive Sciences 15, 241.CrossRefGoogle ScholarPubMed
Leeb, RT, Paulozzi, L, Melanson, C, Simon, TR, Arias, I (2008). Uniform Definitions for Public Health and Recommended Data Elements. Centers for Disease Control and Prevention: Atlanta, GA.Google Scholar
Liao, W, Chen, H, Feng, Y, Mantini, D, Gentili, C, Pan, Z, Ding, J, Duan, X, Qiu, C, Lui, S, Gong, Q, Zhang, W (2010). Selective aberrant functional connectivity of resting state networks in social anxiety disorder. NeuroImage 52, 1549–1558.CrossRefGoogle ScholarPubMed
Lou, HC, Luber, B, Crupain, M, Keenan, JP, Nowak, M, Kjaer, TW, Sackeim, HA, Lisanby, SH (2004). Parietal cortex and representation of the mental self. Proceedings of the National Academy of Sciences USA 101, 6827–6832.CrossRefGoogle ScholarPubMed
Margulies, DS, Kelly, AM, Uddin, LQ, Biswal, BB, Castellanos, FX, Milham, MP (2007). Mapping the functional connectivity of anterior cingulate cortex. NeuroImage 37, 579–588.CrossRefGoogle ScholarPubMed
McEwen, BS (2001). Plasticity of the hippocampus: adaptation to chronic stress and allostatic load. Annals of the New York Academy of Sciences 933, 265–277.CrossRefGoogle ScholarPubMed
McLewin, LA, Muller, RT (2006). Attachment and social support in the prediction of psychopathology among young adults with and without a history of physical maltreatment. Child Abuse and Neglect 30, 171–191.CrossRefGoogle ScholarPubMed
Montgomery, SA, Asberg, M (1979). A new depression scale designed to be sensitive to change. British Journal of Psychiatry 134, 382–389.CrossRefGoogle ScholarPubMed
Muhammad, A, Carroll, C, Kolb, B (2012). Stress during development alters dendritic morphology in the nucleus accumbens and prefrontal cortex. Neuroscience 216, 103–109.CrossRefGoogle ScholarPubMed
Nanni, V, Uher, R, Danese, A (2012). Childhood maltreatment predicts unfavorable course of illness and treatment outcome in depression: a meta-analysis. American Journal of Psychiatry 169, 141–151.CrossRefGoogle ScholarPubMed
Oakes, TR, Fox, AS, Johnstone, T, Chung, MK, Kalin, N, Davidson, RJ (2007). Integrating VBM into the General Linear Model with voxelwise anatomical covariates. NeuroImage 34, 500–508.CrossRefGoogle ScholarPubMed
Oei, NY, Veer, IM, Wolf, OT, Spinhoven, P, Rombouts, SA, Elzinga, BM (2012). Stress shifts brain activation towards ventral ‘affective’ areas during emotional distraction. Social Cognitive and Affective Neuroscience 7, 403–412.CrossRefGoogle ScholarPubMed
Penninx, BW, Beekman, AT, Smit, JH, Zitman, FG, Nolen, WA, Spinhoven, P, Cuijpers, P, De Jong, PJ, Van Marwijk, HW, Assendelft, WJ, Van Der Meer, K, Verhaak, P, Wensing, M, De Graaf, R, Hoogendijk, WJ, Ormel, J, Van Dyck, R; NESDA Research Consortium (2008). The Netherlands Study of Depression and Anxiety (NESDA): rationale, objectives and methods. International Journal of Methods in Psychiatric Research 17, 121–140.CrossRefGoogle ScholarPubMed
Pessoa, L (2008). On the relationship between emotion and cognition. Nature Reviews. Neuroscience 9, 148–158.CrossRefGoogle ScholarPubMed
Raichle, ME, MacLeod, AM, Snyder, AZ, Powers, WJ, Gusnard, DA, Shulman, GL (2001). A default mode of brain function. Proceedings of the National Academy of Sciences USA 98, 676–682.CrossRefGoogle ScholarPubMed
Rellini, AH, Vujanovic, AA, Gilbert, M, Zvolensky, MJ (2012). Childhood maltreatment and difficulties in emotion regulation: associations with sexual and relationship satisfaction among young adult women. Journal of Sex Research 49, 434–442.CrossRefGoogle ScholarPubMed
Robins, LN, Wing, J, Wittchen, HU, Helzer, JE, Babor, TF, Burke, J, Farmer, A, Jablenski, A, Pickens, R, Regier, DA (1988). The Composite International Diagnostic Interview. An epidemiologic instrument suitable for use in conjunction with different diagnostic systems and in different cultures. Archives of General Psychiatry 45, 1069–1077.CrossRefGoogle ScholarPubMed
Roy, AK, Shehzad, Z, Margulies, DS, Kelly, AM, Uddin, LQ, Gotimer, K, Biswal, BB, Castellanos, FX, Milham, MP (2009). Functional connectivity of the human amygdala using resting state fMRI. NeuroImage 45, 614–626.CrossRefGoogle ScholarPubMed
Rush, AJ, Gullion, CM, Basco, MR, Jarrett, RB, Trivedi, MH (1996). The Inventory of Depressive Symptomatology (IDS): psychometric properties. Psychological Medicine 26, 477–486.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Shin, LM, Liberzon, I (2010). The neurocircuitry of fear, stress, and anxiety disorders. Neuropsychopharmacology 35, 169–191.CrossRefGoogle ScholarPubMed
Smith, SM, Jenkinson, M, Woolrich, MW, Beckmann, CF, Behrens, TE, Johansen-Berg, H, Bannister, PR, De Luca, M, Drobnjak, I, Flitney, DE, Niazy, RK, Saunders, J, Vickers, J, Zhang, Y, De Stefano, N, Brady, JM, Matthews, PM (2004). Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage 23 (Suppl. 1), S208–S219.CrossRefGoogle ScholarPubMed
Spinhoven, P, Elzinga, BM, Hovens, JG, Roelofs, K, Zitman, FG, van Oppen, P, Penninx, BW (2010). The specificity of childhood adversities and negative life events across the life span to anxiety and depressive disorders. Journal of Affective Disorders 126, 103–112.CrossRefGoogle ScholarPubMed
Taussig, HN, Culhane, SE (2010). Emotional maltreatment and psychosocial functioning in preadolescent youth placed in out-of-home care. Journal of Aggression, Maltreatment and Trauma 19, 52–74.CrossRefGoogle ScholarPubMed
Teicher, MH, Samson, JA, Polcari, A, McGreenery, CE (2006). Sticks, stones, and hurtful words: relative effects of various forms of childhood maltreatment. American Journal of Psychiatry 163, 993–1000.CrossRefGoogle ScholarPubMed
Tsujimoto, S, Genovesio, A, Wise, SP (2011). Frontal pole cortex: encoding ends at the end of the endbrain. Trends in Cognitive Sciences 15, 169–176.CrossRefGoogle ScholarPubMed
U.S. Department of Health and Human Services (2009). Child Maltreatment 2009. Children's Bureau. Administration for Children and Families. U.S. Government Printing Office: Washington, DC.Google Scholar
van Harmelen, AL, de Jong, PJ, Glashouwer, KA, Spinhoven, P, Penninx, BW, Elzinga, BM (2010 a). Child abuse and negative explicit and automatic self-associations: the cognitive scars of emotional maltreatment. Behaviour Research and Therapy 48, 486–494.CrossRefGoogle ScholarPubMed
van Harmelen, AL, van Tol, MJ, Demenescu, LR, van der Wee, NJ, Veltman, DJ, Aleman, A, van Buchem, MA, Spinhoven, P, Penninx, BW, Elzinga, BM (2012). Enhanced amygdala reactivity to emotional faces in adults reporting childhood emotional maltreatment. Social Cognitive and Affective Neuroscience. Published online: 7 June 2012. doi:10.1093/scan/nss007.Google ScholarPubMed
van Harmelen, AL, van Tol, MJ, van der Wee, NJ, Veltman, DJ, Aleman, A, Spinhoven, P, van Buchem, MA, Zitman, FG, Penninx, BW, Elzinga, BM (2010 b). Reduced medial prefrontal cortex volume in adults reporting childhood emotional maltreatment. Biological Psychiatry 68, 832–838.CrossRefGoogle ScholarPubMed
van Marle, HJ, Hermans, EJ, Qin, S, Fernandez, G (2009). From specificity to sensitivity: how acute stress affects amygdala processing of biologically salient stimuli. Biological Psychiatry 66, 649–655.CrossRefGoogle ScholarPubMed
van Tol, MJ, van der Wee, NJ, Demenescu, LR, Nielen, MM, Aleman, A, Renken, R, van Buchem, MA, Zitman, FG, Veltman, DJ (2011). Functional MRI correlates of visuospatial planning in out-patient depression and anxiety. Acta Psychiatrica Scandinavica 124, 273–284.CrossRefGoogle ScholarPubMed
van Wingen, GA, Geuze, E, Vermetten, E, Fernandez, G (2011). The neural consequences of combat stress: long-term follow-up. Molecular Psychiatry 17, 116–118.CrossRefGoogle ScholarPubMed
Veer, IM, Beckmann, CF, van Tol, MJ, Ferrarini, L, Milles, J, Veltman, DJ, Aleman, A, van Buchem, MA, van der Wee, NJ, Rombouts, SA (2010). Whole brain resting-state analysis reveals decreased functional connectivity in major depression. Frontiers in Systems Neuroscience 4, 41.CrossRefGoogle ScholarPubMed
Veer, IM, Oei, NY, Spinhoven, P, van Buchem, MA, Elzinga, BM, Rombouts, SA (2011). Beyond acute social stress: increased functional connectivity between amygdala and cortical midline structures. NeuroImage 57, 1534–1541.CrossRefGoogle ScholarPubMed
Vermetten, E, Bremner, JD (2002). Circuits and systems in stress. II. Applications to neurobiology and treatment in posttraumatic stress disorder. Depression and Anxiety 16, 14–38.CrossRefGoogle ScholarPubMed
Wright, MO, Crawford, E, Del Castillo, D (2009). Childhood emotional maltreatment and later psychological distress among college students: the mediating role of maladaptive schemas. Child Abuse and Neglect 33, 59–68.CrossRefGoogle ScholarPubMed
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