Skip to main content Accessibility help
×
Home

Resting-state functional connectivity in adults with childhood emotional maltreatment

  • S. J. A. van der Werff (a1) (a2) (a3), J. N. Pannekoek (a1) (a2), I. M. Veer (a2) (a4) (a5), M.-J. van Tol (a6), A. Aleman (a6), D. J. Veltman (a7), F. G. Zitman (a1), S. A. R. B. Rombouts (a2) (a4) (a5), B. M. Elzinga (a2) (a5) and N. J. A. van der Wee (a1) (a2) (a3)...

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.

Copyright

Corresponding author

*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)

References

Hide All
Beck, AT, Epstein, N, Brown, G, Steer, RA (1988). An inventory for measuring clinical anxiety: psychometric properties. Journal of Consulting and Clinical Psychology 56, 893897.
Bennett, MR (2011). The prefrontal-limbic network in depression: modulation by hypothalamus, basal ganglia and midbrain. Progress in Neurobiology 93, 468487.
Binggeli, NJ, Hart, SN, Brassard, MR (2001). Psychological Maltreatment of Children. The APSAC Study Guides, Vol. 4. Sage: Thousand Oaks, CA.
Birn, RM, Diamond, JB, Smith, MA, Bandettini, PA (2006). Separating respiratory-variation-related fluctuations from neuronal-activity-related fluctuations in fMRI. NeuroImage 31, 15361548.
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, 537541.
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, 47344739.
Bremner, JD (2007 a). Functional neuroimaging in post-traumatic stress disorder. Expert Review of Neurotherapeutics 7, 393405.
Bremner, JD (2007 b). Neuroimaging in posttraumatic stress disorder and other stress-related disorders. Neuroimaging Clinics of North America 17, 523538, ix.
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, 279296.
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, 138.
Cavanna, AE, Trimble, MR (2006). The precuneus: a review of its functional anatomy and behavioural correlates. Brain 129, 564583.
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.
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, 1384813853.
Danese, A, McEwen, BS (2012). Adverse childhood experiences, allostasis, allostatic load, and age-related disease. Physiology and Behavior 106, 2939.
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, 620629.
Egeland, B (2009). Taking stock: childhood emotional maltreatment and developmental psychopathology. Child Abuse and Neglect 33, 2226.
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, 403416.
Finzi, R, Cohen, O, Sapir, Y, Weizman, A (2000). Attachment styles in maltreated children: a comparative study. Child Psychiatry and Human Development 31, 113128.
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, 195200.
Fox, MD, Raichle, ME (2007). Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nature Reviews. Neuroscience 8, 700711.
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, 96739678.
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, 661672.
Gibb, BE (2002). Childhood maltreatment and negative cognitive styles. A quantitative and qualitative review. Clinical Psychology Review 22, 223246.
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, 256263.
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, 6881.
Greicius, M (2008). Resting-state functional connectivity in neuropsychiatric disorders. Current Opinion in Neurology 21, 424430.
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, 253258.
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, 10591067.
Joels, M, Krugers, H, Karst, H (2008). Stress-induced changes in hippocampal function. Progress in Brain Research 167, 315.
Kahnt, T, Grueschow, M, Speck, O, Haynes, JD (2011). Perceptual learning and decision-making in human medial frontal cortex. Neuron 70, 549559.
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, 966977.
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, 133144.
Kjaer, TW, Nowak, M, Lou, HC (2002). Reflective self-awareness and conscious states: PET evidence for a common midline parietofrontal core. NeuroImage 17, 10801086.
Koechlin, E (2011). Frontal pole function: what is specifically human? Trends in Cognitive Sciences 15, 241.
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.
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, 15491558.
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, 68276832.
Margulies, DS, Kelly, AM, Uddin, LQ, Biswal, BB, Castellanos, FX, Milham, MP (2007). Mapping the functional connectivity of anterior cingulate cortex. NeuroImage 37, 579588.
McEwen, BS (2001). Plasticity of the hippocampus: adaptation to chronic stress and allostatic load. Annals of the New York Academy of Sciences 933, 265277.
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, 171191.
Montgomery, SA, Asberg, M (1979). A new depression scale designed to be sensitive to change. British Journal of Psychiatry 134, 382389.
Muhammad, A, Carroll, C, Kolb, B (2012). Stress during development alters dendritic morphology in the nucleus accumbens and prefrontal cortex. Neuroscience 216, 103109.
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, 141151.
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, 500508.
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, 403412.
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, 121140.
Pessoa, L (2008). On the relationship between emotion and cognition. Nature Reviews. Neuroscience 9, 148158.
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, 676682.
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, 434442.
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, 10691077.
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, 614626.
Rush, AJ, Gullion, CM, Basco, MR, Jarrett, RB, Trivedi, MH (1996). The Inventory of Depressive Symptomatology (IDS): psychometric properties. Psychological Medicine 26, 477486.
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, 23492356.
Shin, LM, Liberzon, I (2010). The neurocircuitry of fear, stress, and anxiety disorders. Neuropsychopharmacology 35, 169191.
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), S208S219.
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, 103112.
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, 5274.
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, 9931000.
Tsujimoto, S, Genovesio, A, Wise, SP (2011). Frontal pole cortex: encoding ends at the end of the endbrain. Trends in Cognitive Sciences 15, 169176.
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.
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, 486494.
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.
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, 832838.
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, 649655.
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, 273284.
van Wingen, GA, Geuze, E, Vermetten, E, Fernandez, G (2011). The neural consequences of combat stress: long-term follow-up. Molecular Psychiatry 17, 116118.
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.
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, 15341541.
Vermetten, E, Bremner, JD (2002). Circuits and systems in stress. II. Applications to neurobiology and treatment in posttraumatic stress disorder. Depression and Anxiety 16, 1438.
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, 5968.

Keywords

Type Description Title
WORD
Supplementary materials

van der Werff Supplementary Material
Appendix

 Word (94 KB)
94 KB

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed