Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-28T19:56:49.013Z Has data issue: false hasContentIssue false
  • English
  • Français

Childhood stress, grown-up brain networks: corticolimbic correlates of threat-related early life stress and adult stress response

Published online by Cambridge University Press:  25 September 2017

R. H. Kaiser ,
R. Clegg ,
F. Goer ,
P. Pechtel ,
M. Beltzer ,
G. Vitaliano ,
D. P. Olson ,
M. H. Teicher  and
D. A. Pizzagalli
R. H. Kaiser
Affiliation:
Center for Depression, Anxiety and Stress Research, McLean Hospital, Belmont, MA, USA Department of Psychiatry, Harvard Medical School, Boston, MA, USA Department of Psychology, University of California Los Angeles, Los Angeles, CA, USA
R. Clegg
Affiliation:
Center for Depression, Anxiety and Stress Research, McLean Hospital, Belmont, MA, USA
F. Goer
Affiliation:
Center for Depression, Anxiety and Stress Research, McLean Hospital, Belmont, MA, USA
P. Pechtel
Affiliation:
Center for Depression, Anxiety and Stress Research, McLean Hospital, Belmont, MA, USA Department of Psychiatry, Harvard Medical School, Boston, MA, USA
M. Beltzer
Affiliation:
Center for Depression, Anxiety and Stress Research, McLean Hospital, Belmont, MA, USA
G. Vitaliano
Affiliation:
Department of Psychiatry, Harvard Medical School, Boston, MA, USA McLean Imaging Center, McLean Hospital, Belmont, MA, USA
D. P. Olson
Affiliation:
Department of Psychiatry, Harvard Medical School, Boston, MA, USA McLean Imaging Center, McLean Hospital, Belmont, MA, USA
M. H. Teicher
Affiliation:
Department of Psychiatry, Harvard Medical School, Boston, MA, USA
D. A. Pizzagalli*
Affiliation:
Center for Depression, Anxiety and Stress Research, McLean Hospital, Belmont, MA, USA Department of Psychiatry, Harvard Medical School, Boston, MA, USA McLean Imaging Center, McLean Hospital, Belmont, MA, USA
*
Author for correspondence: D. A. Pizzagalli, E-mail: dap@mclean.harvard.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Exposure to threat-related early life stress (ELS) has been related to vulnerability for stress-related disorders in adulthood, putatively via disrupted corticolimbic circuits involved in stress response and regulation. However, previous research on ELS has not examined both the intrinsic strength and flexibility of corticolimbic circuits, which may be particularly important for adaptive stress responding, or associations between these dimensions of corticolimbic dysfunction and acute stress response in adulthood.

Methods

Seventy unmedicated women varying in history of threat-related ELS completed a functional magnetic resonance imaging scan to evaluate voxelwise static (overall) and dynamic (variability over a series of sliding windows) resting-state functional connectivity (RSFC) of bilateral amygdala. In a separate session and subset of participants (n = 42), measures of salivary cortisol and affect were collected during a social-evaluative stress challenge.

Results

Higher severity of threat-related ELS was related to more strongly negative static RSFC between amygdala and left dorsolateral prefrontal cortex (DLPFC), and elevated dynamic RSFC between amygdala and rostral anterior cingulate cortex (rACC). Static amygdala-DLPFC antagonism mediated the relationship between higher severity of threat-related ELS and blunted cortisol response to stress, but increased dynamic amygdala-rACC connectivity weakened this mediated effect and was related to more positive post-stress mood.

Conclusions

Threat-related ELS was associated with RSFC within lateral corticolimbic circuits, which in turn was related to blunted physiological response to acute stress. Notably, increased flexibility between the amygdala and rACC compensated for this static disruption, suggesting that more dynamic medial corticolimbic circuits might be key to restoring healthy stress response.

Keywords

Childhood traumacortisolearly life stressresting-state functional connectivity
Type
Original Articles
Information
Psychological Medicine , Volume 48 , Issue 7 , May 2018 , pp. 1157 - 1166
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adams, T and Rosenkranz, JA (2016) Social isolation during postweaning development causes hypoactivity of neurons in the medial nucleus of the male Rat amygdala. Neuropsychopharmacology 41, 1929–1940.CrossRefGoogle ScholarPubMed
Allen, EA, Damaraju, E, Plis, SM, Erhardt, EB, Eichele, T and Calhoun, VD (2014) Tracking whole-brain connectivity dynamics in the resting state. Cerebral Cortex 24, 663–676.CrossRefGoogle ScholarPubMed
Amat, J, Baratta, MV, Paul, E, Bland, ST, Watkins, LR and Maier, SF (2005) Medial prefrontal cortex determines how stressor controllability affects behavior and dorsal raphe nucleus. Nature Neuroscience 8, 365–371.Google Scholar
Andersen, SL (2015) Exposure to early adversity: points of cross-species translation that can lead to improved understanding of depression. Development and Psychopathology 27, 477–491.CrossRefGoogle ScholarPubMed
Andersen, SL, Tomada, A, Vincow, ES, Valente, E, Polcari, A and Teicher, MH (2008) Preliminary evidence for sensitive periods in the effect of childhood sexual abuse on regional brain development. Journal of Neuropsychiatry and Clinical Neurosciences 20, 292–301.Google Scholar
Banich, MT (2009) Executive function: the search for an integrated account. Current Directions in Psychological Science 18, 89–94.Google Scholar
Banich, MT, Mackiewicz, KL, Depue, BE, Whitmer, AJ, Miller, GA and Heller, W (2009) Cognitive control mechanisms, emotion and memory: a neural perspective with implications for psychopathology. Neuroscience and Biobehavioral Reviews 33, 613–630.Google Scholar
Banks, SJ, Eddy, KT, Angstadt, M, Nathan, PJ and Phan, KL (2007) Amygdala - frontal connectivity during emotion regulation. Social Cognitive and Affective Neuroscience 2, 303–312.Google Scholar
Banny, AM, Cicchetti, D, Rogosch, FA, Oshri, A and Crick, NR (2013) Vulnerability to depression: a moderated mediation model of the roles of child maltreatment, peer victimization, and serotonin transporter linked polymorphic region genetic variation among children from low socioeconomic status backgrounds. Development and Psychopathology 25, 599–614.Google Scholar
Beck, AT, Steer, RA, Ball, R and Ranieri, WF (1996) Comparison of beck depression inventories-IA and -II in psychiatric outpatients. Journal of Personality Assessment 67, 588–597.Google Scholar
Birn, RM, Patriat, R, Phillips, ML, Germain, A and Herringa, RJ (2014) Childhood maltreatment and combat posttraumatic stress differentially predict fear-related fronto-subcortical connectivity. Depression and Anxiety 31, 880–892.CrossRefGoogle ScholarPubMed
Biswal, B, Yetkin, FZ, Haughton, VM and Hyde, JS (1995) Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magnetic Resonance in Medicine 34, 537–541.Google Scholar
Brown, VM, Labar, KS, Haswell, CC, Gold, AL, McCarthy, G, Morey, RA et al. (2014) Altered resting-state functional connectivity of basolateral and centromedial amygdala complexes in posttraumatic stress disorder. Neuropsychopharmacology 39, 351–359.Google Scholar
Burghy, CA, Stodola, DE, Ruttle, PL, Molloy, EK, Armstrong, JM, Oler, JA et al. (2012) Developmental pathways to amygdala-prefrontal function and internalizing symptoms in adolescence. Nature Neuroscience 15, 1736.Google Scholar
Bush, G, Luu, P and Posner, MI (2000) Cognitive and emotional influences in anterior cingulate cortex. Trends in Cognitive Sciences 4, 215–222.Google Scholar
Calhoun, VD, Miller, R, Pearlson, G and Adali, T (2014) The chronnectome: time-varying connectivity networks as the next frontier in fMRI data discovery. Neuron 84, 262–274.Google Scholar
Carpenter, LL, Tyrka, AR, Ross, NS, Khoury, L, Anderson, GM and Price, LH (2009) Effect of childhood emotional abuse and Age on cortisol responsivity in adulthood. Biological Psychiatry 66, 69–75.Google Scholar
Danese, A and McEwen, BS (2012) Adverse childhood experiences, allostasis, allostatic load, and age-related disease. Physiology & Behavior 106, 29–39.Google Scholar
Davies, DA, Molder, JJ, Greba, Q and Howland, JG (2013) Inactivation of medial prefrontal cortex or acute stress impairs odor span in rats. Learning & Memory 20, 665–669.Google Scholar
Diekhof, EK, Geier, K, Falkai, P and Gruber, O (2011) Fear is only as deep as the mind allows: a coordinate-based meta-analysis of neuroimaging studies on the regulation of negative affect. NeuroImage 58, 275–285.CrossRefGoogle ScholarPubMed
Doom, JR, Cicchetti, D, Rogosch, FA and Dackis, MN (2013) Child maltreatment and gender interactions as predictors of differential neuroendocrine profiles. Psychoneuroendocrinology 38, 1442–1454.Google Scholar
Duff, EP, Cunnington, R and Egan, GF (2007) REX: response exploration for neuroimaging datasets. Neuroinformatics 5, 223–234.Google Scholar
Eklund, A, Nichols, TE and Knutsson, H (2016) Cluster failure: why fMRI inferences for spatial extent have inflated false-positive rates. Proceedings of the National Academy of Sciences of the United States of America 113, 7900–7905.Google Scholar
Etkin, A, Buchel, C and Gross, JJ (2015) The neural bases of emotion regulation. Nature Reviews Neuroscience 16, 693.Google Scholar
First, M, Spitzer, R, Gibbon, M and Williams, J (2002) Structured Clinical Interview for DSM-IV-TR Axis I Disorders, Research Version, Non-Patient Edition. (SCID-I/NP). New York: Biometrics Research, New York State Psychiatric Institute.Google Scholar
Folstein, MF and Luria, R (1973) Reliability, validity, and clinical application of visual analog mood scale. Psychological Medicine 3, 479–486.Google Scholar
Gabard-Durnam, LJ, Flannery, J, Goff, B, Gee, DG, Humphreys, KL, Telzer, E et al. (2014) The development of human amygdala functional connectivity at rest from 4 to 23 years: a cross-sectional study. NeuroImage 95, 193–207.Google Scholar
Grant, MM, Wood, K, Sreenivasan, K, Wheelock, M, White, D, Thomas, J et al. (2015) Influence of early life stress on intra- and extra-amygdaloid causal connectivity. Neuropsychopharmacology 40, 1782–1793.Google Scholar
Green, JG, McLaughlin, KA, Berglund, PA, Gruber, MJ, Sampson, NA, Zaslavsky, AM et al. (2010) Childhood adversities and adult psychiatric disorders in the national comorbidity survey replication I associations with first onset of DSM-IV disorders. Archives of General Psychiatry 67, 113–123.CrossRefGoogle ScholarPubMed
Hanson, JL, Knodt, AR, Brigidi, BD and Hariri, AR (2015) Lower structural integrity of the uncinate fasciculus is associated with a history of child maltreatment and future psychological vulnerability to stress. Development and Psychopathology 27, 1611–1619.Google Scholar
Heim, C and Nemeroff, CB (2001) The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies. Biological Psychiatry 49, 1023–1039.CrossRefGoogle ScholarPubMed
Herman, JL, Perry, JC and Vanderkolk, BA (1989) Childhood trauma in borderline personality-disorder. American Journal of Psychiatry 146, 490–495.Google Scholar
Herringa, RJ, Birn, RM, Ruttle, PL, Burghy, CA, Stodola, DE, Davidson, RJ et al. (2013) Childhood maltreatment is associated with altered fear circuitry and increased internalizing symptoms by late adolescence. Proceedings of the National Academy of Sciences of the United States of America 110, 19119–19124.CrossRefGoogle ScholarPubMed
Hutchison, RM and Morton, JB (2015) Tracking the brain's functional coupling dynamics over development. Journal of Neuroscience 35, 6849–6859.Google Scholar
Hutchison, RM, Womelsdorf, T, Allen, EA, Bandettini, PA, Calhoun, VD, Corbetta, M et al. (2013a) Dynamic functional connectivity: promise, issues, and interpretations. NeuroImage 80, 360–378.Google Scholar
Hutchison, RM, Womelsdorf, T, Gati, JS, Everling, S and Menon, RS (2013b) Resting-state networks show dynamic functional connectivity in awake humans and anesthetized macaques. Human Brain Mapping 34, 2154–2177.Google Scholar
Jedd, K, Hunt, RH, Cicchetti, D, Hunt, E, Cowell, RA, Rogosch, FA et al. (2015) Long-term consequences of childhood maltreatment: altered amygdala functional connectivity. Development and Psychopathology 27, 1577–1589.Google Scholar
Kaiser, RH, Andrews-Hanna, JR, Wager, TD and Pizzagalli, DA (2015) Large-scale network dysfunction in major depressive disorder: a meta-analysis of resting-state functional connectivity. JAMA Psychiatry 72, 603–611.Google Scholar
Kaiser, RH, Whitfield-Gabrieli, S, Dillon, DG, Goer, F, Beltzer, M, Minkel, J et al. (2016) Dynamic resting-state functional connectivity in major depression. Neuropsychopharmacology 41, 1822–1830.CrossRefGoogle ScholarPubMed
Khan, A, McCormack, HC, Bolger, EA, McGreenery, CE, Vitaliano, G, Polcari, A et al. (2015) Childhood maltreatment, depression, and suicidal ideation: critical importance of parental and peer emotional abuse during developmental sensitive periods in males and females. Frontiers in Psychiatry 6, 30.CrossRefGoogle ScholarPubMed
Laumann, TO, Snyder, AZ, Mitra, AN, Gordon, EM, Gratton, C, Adeyemo, B et al. (2016) On the stability of BOLD fMRI correlations. Cerebral Cortex [Epub ahead of print].Google Scholar
LeDoux, JE (2000) Emotion circuits in the brain. Annual Review of Neuroscience 23, 155–184.Google Scholar
Leonardi, N and Van De Ville, D (2015) On spurious and real fluctuations of dynamic functional connectivity during rest. NeuroImage 104, 430–436.CrossRefGoogle ScholarPubMed
MacKinnon, DP, Lockwood, CM and Williams, J (2004) Confidence limits for the indirect effect: distribution of the product and resampling methods. Multivariate Behavioral Research 39, 99–128.CrossRefGoogle ScholarPubMed
McEwen, BS (2007) Physiology and neurobiology of stress and adaptation: central role of the brain. Physiological Reviews 87, 873–904.Google Scholar
McLaughlin, KA, Green, JG, Gruber, MJ, Sampson, NA, Zaslavsky, AM and Kessler, RC (2010) Childhood adversities and adult psychopathology in the national comorbidity survey replication (NCS-R) III: associations with functional impairment related to DSM-IV disorders. Psychological Medicine 40, 847–859.Google Scholar
Moriceau, S, Raineki, C, Holman, JD, Holman, JG and Sullivan, RM (2009) Enduring neurobehavioral effects of early life trauma mediated through learning and corticosterone suppression. Frontiers in Behavioral Neuroscience 3, 13.Google Scholar
Nomi, JS, Bolt, TS, Ezie, CC, Uddin, LQ and Heller, AS (2017) Moment-to-moment BOLD signal variability reflects regional changes in neural flexibility across the lifespan. The Journal of Neuroscience 37, 10.Google Scholar
Oomen, CA, Soeters, H, Audureau, N, Vermunt, L, van Hasselt, FN, Manders, EMM et al. (2010) Severe early life stress hampers spatial learning and neurogenesis, but improves hippocampal synaptic plasticity and emotional learning under high-stress conditions in adulthood. Journal of Neuroscience 30, 6635–6645.Google Scholar
Paquola, C, Bennett, MR and Lagopoulos, J (2016) Understanding heterogeneity in grey matter research of adults with childhood maltreatment-A meta-analysis and review. Neuroscience and Biobehavioral Reviews 69, 299–312.Google Scholar
Pechtel, P and Pizzagalli, DA (2011) Effects of early life stress on cognitive and affective function: an integrated review of human literature. Psychopharmacology 214, 55–70.Google Scholar
Petersen, SE and Posner, MI (2012) The attention system of the human brain: 20 years after. In Hyman, S. E. (ed.) Annual Review of Neuroscience, vol. 35. Palo Alto: Annual Reviews. pp. 73–89Google Scholar
Pezawas, L, Meyer-Lindenberg, A, Drabant, EM, Verchinski, BA, Munoz, KE, Kolachana, BS et al. (2005) 5-HTTLPR polymorphism impacts human cingulate-amygdala interactions: a genetic susceptibility mechanism for depression. Nature Neuroscience 8, 828–834.CrossRefGoogle ScholarPubMed
Power, JD, Schlaggar, BL and Petersen, SE (2015) Recent progress and outstanding issues in motion correction in resting state fMRI. NeuroImage 105, 536–551.Google Scholar
Pruessner, JC, Kirschbaum, C, Meinlschmid, G and Hellhammer, DH (2003) Two formulas for computation of the area under the curve represent measures of total hormone concentration versus time-dependent change. Psychoneuroendocrinology 28, 916–931.CrossRefGoogle ScholarPubMed
Roy, AK, Shehzad, Z, Margulies, DS, Kelly, AMC, Uddin, LQ, Gotimer, K et al. (2009) Functional connectivity of the human amygdala using resting state fMRI. NeuroImage 45, 614–626.Google Scholar
Rucker, DD, Preacher, KJ, Tormala, ZL and Petty, RE (2011) Mediation analysis in social psychology: current practices and new recommendations. Social and Personality Psychology Compass 5, 13.Google Scholar
Saleh, A, Potter, GG, McQuoid, DR, Boyd, B, Turner, R, MacFall, JR et al. (2017) Effects of early life stress on depression, cognitive performance and brain morphology. Psychological Medicine 47, 171–181.Google Scholar
Saleptsi, E, Bichescu, D, Rockstroh, B, Neuner, F, Schauer, M, Studer, K et al. (2004) Negative and positive childhood experiences across developmental periods in psychiatric patients with different diagnoses - an explorative study. BMC Psychiatry 4, 14.Google Scholar
Schwabe, L, Joels, M, Roozendaal, B, Wolf, OT and Oitzl, MS (2012) Stress effects on memory: an update and integration. Neuroscience and Biobehavioral Reviews 36, 1740–1749.CrossRefGoogle ScholarPubMed
Smeets, T, Cornelisse, S, Quaedflieg, C, Meyer, T, Jelicic, M and Merckelbach, H (2012) Introducing the maastricht acute stress test (MAST): a quick and non-invasive approach to elicit robust autonomic and glucocorticoid stress responses. Psychoneuroendocrinology 37, 1998–2008.Google Scholar
Stoltenborgh, M, Bakermans-Kranenburg, MJ, Alink, LRA and van Ijzendoorn, MH (2015) The prevalence of child maltreatment across the globe: review of a series of meta-analyses. Child Abuse Review 24, 37–50.CrossRefGoogle Scholar
Struber, N, Struber, D and Roth, G (2014) Impact of early adversity on glucocorticoid regulation and later mental disorders. Neuroscience and Biobehavioral Reviews 38, 17–37.Google Scholar
Teicher, MH, Andersen, SL, Polcari, A, Anderson, CM, Navalta, CP and Kim, DM (2003) The neurobiological consequences of early stress and childhood maltreatment. Neuroscience and Biobehavioral Reviews 27, 33–44.Google Scholar
Teicher, MH and Samson, JA (2016) Annual research review: enduring neurobiological effects of childhood abuse and neglect. Journal of Child Psychology and Psychiatry 57, 241–266.Google Scholar
Teicher, MH, Samson, JA, Anderson, CM and Ohashi, K (2016) The effects of childhood maltreatment on brain structure, function and connectivity. Nature Reviews Neuroscience 17, 652.Google Scholar
Teicher, MH, Samson, JA, Sheu, YS, Polcari, A and McGreenery, CE (2010) Hurtful words: association of exposure to peer verbal abuse With elevated psychiatric symptom scores and corpus callosum abnormalities. American Journal of Psychiatry 167, 1464–1471.Google Scholar
Tottenham, N and Sheridan, MA (2010) A review of adversity, the amygdala and the hippocampus: a consideration of developmental timing. Frontiers in Human Neuroscience 3, 18.Google Scholar
Tzourio-Mazoyer, N, Landeau, B, Papathanassiou, D, Crivello, F, Etard, O, Delcroix, N et al. (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage 15, 273–289.CrossRefGoogle ScholarPubMed
van Velzen, LS, Schmaal, L, Jansen, R, Milaneschi, Y, Opmeer, EM, Elzinga, BM et al. (2016) Effect of childhood maltreatment and brain-derived neurotrophic factor on brain morphology. Social Cognitive and Affective Neuroscience 11, 1841–1852.Google Scholar
Vanderkolk, BA, Perry, JC and Herman, JL (1991) Childhood origins of self-destructive behavior. American Journal of Psychiatry 148, 1665–1671.Google Scholar
Wager, TD, Davidson, ML, Hughes, BL, Lindquist, MA and Ochsner, KN (2008) Prefrontal-subcortical pathways mediating successful emotion regulation. Neuron 59, 1037–1050.Google Scholar
Wieck, A, Grassi-Oliveira, R, do Prado, CH, Teixeira, AL and Bauer, ME (2014) Neuroimmunoendocrine interactions in post-traumatic stress disorder: focus on long-term implications of childhood maltreatment. Neuroimmunomodulation 21, 145–151.Google Scholar
Wolf, RC and Herringa, RJ (2016) Prefrontal-Amygdala dysregulation to threat in pediatric posttraumatic stress disorder. Neuropsychopharmacology 41, 822–831.Google Scholar
Supplementary material: File

Kaiser et al supplementary material

Kaiser et al supplementary material 1

Download Kaiser et al supplementary material(File)
File 6.1 MB