Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-24T01:18:27.109Z Has data issue: false hasContentIssue false
  • English
  • Français

The roles of early-life adversity and rumination in neural response to emotional faces amongst anxious and depressed adults

Published online by Cambridge University Press:  13 November 2018

Amy T. Peters ,
Katie L. Burkhouse ,
Kerry L. Kinney  and
K. Luan Phan
Amy T. Peters*
Affiliation:
Massachusetts General Hospital, Department of Psychiatry, Boston, MA, USA Harvard Medical School, Department of Psychiatry, Boston, MA, USA
Katie L. Burkhouse
Affiliation:
University of Illinois at Chicago, Department of Psychiatry, Chicago, IL, USA
Kerry L. Kinney
Affiliation:
University of Illinois at Chicago, Department of Psychiatry, Chicago, IL, USA
K. Luan Phan
Affiliation:
University of Illinois at Chicago, Department of Psychiatry, Chicago, IL, USA
*
Author for correspondence: Amy T. Peters, E-mail: [email protected]; [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Early-life adversity (ELA) is a risk factor for internalizing psychopathology (IP). ELA is also linked to alterations in neural phenotypes of emotion processing and maladaptive emotion regulatory strategies, such as ruminative brooding, in adulthood. We therefore expected that ELA would predict cortical brain activation to emotional faces in transdiagnostic IP and in turn, mediate the extent of rumination amongst patients with IPs and ELA (IP + ELA).

Method

One hundred and thirty-two individuals, including 102 treatment-seeking adults with heterogeneous IPs and 30 healthy controls (HCs) performed an Emotional Face-Matching Task during functional magnetic resonance imaging. Whole-brain analyses compared HC (n = 30), IP (n = 52), and IP + ELA (n = 50) neural responses to emotional (angry, fearful, happy, and sad) faces v. shapes, controlling for depression and anxiety symptoms. Parameter estimates of activation were extracted for significant between-group differences and tested as a mediator of ruminative brooding in IP + ELA.

Results

IP + ELA demonstrated increased activation in the superior frontal gyrus and anterior cingulate cortex (fear), superior parietal lobule, precuneus, posterior cingulate, and inferior temporal gyrus (fear only), and cuneus (fear and angry). These regions were preferentially correlated with ruminative brooding in IP + ELA, many of which mediated the link between IP + ELA and ruminative brooding.

Conclusions

Results provide evidence that ELA history amongst IP patients augments engagement of brain regions involved in emotion processing, above and beyond what is accounted for by current symptoms. Though longitudinal designs are needed, alterations in the neural correlates of maladaptive processing of socio-emotional information may be a common pathway by which ELA poses risk for psychopathology.

Keywords

Anxietydepressionearly childhood adversityemotion processingfunctional neuroimagingrumination
Type
Original Articles
Information
Psychological Medicine , Volume 49 , Issue 13 , October 2019 , pp. 2267 - 2278
Copyright
Copyright © Cambridge University Press 2018 

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

Ahmed-Leitao, F, Spies, G, van den Heuvel, L and Seedat, S (2016) Hippocampal and amygdala volumes in adults with posttraumatic stress disorder secondary to childhood abuse or maltreatment: a systematic review. Psychiatry Research 256, 33–43.Google Scholar
Aldao, A, Nolen-Hoeksema, S and Schweizer, S (2010) Emotion-regulation strategies across psychopathology: a meta-analytic review. Clinical Psychology Review 30, 217–237.Google Scholar
Allbaugh, LJ, Wright, MO and Folger, SF (2016) The role of repetitive thought in determining posttraumatic growth and distress following interpersonal trauma. Anxiety, Stress, and Coping 29, 21–37.Google Scholar
Arnow, BA (2004) Relationships between childhood maltreatment, adult health and psychiatric outcomes, and medical utilization. Journal of Clinical Psychiatry 65(Suppl. 12), 10–15.Google Scholar
Bekhbat, M and Neigh, GN (2018) Sex differences in the neuro-immune consequences of stress: focus on depression and anxiety. Brain Behavior and Immunity 67, 1–12.Google Scholar
Benjamini, Y and Hochberg, Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society. Series B (Methodological) 57, 289–300.Google Scholar
Bernstein, DP, Ahluvalia, T, Pogge, D and Handelsman, L (1997) Validity of the Childhood Trauma Questionnaire in an adolescent psychiatric population. Journal of the American Academy of Child & Adolescent Psychiatry 36, 340–348.Google Scholar
Bernstein, DP, Stein, JA, Newcomb, MD, Walker, E, Pogge, D, Ahluvalia, T, Stokes, J, Handelsman, L, Medrano, M, Desmond, D and Zule, W (2003) Development and validation of a brief screening version of the Childhood Trauma Questionnaire. Child Abuse Neglect 27, 169–190.Google Scholar
Bevilacqua, L, Carli, V, Sarchiapone, M, George, DK, Goldman, D, Roy, A and Enoch, MA (2012) Interaction between FKBP5 and childhood trauma and risk of aggressive behavior. Archives of General Psychiatry 69, 62–70.Google Scholar
Bowes, L and Jaffee, SR (2013) Biology, genes, and resilience: toward a multidisciplinary approach. Trauma, Violence & Abuse 14, 195–208.Google Scholar
Buff, C, Brinkmann, L, Neumeister, P, Feldker, K, Heitmann, C, Gathmann, B, Andor, T and Straube, T (2016) Specifically altered brain responses to threat in generalized anxiety disorder relative to social anxiety disorder and panic disorder. Neuroimage Clinical 12, 698–706.Google Scholar
Burkhouse, KL, Jacobs, RH, Peters, AT, Ajilore, O, Watkins, ER and Langenecker, SA (2017) Neural correlates of rumination in adolescents with remitted major depressive disorder and healthy controls. Cognitive Affective & Behavioral Neuroscience 17, 394–405.Google Scholar
Busso, DS, McLaughlin, KA and Sheridan, MA (2017) Dimensions of adversity, physiological reactivity, and externalizing psychopathology in adolescence: deprivation and threat. Psychosomatic Medicine 79, 162–171.Google Scholar
Clark, IA and Mackay, CE (2015) Mental imagery and post-traumatic stress disorder: a neuroimaging and experimental psychopathology approach to intrusive memories of trauma. Frontiers in Psychiatry 6, 104.Google Scholar
Cooney, RE, Joormann, J, Eugene, F, Dennis, EL and Gotlib, IH (2010) Neural correlates of rumination in depression. Cognitive Affective & Behavioral Neuroscience 10, 470–478.Google Scholar
Cuthbert, BN (2014) The RDoC framework: facilitating transition from ICD/DSM to dimensional approaches that integrate neuroscience and psychopathology. World Psychiatry 13, 28–35.Google Scholar
Cuthbert, BN (2015) Research Domain Criteria: toward future psychiatric nosologies. Dialogues in Clinical Neuroscience 17, 89–97.Google Scholar
Danese, A and Baldwin, JR (2017) Hidden wounds? Inflammatory links between childhood trauma and psychopathology. Annual Review of Psychology 68, 517–544.Google Scholar
Dannlowski, U, Stuhrmann, A, Beutelmann, V, Zwanzger, P, Lenzen, T, Grotegerd, D, Domschke, K, Hohoff, C, Ohrmann, P, Bauer, J, Lindner, C, Postert, C, Konrad, C, Arolt, V, Heindel, W, Suslow, T and Kugel, H (2012) Limbic scars: long-term consequences of childhood maltreatment revealed by functional and structural magnetic resonance imaging. Biological Psychiatry 71, 286–293.Google Scholar
Egeland, B (2009) Taking stock: childhood emotional maltreatment and developmental psychopathology. Child Abuse & Neglect 33, 22–26.Google Scholar
Etkin, A and Wager, TD (2007) Functional neuroimaging of anxiety: a meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. American Journal of Psychiatry 164, 1476–1488.Google Scholar
Etkin, A, Egner, T and Kalisch, R (2011) Emotional processing in anterior cingulate and medial prefrontal cortex. Trends in Cognitive Science 15, 85–93.Google Scholar
Feldker, K, Heitmann, CY, Neumeister, P, Tupak, SV, Schrammen, E, Moeck, R, Zwitserlood, P, Bruchmann, M and Straube, T (2017) Transdiagnostic brain responses to disorder-related threat across four psychiatric disorders. Psychological Medicine 47, 730–743.Google Scholar
Filkowski, MM and Haas, BW (2017) Rethinking the use of neutral faces as a baseline in fMRI neuroimaging studies of axis-I psychiatric disorders. Journal of Neuroimaging 27, 281–291.Google Scholar
First, M, Williams, J, Karg, R and Spitzer, R (2015) Structured Clinical Interview for DSM-5 – research version (SCID-5 for DSM-5, research version; SCID-5-RV). Arlington, VA: American Psychiatric Association.Google Scholar
Gaddy, MA and Ingram, RE (2014) A meta-analytic review of mood-congruent implicit memory in depressed mood. Clinical Psychology Review 34, 402–416.Google Scholar
Garvey, M, Avenevoli, S and Anderson, K (2016) The National Institute of Mental Health research domain criteria and clinical research in child and adolescent psychiatry. Journal of the American Academy of Child and Adolescent Psychiatry 55, 93–98.Google Scholar
Gentili, C, Cristea, IA, Angstadt, M, Klumpp, H, Tozzi, L, Phan, KL and Pietrini, P (2016) Beyond emotions: a meta-analysis of neural response within face processing system in social anxiety. Experimental Biology & Medicine (Maywood) 241, 225–237.Google Scholar
Gibb, BE, Schofield, CA and Coles, ME (2009) Reported history of childhood abuse and young adults’ information-processing biases for facial displays of emotion. Child Maltreatment 14, 148–156.Google Scholar
Gilbert, R, Widom, CS, Browne, K, Fergusson, D, Webb, E and Janson, S (2009) Burden and consequences of child maltreatment in high-income countries. The Lancet 373, 68–81.Google Scholar
Gorka, SM, Fitzgerald, DA, Labuschagne, I, Hosanagar, A, Wood, AG, Nathan, PJ and Phan, KL (2015) Oxytocin modulation of amygdala functional connectivity to fearful faces in generalized social anxiety disorder. Neuropsychopharmacology 40, 278.Google Scholar
Grierson, AB, Hickie, IB, Naismith, SL and Scott, J (2016) The role of rumination in illness trajectories in youth: linking trans-diagnostic processes with clinical staging models. Psychological Medicine 46, 2467–2484.Google Scholar
Gur, RC, Schroeder, L, Turner, T, McGrath, C, Chan, RM, Turetsky, BI, Alsop, D, Maldjian, J and Gur, RE (2002) Brain activation during facial emotion processing. Neuroimage 16, 651–662.Google Scholar
Hamilton, M (1959) The assessment of anxiety states by rating. Psychology and Psychotherapy: Theory, Research and Practice 32, 50–55.Google Scholar
Hamilton, M (1960) A rating scale for depression. Journal of Neurology, Neurosurgery, and Psychiatry 23, 56.Google Scholar
Hamilton, JP, Etkin, A, Furman, DJ, Lemus, MG, Johnson, RF and Gotlib, IH (2012) Functional neuroimaging of major depressive disorder: a meta-analysis and new integration of base line activation and neural response data. American Journal of Psychiatry 169, 693–703.Google Scholar
Hariri, AR, Tessitore, A, Mattay, VS, Fera, F and Weinberger, DR (2002) The amygdala response to emotional stimuli: a comparison of faces and scenes. Neuroimage 17, 317–323.Google Scholar
Hart, H and Rubia, K (2012) Neuroimaging of child abuse: a critical review. Frontiers in Human Neuroscience 6, 52.Google Scholar
Hayes, AF (2012) PROCESS: A Versatile Computational Tool for Observed Variable Mediation, Moderation, and Conditional Process Modeling. KS: University of Kansas.Google Scholar
Heany, SJ, Groenewold, NA, Uhlmann, A, Dalvie, S, Stein, DJ and Brooks, SJ (2018) The neural correlates of Childhood Trauma Questionnaire scores in adults: a meta-analysis and review of functional magnetic resonance imaging studies. Development and Psychopathology 30, 1475–1485.Google Scholar
Hein, TC and Monk, CS (2017) Research review: neural response to threat in children, adolescents, and adults after child maltreatment – a quantitative meta-analysis. Journal of Child Psychology and Psychiatry 58, 222–230.Google Scholar
Heller, AS (2016) Cortical-subcortical interactions in depression: from animal models to human psychopathology. Frontiers in Systems Neuroscience 10, 20.Google Scholar
Holz, NE, Buchmann, AF, Boecker, R, Blomeyer, D, Baumeister, S, Wolf, I, Rietschel, M, Witt, SH, Plichta, MM, Meyer-Lindenberg, A, Banaschewski, T, Brandeis, D and Laucht, M (2015) Role of FKBP5 in emotion processing: results on amygdala activity, connectivity and volume. Brain Structure & Function 220, 1355–1368.Google Scholar
Insel, TR (2014) The NIMH Research Domain Criteria (RDoC) Project: precision medicine for psychiatry. American Journal of Psychiatry 171, 395–397.Google Scholar
Johnson, AL, Benas, JS and Gibb, BE (2011) Depressive implicit associations and adults’ reports of childhood abuse. Cognition & Emotion 25, 328–333.Google Scholar
Jones, SH, Thornicroft, G, Coffey, M and Dunn, G (1995) A brief mental health outcome scale-reliability and validity of the Global Assessment of Functioning (GAF). The British Journal of Psychiatry 166, 654–659.Google Scholar
Kim, JS, Jin, MJ, Jung, W, Hahn, SW and Lee, SH (2017) Rumination as a mediator between childhood trauma and adulthood depression/anxiety in non-clinical participants. Frontiers in Psychology 8, 1597.Google Scholar
Kim-Cohen, J and Turkewitz, R (2012) Resilience and measured gene-environment interactions. Developmental Psychopathol 24, 1297–1306.Google Scholar
Kozak, MJ and Cuthbert, BN (2016) The NIMH research domain criteria initiative: background, issues, and pragmatics. Psychophysiology 53, 286–297.Google Scholar
Kudinova, AY, Gibb, BE, McGeary, JE and Knopik, VS (2015) Brain derived neurotrophic factor (BDNF) polymorphism moderates the interactive effect of 5-HTTLPR polymorphism and childhood abuse on diagnoses of major depression in women. Psychiatry Research 225, 746–747.Google Scholar
Lee, V and Hoaken, PN (2007) Cognition, emotion, and neurobiological development: mediating the relation between maltreatment and aggression. Childhood Maltreatreant 12, 281–298.Google Scholar
Levy, BJ and Anderson, MC (2008) Individual differences in the suppression of unwanted memories: the executive deficit hypothesis. Acta Psychologica (Amst) 127, 623–635.Google Scholar
Lim, L, Radua, J and Rubia, K (2014) Gray matter abnormalities in childhood maltreatment: a voxel-wise meta-analysis. American Journal of Psychiatry 171, 854–863.Google Scholar
Lovibond, PF and Lovibond, SH (1995) The structure of negative emotional states: comparison of the Depression Anxiety Stress Scales (DASS) with the Beck Depression and Anxiety Inventories. Behaviour Research and Therapy 33, 335–343.Google Scholar
Lu, S, Peng, H, Wang, L, Vasish, S, Zhang, Y, Gao, W, Wu, W, Liao, M, Wang, M, Tang, H, Li, W, Li, W, Li, Z, Zhou, J, Zhang, Z and Li, L (2013) Elevated specific peripheral cytokines found in major depressive disorder patients with childhood trauma exposure: a cytokine antibody array analysis. Comprehensive Psychiatry 54, 953–961.Google Scholar
MacNamara, A, Klumpp, H, Kennedy, AE, Langenecker, SA and Phan, KL (2017) Transdiagnostic neural correlates of affective face processing in anxiety and depression. Depression and Anxiety 34, 621–631.Google Scholar
McCrory, EJ and Viding, E (2015) The theory of latent vulnerability: reconceptualizing the link between childhood maltreatment and psychiatric disorder. Developmental Psychopathology 27, 493–505.Google Scholar
McCrory, E, De Brito, SA and Viding, E (2012) The link between child abuse and psychopathology: a review of neurobiological and genetic research. Journal of the Royal Society of Medicine 105, 151–156.Google Scholar
McCrory, EJ, Gerin, MI and Viding, E (2017) Annual research review: childhood maltreatment, latent vulnerability and the shift to preventative psychiatry – the contribution of functional brain imaging. Journal of Child Psychology and Psychiatry 58, 338–357.Google Scholar
McLaughlin, KA and Nolen-Hoeksema, S (2011) Rumination as a transdiagnostic factor in depression and anxiety. Behaviour Research and Therapy 49, 186–193.Google Scholar
Nolen-Hoeksema, S and Watkins, ER (2011) A heuristic for developing transdiagnostic models of psychopathology: explaining multifinality and divergent trajectories. Perspectives on Psycholigcal Science 6, 589–609.Google Scholar
Nolen-Hoeksema, S, Wisco, BE and Lyubomirsky, S (2008) Rethinking rumination. Perspectives on Psychological Science 3, 400–424.Google Scholar
Ono, M, Devilly, GJ and Shum, DH (2016) A meta-analytic review of overgeneral memory: the role of trauma history, mood, and the presence of posttraumatic stress disorder. Psychological Trauma 8, 157–164.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 Biobehavioral Reviews 69, 299–312.Google Scholar
Phan, KL, Coccaro, EF, Angstadt, M, Kreger, KJ, Mayberg, HS, Liberzon, I and Stein, MB (2013) Corticolimbic brain reactivity to social signals of threat before and after sertraline treatment in generalized social phobia. Biological Psychiatry 73, 329–336.Google Scholar
Pollak, SD and Tolley-Schell, SA (2003) Selective attention to facial emotion in physically abused children. Journal of Abnormal Psychology 112, 323–338.Google Scholar
Pollak, SD, Cicchetti, D, Hornung, K and Reed, A (2000) Recognizing emotion in faces: developmental effects of child abuse and neglect. Developmental Psychology 36, 679–688.Google Scholar
Preacher, KJ and Hayes, AF (2004) SPSS and SAS procedures for estimating indirect effects in simple mediation models. Behavior Research Methods, Instruments, & Computers 36, 717–731.Google Scholar
Puetz, VB and McCrory, E (2015) Exploring the relationship between childhood maltreatment and addiction: a review of the neurocognitive evidence. Current Addiction Reports 2, 318–325.Google Scholar
Raes, F and Hermans, D (2008) On the mediating role of subtypes of rumination in the relationship between childhood emotional abuse and depressed mood: brooding versus reflection. Depression and Anxiety 25, 1067–1070.Google Scholar
Riem, MM, Alink, LR, Out, D, Van Ijzendoorn, MH and Bakermans-Kranenburg, MJ (2015) Beating the brain about abuse: empirical and meta-analytic studies of the association between maltreatment and hippocampal volume across childhood and adolescence. Developmental Psychopathology 27, 507–520.Google Scholar
Schonfeld, S and Ehlers, A (2017) Posttraumatic stress disorder and autobiographical memories in everyday life. Clinical Psychological Science 5, 325–340.Google Scholar
Schurz, M, Radua, J, Aichhorn, M, Richlan, F and Perner, J (2014) Fractionating theory of mind: a meta-analysis of functional brain imaging studies. Neuroscience Biobehavioral Reviews 42, 9–34.Google Scholar
Shackman, JE and Pollak, SD (2014) Impact of physical maltreatment on the regulation of negative affect and aggression. Developmental Psychopathology 26, 1021–1033.Google Scholar
Sharp, C, Fowler, JC, Salas, R, Nielsen, D, Allen, J, Oldham, J, Kosten, T, Mathew, S, Madan, A, Frueh, BC and Fonagy, P (2016) Operationalizing NIMH Research Domain Criteria (RDoC) in naturalistic clinical settings. Bulletine of the Menninger Clinic 80, 187–212.Google Scholar
Sheng, Y and Sheng, Z (2012) Is coefficient alpha robust to non-normal data? Frontiers in Psychology 3, 34.Google Scholar
Shin, LM and Liberzon, I (2010) The neurocircuitry of fear, stress, and anxiety disorders. Neuropsychopharmacology 35, 169–191.Google Scholar
Smith, JM and Alloy, LB (2009) A roadmap to rumination: a review of the definition, assessment, and conceptualization of this multifaceted construct. Clinical Psychology Review 29, 116–128.Google Scholar
Teicher, MH, Andersen, SL, Polcari, A, Anderson, CM and Navalta, CP (2002) Developmental neurobiology of childhood stress and trauma. Psychiatric Clinics of North America 25, 397–426, vii-viii.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, 652–666.Google Scholar
Treynor, W, Gonzalez, R and Nolen-Hoeksema, S (2003) Rumination reconsidered: a psychometric analysis. Cognitive Therapy and Research 27, 247–259.Google Scholar
Vuilleumier, P and Pourtois, G (2007) Distributed and interactive brain mechanisms during emotion face perception: evidence from functional neuroimaging. Neuropsychologia 45, 174–194.Google Scholar
Walker, EA, Unutzer, J, Rutter, C, Gelfand, A, Saunders, K, VonKorff, M, Koss, MP and Katon, W (1999) Costs of health care use by women HMO members with a history of childhood abuse and neglect. Archives of General Psychiatry 56, 609–613.Google Scholar
Walter, B, Blecker, C, Kirsch, P, Sammer, G, Schienle, A, Stark, R and Vaitl, D (2003) MARINA: an easy to use tool for the creation of MAsks for Region of INterest Analyses. Neuroimage 19, e1899.Google Scholar
Waters, AM and Craske, MG (2016) Towards a cognitive-learning formulation of youth anxiety: a narrative review of theory and evidence and implications for treatment. Clinical Psychology Review 50, 50–66.Google Scholar
Wegman, HL and Stetler, C (2009) A meta-analytic review of the effects of childhood abuse on medical outcomes in adulthood. Psychosomatic Medicine 71, 805–812.Google Scholar
Widom, CS, DuMont, K and Czaja, SJ (2007) A prospective investigation of major depressive disorder and comorbidity in abused and neglected children grown up. Archives of General Psychiatry 64, 49–56.Google Scholar
Supplementary material: Image

Peters et al. supplementary material

Figure S1

Download Peters et al. supplementary material(Image)
Image 2.1 MB