Hostname: page-component-8448b6f56d-42gr6 Total loading time: 0 Render date: 2024-04-23T16:22:00.929Z Has data issue: false hasContentIssue false
  • English
  • Français

Trauma-associated anterior cingulate connectivity during reward learning predicts affective and anxiety states in young adults

Published online by Cambridge University Press:  19 September 2018

Kristen L. Eckstrand ,
Lindsay C. Hanford ,
Michele A. Bertocci ,
Henry W. Chase ,
Tsafrir Greenberg ,
Jeanette Lockovich ,
Ricki Stiffler ,
Haris A. Aslam ,
Simona Graur  and
Genna Bebko
...Show all authors
Kristen L. Eckstrand*
Affiliation:
Department of Psychiatry, University of Pittsburgh, Pittsburgh, PA, USA
Lindsay C. Hanford
Affiliation:
Department of Psychiatry, University of Pittsburgh, Pittsburgh, PA, USA
Michele A. Bertocci
Affiliation:
Department of Psychiatry, University of Pittsburgh, Pittsburgh, PA, USA
Henry W. Chase
Affiliation:
Department of Psychiatry, University of Pittsburgh, Pittsburgh, PA, USA
Tsafrir Greenberg
Affiliation:
Department of Psychiatry, University of Pittsburgh, Pittsburgh, PA, USA
Jeanette Lockovich
Affiliation:
Department of Psychiatry, University of Pittsburgh, Pittsburgh, PA, USA
Ricki Stiffler
Affiliation:
Department of Psychiatry, University of Pittsburgh, Pittsburgh, PA, USA
Haris A. Aslam
Affiliation:
Department of Psychiatry, University of Pittsburgh, Pittsburgh, PA, USA
Simona Graur
Affiliation:
Department of Psychiatry, University of Pittsburgh, Pittsburgh, PA, USA
Genna Bebko
Affiliation:
Department of Psychiatry, University of Pittsburgh, Pittsburgh, PA, USA
Erika E. Forbes
Affiliation:
Department of Psychiatry, University of Pittsburgh, Pittsburgh, PA, USA
Mary L. Phillips
Affiliation:
Department of Psychiatry, University of Pittsburgh, Pittsburgh, PA, USA
*
Author for correspondence: Kristen Eckstrand, E-mail: eckstrandkl@upmc.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Trauma exposure is associated with development of depression and anxiety; yet, some individuals are resilient to these trauma-associated effects. Differentiating mechanisms underlying development of negative affect and resilience following trauma is critical for developing effective interventions. One pathway through which trauma could exert its effects on negative affect is reward-learning networks. In this study, we examined relationships among lifetime trauma, reward-learning network function, and emotional states in young adults.

Methods

One hundred eleven young adults self-reported trauma and emotional states and underwent functional magnetic resonance imaging during a monetary reward task. Trauma-associated neural activation and functional connectivity were analyzed during reward prediction error (RPE). Relationships between trauma-associated neural functioning and affective and anxiety symptoms were examined.

Results

Number of traumatic events was associated with greater ventral anterior cingulate cortex (vACC) activation, and lower vACC connectivity with the right insula, frontopolar, inferior parietal, and temporoparietal regions, during RPE. Lower trauma-associated vACC connectivity with frontoparietal regions implicated in regulatory and decision-making processes was associated with heightened affective and anxiety symptoms; lower vACC connectivity with insular regions implicated in interoception was associated with lower affective and anxiety symptoms.

Conclusions

In a young adult sample, two pathways linked the impact of trauma on reward-learning networks with higher v. lower negative affective and anxiety symptoms. The disconnection between vACC and regions implicated in decision-making and self-referential processes may reflect aberrant regulatory but appropriate self-focused mechanisms, respectively, conferring risk for v. resilience against negative affective and anxiety symptoms.

Keywords

Anxietydepressionresiliencereward learningreward predictiontrauma
Type
Original Articles
Information
Psychological Medicine , Volume 49 , Issue 11 , August 2019 , pp. 1831 - 1840
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

Amemori, K-i and Graybiel, AM (2012) Localized microstimulation of primate pregenual cingulate cortex induces negative decision-making. Nature Neuroscience 15, 776–785.Google Scholar
Amiez, C, Joseph, J-P and Procyk, E (2005) Reward encoding in the monkey anterior cingulate cortex. Cerebral Cortex 16, 1040–1055.Google Scholar
Anda, RF, Felitti, VJ, Bremner, JD, Walker, JD, Whitfield, C, Perry, BD, Dube, SR and Giles, WH (2006) The enduring effects of abuse and related adverse experiences in childhood. A convergence of evidence from neurobiology and epidemiology. European Archives of Psychiatry and Clinical Neuroscience 256, 174–186.Google Scholar
Barker, JM, Taylor, JR and Chandler, LJ (2014) A unifying model of the role of the infralimbic cortex in extinction and habits. Learning & Memory 21, 441–448.Google Scholar
Beckmann, M, Johansen-Berg, H and Rushworth, MF (2009) Connectivity-based parcellation of human cingulate cortex and its relation to functional specialization. Journal of Neuroscience 29, 1175–1190.Google Scholar
Behzadi, Y, Restom, K, Liau, J and Liu, TT (2007) A component based noise correction method (CompCor) for BOLD and perfusion based fMRI. Neuroimage 37, 90–101.Google Scholar
Boschin, EA, Piekema, C and Buckley, MJ (2015) Essential functions of primate frontopolar cortex in cognition. Proceedings of the National Academy of Sciences of the United States of America 112, E1020–E1027.Google Scholar
Chapman, DP, Whitfield, CL, Felitti, VJ, Dube, SR, Edwards, VJ and Anda, RF (2004) Adverse childhood experiences and the risk of depressive disorders in adulthood. Journal of Affective Disorders 82, 217–225.Google Scholar
Chase, HW, Fournier, JC, Bertocci, MA, Greenberg, T, Aslam, H, Stiffler, R, Lockovich, J, Graur, S, Bebko, G, Forbes, EE and Phillips, ML (2017) A pathway linking reward circuitry, impulsive sensation-seeking and risky decision-making in young adults: identifying neural markers for new interventions. Translational Psychiatry 7, e1096.Google Scholar
Corral-Frias, NS, Nikolova, YS, Michalski, LJ, Baranger, DA, Hariri, AR and Bogdan, R (2015) Stress-related anhedonia is associated with ventral striatum reactivity to reward and transdiagnostic psychiatric symptomatology. Psychological Medicine 45, 2605–2617.Google Scholar
Cox, CL, Uddin, LQ, Di Martino, A, Castellanos, FX, Milham, MP and Kelly, C (2011) The balance between feeling and knowing: affective and cognitive empathy are reflected in the brain's intrinsic functional dynamics. Social Cognitive and Affective Neuroscience 7, 727–737.Google Scholar
Delgado, MR, Nystrom, LE, Fissell, C, Noll, DC and Fiez, JA (2000) Tracking the hemodynamic responses to reward and punishment in the striatum. Journal of Neurophysiology 84, 3072–3077.Google Scholar
Demirtaş, M, Tornador, C, Falcon, C, López-Solà, M, Hernández-Ribas, R, Pujol, J, Menchon, JM, Ritter, P, Cardoner, N and Soriano-Mas, C (2016) Dynamic functional connectivity reveals altered variability in functional connectivity among patients with major depressive disorder. Human Brain Mapping 37, 2918–2930.Google Scholar
Dennison, MJ, Sheridan, MA, Busso, DS, Jenness, JL, Peverill, M, Rosen, ML and McLaughlin, KA (2016) Neurobehavioral markers of resilience to depression amongst adolescents exposed to child abuse. Journal of Abnormal Psychology 125, 1201–1212.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 113, 7900–7905.Google Scholar
Elsey, J, Coates, A, Lacadie, CM, McCrory, EJ, Sinha, R, Mayes, LC and Potenza, MN (2015) Childhood trauma and neural responses to personalized stress, favorite-food and neutral-relaxing cues in adolescents. Neuropsychopharmacology 40, 1580–1589.Google Scholar
Etkin, A, Egner, T and Kalisch, R (2011) Emotional processing in anterior cingulate and medial prefrontal cortex. Trends in Cognitive Sciences 15, 85–93.Google Scholar
Forbes, EE, Hariri, AR, Martin, SL, Silk, JS, Moyles, DL, Fisher, PM, Brown, SM, Ryan, ND, Birmaher, B and Axelson, DA (2009) Altered striatal activation predicting real-world positive affect in adolescent major depressive disorder. American Journal of Psychiatry. 166, 64–73.Google Scholar
Fournier, JC, Chase, HW, Almeida, J and Phillips, ML (2014) Model specification and the reliability of fMRI results: implications for longitudinal neuroimaging studies in psychiatry. PLoS One 9, e105169.Google Scholar
Goff, B, Gee, DG, Telzer, EH, Humphreys, KL, Gabard-Durnam, L, Flannery, J and Tottenham, N (2013) Reduced nucleus accumbens reactivity and adolescent depression following early-life stress. Neuroscience 249, 129–138.Google Scholar
Gorgolewski, K, Burns, CD, Madison, C, Clark, D, Halchenko, YO, Waskom, ML and Ghosh, SS (2011) Nipype: a flexible, lightweight and extensible neuroimaging data processing framework in python. Frontiers in Neuroinformatics 5, 13.Google Scholar
Guyer, AE, Nelson, EE, Perez-Edgar, K, Hardin, MG, Roberson-Nay, R, Monk, CS, Bjork, JM, Henderson, HA, Pine, DS and Fox, NA (2006) Striatal functional alteration in adolescents characterized by early childhood behavioral inhibition. Journal of Neuroscience 26, 6399–6405.Google Scholar
Hamilton, M (1959) The assessment of anxiety states by rating. British Journal of Medical Psychology 32, 50–55.Google Scholar
Hamilton, M (1960) A rating scale for depression. Journal of Neurology, Neurosurgery & Psychiatry 23, 56–62.Google Scholar
Hanson, JL, Albert, D, Iselin, AR, Carre, JM, Dodge, KA and Hariri, AR (2015) Cumulative stress in childhood is associated with blunted reward-related brain activity in adulthood. Social Cognitive and Affective Neuroscience 11, 405–412.Google Scholar
Heponiemi, T, Keltikangas-Järvinen, L, Puttonen, S and Ravaja, N (2003) BIS/BAS sensitivity and self-rated affects during experimentally induced stress. Personality and Individual Differences 34, 943–957.Google Scholar
Herringa, RJ, Birn, RM, Ruttle, PL, Burghy, CA, Stodola, DE, Davidson, RJ and Essex, MJ (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.Google Scholar
Hooper, LM, Stockton, P, Krupnick, JL and Green, BL (2011) Development, use, and psychometric properties of the Trauma History Questionnaire. Journal of Loss and Trauma 16, 258–283.Google Scholar
Iadipaolo, AS, Marusak, HA, Sala-Hamrick, K, Crespo, LM, Thomason, ME and Rabinak, CA (2017) Behavioral activation sensitivity and default mode network-subgenual cingulate cortex connectivity in youth. Behavioural Brain Research 333, 135–141.Google Scholar
Kaczkurkin, AN, Moore, TM, Ruparel, K, Ciric, R, Calkins, ME, Shinohara, RT, Elliott, MA, Hopson, R, Roalf, DR and Vandekar, SN (2016) Elevated amygdala perfusion mediates developmental sex differences in trait anxiety. Biological Psychiatry 80, 775–785.Google Scholar
Kessler, RC, Amminger, GP, Aguilar-Gaxiola, S, Alonso, J, Lee, S and Ustun, TB (2007) Age of onset of mental disorders: a review of recent literature. Current Opinion in Psychiatry 20, 359–364.Google Scholar
Kilpatrick, DG, Resnick, HS, Milanak, ME, Miller, MW, Keyes, KM and Friedman, MJ (2013) National estimates of exposure to traumatic events and PTSD prevalence using DSM-IV and DSM-5 criteria. Journal of Traumatic Stress 26, 537–547.Google Scholar
Kristjansson, S, McCutcheon, VV, Agrawal, A, Lynskey, MT, Conroy, E, Statham, DJ, Madden, PA, Henders, AK, Todorov, AA, Bucholz, KK, Degenhardt, L, Martin, NG, Heath, AC and Nelson, EC (2016) The variance shared across forms of childhood trauma is strongly associated with liability for psychiatric and substance use disorders. Brain and Behavior 6, e00432. doi: 10.1002/brb3.432.Google Scholar
Li, M, D'arcy, C and Meng, X (2016) Maltreatment in childhood substantially increases the risk of adult depression and anxiety in prospective cohort studies: systematic review, meta-analysis, and proportional attributable fractions. Psychological Medicine 46, 717–730.Google Scholar
Lim, L, Hart, H, Mehta, MA, Simmons, A, Mirza, K and Rubia, K (2015) Neural correlates of error processing in young people with a history of severe childhood abuse: an fMRI study. American Journal of Psychiatry 172, 892–900.Google Scholar
Marusak, HA, Martin, KR, Etkin, A and Thomason, ME (2015) Childhood trauma exposure disrupts the automatic regulation of emotional processing. Neuropsychopharmacology 40, 1250–1258.Google Scholar
McLaughlin, KA, Peverill, M, Gold, AL, Alves, S and Sheridan, MA (2015) Child maltreatment and neural systems underlying emotion regulation. Journal of the American Academy of Child & Adolescent Psychiatry 54, 753–762.Google Scholar
Mehta, MA, Gore-Langton, E, Golembo, N, Colvert, E, Williams, SC and Sonuga-Barke, E (2010) Hyporesponsive reward anticipation in the basal ganglia following severe institutional deprivation early in life. Journal of Cognitive Neuroscience 22, 2316–2325.Google Scholar
Merikangas, KR, Nakamura, EF and Kessler, RC (2009) Epidemiology of mental disorders in children and adolescents. Dialogues in Clinical Neuroscience 11, 7–20.Google Scholar
Myers, HF, Wyatt, GE, Ullman, JB, Loeb, TB, Chin, D, Prause, N, Zhang, M, Williams, JK, Slavich, GM and Liu, H (2015) Cumulative burden of lifetime adversities: trauma and mental health in low-SES African Americans and Latino/as. Psychological Trauma 7, 243–251.Google Scholar
Nanni, V, Uher, R and 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.Google Scholar
Niki, H and Watanabe, M (1979) Prefrontal and cingulate unit activity during timing behavior in the monkey. Brain Research 171, 213–224.Google Scholar
Nikolova, YS, Bogdan, R, Brigidi, BD and Hariri, AR (2012) Ventral striatum reactivity to reward and recent life stress interact to predict positive affect. Biological Psychiatry 72, 157–163.Google Scholar
O'Doherty, JP, Dayan, P, Friston, K, Critchley, H and Dolan, RJ (2003) Temporal difference models and reward-related learning in the human brain. Neuron 38, 329–337.Google Scholar
O'Reilly, JX, Woolrich, MW, Behrens, TE, Smith, SM and Johansen-Berg, H (2012) Tools of the trade: psychophysiological interactions and functional connectivity. Social Cognitive and Affective Neuroscience 7, 604–609.Google Scholar
Peters, J, Kalivas, PW and Quirk, GJ (2009) Extinction circuits for fear and addiction overlap in prefrontal cortex. Learning & Memory 16, 279–288.Google Scholar
Pizzagalli, DA (2014) Depression, stress, and anhedonia: toward a synthesis and integrated model. Annual Review of Clinical Psychology 10, 393–423.Google Scholar
Polanía, R, Moisa, M, Opitz, A, Grueschow, M and Ruff, CC (2015) The precision of value-based choices depends causally on fronto-parietal phase coupling. Nature Communications 6, 8090.Google Scholar
Pollatos, O, Gramann, K and Schandry, R (2007) Neural systems connecting interoceptive awareness and feelings. Human Brain Mapping 28, 9–18.Google Scholar
Price, M and van Stolk-Cooke, K (2015) Examination of the interrelations between the factors of PTSD, major depression, and generalized anxiety disorder in a heterogeneous trauma-exposed sample using DSM 5 criteria. Journal of Affective Disorders 186, 149–155.Google Scholar
Ptak, R (2012) The frontoparietal attention network of the human brain: action, saliency, and a priority map of the environment. The Neuroscientist 18, 502–515.Google Scholar
Puetz, VB, Kohn, N, Dahmen, B, Zvyagintsev, M, Schüppen, A, Schultz, RT, Heim, CM, Fink, GR, Herpertz-Dahlmann, B and Konrad, K (2014) Neural response to social rejection in children with early separation experiences. Journal of the American Academy of Child & Adolescent Psychiatry 53, 1328–1337, e8.Google Scholar
Rushworth, MF and Behrens, TE (2008) Choice, uncertainty and value in prefrontal and cingulate cortex. Nature Neuroscience 11, 389–397.Google Scholar
Rutledge, RB, Moutoussis, M, Smittenaar, P, Zeidman, P, Taylor, T, Hrynkiewicz, L, Lam, J, Skandali, N, Siegel, JZ, Ousdal, OT, Prabhu, G, Dayan, P, Fonagy, P and Dolan, RJ (2017) Association of neural and emotional impacts of reward prediction errors with major depression. JAMA Psychiatry 74, 790–797.Google Scholar
Sadeh, N, Miller, MW, Wolf, EJ and Harkness, KL (2015) Negative emotionality and disconstraint influence PTSD symptom course via exposure to new major adverse life events. Journal of Anxiety Disorders 31, 20–27.Google Scholar
Schultz, W (2016) Dopamine reward prediction error coding. Dialogues in Clinical Neuroscience 18, 23–32.Google Scholar
Snaith, RP, Hamilton, M, Morley, S, Humayan, A, Hargreaves, D and Trigwell, P (1995) A scale for the assessment of hedonic tone the Snaith-Hamilton Pleasure Scale. British Journal of Psychiatry 167, 99–103.Google Scholar
Stringaris, A, Vidal-Ribas Belil, P, Artiges, E, Lemaitre, H, Gollier-Briant, F, Wolke, S, Vulser, H, Miranda, R, Penttilä, J and Struve, M (2015) The brain's response to reward anticipation and depression in adolescence: dimensionality, specificity, and longitudinal predictions in a community-based sample. American Journal of Psychiatry 172, 1215–1223.Google Scholar
Sylvester, C, Corbetta, M, Raichle, M, Rodebaugh, T, Schlaggar, B, Sheline, Y, Zorumski, C and Lenze, E (2012) Functional network dysfunction in anxiety and anxiety disorders. Trends in Neurosciences 35, 527–535.Google Scholar
Tolin, DF and Foa, EB (2006) Sex differences in trauma and posttraumatic stress disorder: a quantitative review of 25 years of research. Psychological Bulletin 132, 959–992.Google Scholar
Vincent, JL, Kahn, I, Snyder, AZ, Raichle, ME and Buckner, RL (2008) Evidence for a frontoparietal control system revealed by intrinsic functional connectivity. Journal of Neurophysiology 100, 3328–3342.Google Scholar
von Rhein, D, Beckmann, CF, Franke, B, Oosterlaan, J, Heslenfeld, DJ, Hoekstra, PJ, Hartman, CA, Luman, M, Faraone, SV and Cools, R (2017) Network-level assessment of reward-related activation in patients with ADHD and healthy individuals. Human Brain Mapping 38, 2359–2369.Google Scholar
Vrieze, E, Pizzagalli, DA, Demyttenaere, K, Hompes, T, Sienaert, P, de Boer, P, Schmidt, M and Claes, S (2013) Reduced reward learning predicts outcome in major depressive disorder. Biological Psychiatry 73, 639–645.Google Scholar
Walton, M, Kennerley, S, Bannerman, D, Phillips, P and Rushworth, MF (2006) Weighing up the benefits of work: behavioral and neural analyses of effort-related decision making. Neural Networks 19, 1302–1314.Google Scholar
Wang, Y, Ma, N, He, X, Li, N, Wei, Z, Yang, L, Zha, R, Han, L, Li, X and Zhang, D (2017) Neural substrates of updating the prediction through prediction error during decision making. Neuroimage 157, 1–12.Google Scholar
White, SF, Geraci, M, Lewis, E, Leshin, J, Teng, C, Averbeck, B, Meffert, H, Ernst, M, Blair, JR and Grillon, C (2016) Prediction error representation in individuals with generalized anxiety disorder during passive avoidance. American Journal of Psychiatry 174, 110–117.Google Scholar
Williams, SM and Goldman-Rakic, P (1998) Widespread origin of the primate mesofrontal dopamine system. Cerebral Cortex 8, 321–345.Google Scholar
Woo, CW, Krishnan, A and Wager, TD (2014) Cluster-extent based thresholding in fMRI analyses: pitfalls and recommendations. Neuroimage 91, 412–419.Google Scholar
Yao, Z, Wang, L, Lu, Q, Liu, H and Teng, G (2009) Regional homogeneity in depression and its relationship with separate depressive symptom clusters: a resting-state fMRI study. Journal of Affective Disorders 115, 430–438.Google Scholar
Supplementary material: File

Eckstrand et al. supplementary material

Eckstrand et al. supplementary material 1

Download Eckstrand et al. supplementary material(File)
File 43.7 KB