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The impact of traumatic stress on Pavlovian biases

Published online by Cambridge University Press:  23 June 2017

O. T. Ousdal ,
Q. J. Huys ,
A. M. Milde ,
A. R. Craven ,
L. Ersland ,
T. Endestad ,
A. Melinder ,
K. Hugdahl  and
R. J. Dolan
O. T. Ousdal*
Affiliation:
Department of Radiology, Haukeland University Hospital, Bergen, Norway Wellcome Trust Centre for Neuroimaging, University College London, London, UK
Q. J. Huys
Affiliation:
Translational Neuromodeling Unit, Institute of Biomedical Engineering, University of Zürich and Swiss Federal Institute of Technology (ETH) Zürich, Zurich, Switzerland Department of Psychiatry, Psychotherapy and Psychosomatics, Centre for addiction disorders, Hospital of Psychiatry, University of Zürich, Zurich, Switzerland
A. M. Milde
Affiliation:
Department of Biological and Medical Psychology, University of Bergen, Bergen, Norway Regional Centre for Child and Youth Mental Health and Child Welfare, UNI Research Health, Bergen, Norway
A. R. Craven
Affiliation:
Department of Biological and Medical Psychology, University of Bergen, Bergen, Norway NORMENT, Centre of Excellence, University of Oslo, Oslo, Norway
L. Ersland
Affiliation:
Department of Clinical Engineering, Haukeland University Hospital, Bergen, Norway
T. Endestad
Affiliation:
Institute of Psychology, University of Oslo, Oslo, Norway
A. Melinder
Affiliation:
Institute of Psychology, University of Oslo, Oslo, Norway
K. Hugdahl
Affiliation:
Department of Radiology, Haukeland University Hospital, Bergen, Norway Department of Biological and Medical Psychology, University of Bergen, Bergen, Norway NORMENT, Centre of Excellence, University of Oslo, Oslo, Norway Division of Psychiatry, Haukeland University Hospital, Bergen, Norway KG Jebsen Centre for Neuropsychiatric Disorders, University of Bergen, Bergen, Norway
R. J. Dolan
Affiliation:
Wellcome Trust Centre for Neuroimaging, University College London, London, UK Max Planck-University College London Centre for Computational Psychiatry and Ageing, London, UK
*
*Address for correspondence: Olga Therese Ousdal, M.D. Ph.D., Department of Radiology, Haukeland University Hospital, Jonas Lies vei 65, 5021 Bergen, Norway. (Email: [email protected], [email protected])
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Abstract

Background

Disturbances in Pavlovian valuation systems are reported to follow traumatic stress exposure. However, motivated decisions are also guided by instrumental mechanisms, but to date the effect of traumatic stress on these instrumental systems remain poorly investigated. Here, we examine whether a single episode of severe traumatic stress influences flexible instrumental decisions through an impact on a Pavlovian system.

Methods

Twenty-six survivors of the 2011 Norwegian terror attack and 30 matched control subjects performed an instrumental learning task in which Pavlovian and instrumental associations promoted congruent or conflicting responses. We used reinforcement learning models to infer how traumatic stress affected learning and decision-making. Based on the importance of dorsal anterior cingulate cortex (dACC) for cognitive control, we also investigated if individual concentrations of Glx (=glutamate + glutamine) in dACC predicted the Pavlovian bias of choice.

Results

Survivors of traumatic stress expressed a greater Pavlovian interference with instrumental action selection and had significantly lower levels of Glx in the dACC. Across subjects, the degree of Pavlovian interference was negatively associated with dACC Glx concentrations.

Conclusions

Experiencing traumatic stress appears to render instrumental decisions less flexible by increasing the susceptibility to Pavlovian influences. An observed association between prefrontal glutamatergic levels and this Pavlovian bias provides novel insight into the neurochemical basis of decision-making, and suggests a mechanism by which traumatic stress can impair flexible instrumental behaviours.

Keywords

Decision-makingglutamateinstrumentalPavlovianPTSDstress
Type
Original Articles
Information
Psychological Medicine , Volume 48 , Issue 2 , January 2018 , pp. 327 - 336
Copyright
Copyright © Cambridge University Press 2017 

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Footnotes

†

These two authors contributed equally to this work.

References

Arnsten, AF (2015). Stress weakens prefrontal networks: molecular insults to higher cognition. Nature Neuroscience 18, 1376–1385.Google Scholar
Bellesi, M, Vyazovskiy, VV, Tononi, G, Cirelli, C, Conti, F (2012). Reduction of EEG theta power and changes in motor activity in rats treated with ceftriaxone. PLoS ONE 7, e34139.Google Scholar
Cavanagh, JF, Eisenberg, I, Guitart-Masip, M, Huys, Q, Frank, MJ (2013). Frontal theta overrides pavlovian learning biases. Journal of Neuroscience 33, 8541–8548.Google Scholar
Cavanagh, JF, Frank, MJ (2014). Frontal theta as a mechanism for cognitive control. Trends in Cognitive Sciences 18, 414–421.CrossRefGoogle ScholarPubMed
Cella, M, Dymond, S, Cooper, A (2010). Impaired flexible decision-making in Major Depressive Disorder. Journal of Affective Disorders 124, 207–210.Google Scholar
Dayan, P, Daw, ND (2008). Decision theory, reinforcement learning, and the brain. Cognitive, Affective & Behavioral Neuroscience 8, 429–453.Google Scholar
Dayan, P, Niv, Y, Seymour, B, Daw, ND (2006). The misbehavior of value and the discipline of the will. Neural Networks 19, 1153–1160.Google Scholar
de Berker, AO, Tirole, M, Rutledge, RB, Cross, GF, Dolan, RJ, Bestmann, S (2016). Acute stress selectively impairs learning to act. Scientific Reports 6, 29816.CrossRefGoogle ScholarPubMed
Dias-Ferreira, E, Sousa, JC, Melo, I, Morgado, P, Mesquita, AR, Cerqueira, JJ, Costa, RM, Sousa, N (2009). Chronic stress causes frontostriatal reorganization and affects decision-making. Science 325, 621–625.Google Scholar
Dolan, RJ, Dayan, P (2013). Goals and habits in the brain. Neuron 80, 312–325.Google Scholar
Etkin, A, Egner, T, Kalisch, R (2011). Emotional processing in anterior cingulate and medial prefrontal cortex. Trends in Cognitive Sciences 15, 85–93.Google Scholar
Falkenberg, LE, Westerhausen, R, Specht, K, Hugdahl, K (2012). Resting-state glutamate level in the anterior cingulate predicts blood-oxygen level-dependent response to cognitive control. Proceedings of the National Academy of Sciences of the United States of America 109, 5069–5073.CrossRefGoogle ScholarPubMed
Gallistel, CR, Fairhurst, S, Balsam, P (2004). The learning curve: implications of a quantitative analysis. Proceedings of the National Academy of Sciences of the United States of America 101, 13124–13131.Google Scholar
Gamo, NJ, Lur, G, Higley, MJ, Wang, M, Paspalas, CD, Vijayraghavan, S, Yang, Y, Ramos, BP, Peng, K, Kata, A, Boven, L, Lin, F, Roman, L, Lee, D, Arnsten, AF (2015). Stress impairs prefrontal cortical function via D1 dopamine receptor interactions with hyperpolarization-activated cyclic nucleotide-gated channels. Biological Psychiatry 78, 860–870.Google Scholar
Graybeal, C, Kiselycznyk, C, Holmes, A (2012). Stress-induced deficits in cognition and emotionality: a role of glutamate. Current Topics in Behavioral Neurosciences 12, 189–207.Google Scholar
Guitart-Masip, M, Duzel, E, Dolan, R, Dayan, P (2014a). Action versus valence in decision making. Trends in Cognitive Sciences 18, 194–202.Google Scholar
Guitart-Masip, M, Economides, M, Huys, QJ, Frank, MJ, Chowdhury, R, Duzel, E, Dayan, P, Dolan, RJ (2014b). Differential, but not opponent, effects of L-DOPA and citalopram on action learning with reward and punishment. Psychopharmacology 231, 955–966.Google Scholar
Guitart-Masip, M, Huys, QJ, Fuentemilla, L, Dayan, P, Duzel, E, Dolan, RJ (2012). Go and no-go learning in reward and punishment: interactions between affect and effect. NeuroImage 62, 154–166.Google Scholar
Hollon, NG, Burgeno, LM, Phillips, PE (2015). Stress effects on the neural substrates of motivated behavior. Nature Neuroscience 18, 1405–1412.CrossRefGoogle ScholarPubMed
Huys, QJ, Cools, R, Golzer, M, Friedel, E, Heinz, A, Dolan, RJ, Dayan, P (2011). Disentangling the roles of approach, activation and valence in instrumental and pavlovian responding. PLoS Computational Biology 7, e1002028.Google Scholar
Huys, QJ, Daw, ND, Dayan, P (2015). Depression: a decision-theoretic analysis. Annual Review of Neuroscience 38, 1–23.Google Scholar
Jovanovic, T, Norrholm, SD, Blanding, NQ, Davis, M, Duncan, E, Bradley, B, Ressler, KJ (2010). Impaired fear inhibition is a biomarker of PTSD but not depression. Depression and Anxiety 27, 244–251.Google Scholar
Koolhaas, JM, Bartolomucci, A, Buwalda, B, de Boer, SF, Flugge, G, Korte, SM, Meerlo, P, Murison, R, Olivier, B, Palanza, P, Richter-Levin, G, Sgoifo, A, Steimer, T, Stiedl, O, van Dijk, G, Wohr, M, Fuchs, E (2011). Stress revisited: a critical evaluation of the stress concept. Neuroscience and Biobehavioral Reviews 35, 1291–1301.Google Scholar
Mansouri, FA, Egner, T, Buckley, MJ (2017). Monitoring demands for executive control: shared functions between human and nonhuman primates. Trends in Neurosciences 40, 15–27.Google Scholar
McEwen, BS, Bowles, NP, Gray, JD, Hill, MN, Hunter, RG, Karatsoreos, IN, Nasca, C (2015). Mechanisms of stress in the brain. Nature Neuroscience 18, 1353–1363.Google Scholar
Milad, MR, Pitman, RK, Ellis, CB, Gold, AL, Shin, LM, Lasko, NB, Zeidan, MA, Handwerger, K, Orr, SP, Rauch, SL (2009). Neurobiological basis of failure to recall extinction memory in posttraumatic stress disorder. Biological Psychiatry 66, 1075–1082.Google Scholar
North, CS, Nixon, SJ, Shariat, S, Mallonee, S, McMillen, JC, Spitznagel, EL, Smith, EM (1999). Psychiatric disorders among survivors of the Oklahoma City bombing. JAMA 282, 755–762.CrossRefGoogle ScholarPubMed
North, CS, Pfefferbaum, B (2013). Mental health response to community disasters: a systematic review. JAMA 310, 507–518.Google Scholar
Pitman, RK, Rasmusson, AM, Koenen, KC, Shin, LM, Orr, SP, Gilbertson, MW, Milad, MR, Liberzon, I (2012). Biological studies of post-traumatic stress disorder. Nature Reviews Neuroscience 13, 769–787.Google Scholar
Popoli, M, Yan, Z, McEwen, BS, Sanacora, G (2012). The stressed synapse: the impact of stress and glucocorticoids on glutamate transmission. Nature Reviews Neuroscience 13, 22–37.Google Scholar
Provencher, SW (1993). Estimation of metabolite concentrations from localized in vivo proton NMR spectra. Magnetic Resonance in Medicine 30, 672–679.Google Scholar
Schwabe, L, Wolf, OT (2009). Stress prompts habit behavior in humans. Journal of Neuroscience: the Official Journal of the Society for Neuroscience 29, 7191–7198.CrossRefGoogle ScholarPubMed
Schwabe, L, Wolf, OT (2013). Stress and multiple memory systems: from ‘thinking’ to ‘doing’. Trends in Cognitive Sciences 17, 60–68.Google Scholar
Sebold, M, Deserno, L, Nebe, S, Schad, DJ, Garbusow, M, Hagele, C, Keller, J, Junger, E, Kathmann, N, Smolka, M, Rapp, MA, Schlagenhauf, F, Heinz, A, Huys, QJ (2014). Model-based and model-free decisions in alcohol dependence. Neuropsychobiology 70, 122–131.Google Scholar
Sheehan, D, Janavs, J, Harnett-Sheehan, K, Sheehan, M, Gray, C, Lecrubier, Y, Weiller, E, Hergueta, T, Allgulander, C, Kadri, N, Baldwin, D, Even, C (2009). M.I.N.I.: Mini International Neuropsychiatric Interview, Norwegian version 6.0.0 (DSM-IV).Google Scholar
Silvetti, M, Alexander, W, Verguts, T, Brown, JW (2014). From conflict management to reward-based decision making: actors and critics in primate medial frontal cortex. Neuroscience and Biobehavioral Reviews 46(Pt 1), 44–57.Google Scholar
Van Veen, V, Carter, CS (2002). The timing of action-monitoring processes in the anterior cingulate cortex. Journal of Cognitive Neuroscience 14, 593–602.Google Scholar
Yang, ZY, Quan, H, Peng, ZL, Zhong, Y, Tan, ZJ, Gong, QY (2015). Proton magnetic resonance spectroscopy revealed differences in the glutamate+glutamine/creatine ratio of the anterior cingulate cortex between healthy and pediatric post-traumatic stress disorder patients diagnosed after 2008 Wenchuan earthquake. Psychiatry and Clinical Neurosciences 69, 782–790.CrossRefGoogle ScholarPubMed
Yuan, TF, Hou, G (2015). The effects of stress on glutamatergic transmission in the brain. Molecular Neurobiology 51, 1139–1143.Google Scholar
Yuen, EY, Wei, J, Liu, W, Zhong, P, Li, X, Yan, Z (2012). Repeated stress causes cognitive impairment by suppressing glutamate receptor expression and function in prefrontal cortex. Neuron 73, 962–977.Google Scholar
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