Skip to main content

The impact of traumatic stress on Pavlovian biases

  • O. T. Ousdal (a1) (a2), Q. J. Huys (a3) (a4), A. M. Milde (a5) (a6), A. R. Craven (a5) (a7), L. Ersland (a8), T. Endestad (a9), A. Melinder (a9), K. Hugdahl (a1) (a5) (a7) (a10) (a11) and R. J. Dolan (a2) (a12)...

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.


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.


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.


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.

Corresponding author
*Address for correspondence: Olga Therese Ousdal, M.D. Ph.D., Department of Radiology, Haukeland University Hospital, Jonas Lies vei 65, 5021 Bergen, Norway. (Email:,
Hide All

These two authors contributed equally to this work.

Hide All
Arnsten, AF (2015). Stress weakens prefrontal networks: molecular insults to higher cognition. Nature Neuroscience 18, 13761385.
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.
Cavanagh, JF, Eisenberg, I, Guitart-Masip, M, Huys, Q, Frank, MJ (2013). Frontal theta overrides pavlovian learning biases. Journal of Neuroscience 33, 85418548.
Cavanagh, JF, Frank, MJ (2014). Frontal theta as a mechanism for cognitive control. Trends in Cognitive Sciences 18, 414421.
Cella, M, Dymond, S, Cooper, A (2010). Impaired flexible decision-making in Major Depressive Disorder. Journal of Affective Disorders 124, 207210.
Dayan, P, Daw, ND (2008). Decision theory, reinforcement learning, and the brain. Cognitive, Affective & Behavioral Neuroscience 8, 429453.
Dayan, P, Niv, Y, Seymour, B, Daw, ND (2006). The misbehavior of value and the discipline of the will. Neural Networks 19, 11531160.
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.
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, 621625.
Dolan, RJ, Dayan, P (2013). Goals and habits in the brain. Neuron 80, 312325.
Etkin, A, Egner, T, Kalisch, R (2011). Emotional processing in anterior cingulate and medial prefrontal cortex. Trends in Cognitive Sciences 15, 8593.
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, 50695073.
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, 1312413131.
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, 860870.
Graybeal, C, Kiselycznyk, C, Holmes, A (2012). Stress-induced deficits in cognition and emotionality: a role of glutamate. Current Topics in Behavioral Neurosciences 12, 189207.
Guitart-Masip, M, Duzel, E, Dolan, R, Dayan, P (2014a). Action versus valence in decision making. Trends in Cognitive Sciences 18, 194202.
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, 955966.
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, 154166.
Hollon, NG, Burgeno, LM, Phillips, PE (2015). Stress effects on the neural substrates of motivated behavior. Nature Neuroscience 18, 14051412.
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.
Huys, QJ, Daw, ND, Dayan, P (2015). Depression: a decision-theoretic analysis. Annual Review of Neuroscience 38, 123.
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, 244251.
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, 12911301.
Mansouri, FA, Egner, T, Buckley, MJ (2017). Monitoring demands for executive control: shared functions between human and nonhuman primates. Trends in Neurosciences 40, 1527.
McEwen, BS, Bowles, NP, Gray, JD, Hill, MN, Hunter, RG, Karatsoreos, IN, Nasca, C (2015). Mechanisms of stress in the brain. Nature Neuroscience 18, 13531363.
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, 10751082.
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, 755762.
North, CS, Pfefferbaum, B (2013). Mental health response to community disasters: a systematic review. JAMA 310, 507518.
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, 769787.
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, 2237.
Provencher, SW (1993). Estimation of metabolite concentrations from localized in vivo proton NMR spectra. Magnetic Resonance in Medicine 30, 672679.
Schwabe, L, Wolf, OT (2009). Stress prompts habit behavior in humans. Journal of Neuroscience: the Official Journal of the Society for Neuroscience 29, 71917198.
Schwabe, L, Wolf, OT (2013). Stress and multiple memory systems: from ‘thinking’ to ‘doing’. Trends in Cognitive Sciences 17, 6068.
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, 122131.
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).
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), 4457.
Van Veen, V, Carter, CS (2002). The timing of action-monitoring processes in the anterior cingulate cortex. Journal of Cognitive Neuroscience 14, 593602.
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, 782790.
Yuan, TF, Hou, G (2015). The effects of stress on glutamatergic transmission in the brain. Molecular Neurobiology 51, 11391143.
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, 962977.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Psychological Medicine
  • ISSN: 0033-2917
  • EISSN: 1469-8978
  • URL: /core/journals/psychological-medicine
Please enter your name
Please enter a valid email address
Who would you like to send this to? *


Type Description Title
Supplementary materials

Ousdal supplementary material
Ousdal supplementary material 1

 Word (4.8 MB)
4.8 MB


Altmetric attention score

Full text views

Total number of HTML views: 41
Total number of PDF views: 263 *
Loading metrics...

Abstract views

Total abstract views: 863 *
Loading metrics...

* Views captured on Cambridge Core between 23rd June 2017 - 25th September 2018. This data will be updated every 24 hours.