Asymmetric representation of aversive prediction errors in Pavlovian threat conditioning
Karita E. Ojala,
Athina Tzovara,
Benedikt A. Poser,
Antoine Lutti,
Dominik R. Bach
Affiliations
Karita E. Ojala
Computational Psychiatry Research, Department of Psychiatry, Psychotherapy and Psychosomatics, Psychiatric Hospital, University of Zurich, Lenggstrasse 31, Zurich 8032, Switzerland; Neuroscience Centre Zurich, University of Zurich, Winterthurerstrasse 190, Zürich 8057, Switzerland; Corresponding authors at: Department of Psychiatry, Computational Psychiatry Research, Psychotherapy and Psychosomatics, Psychiatric Hospital, University of Zurich, Lenggstrasse 31, Zurich 8032, Switzerland.
Athina Tzovara
Computational Psychiatry Research, Department of Psychiatry, Psychotherapy and Psychosomatics, Psychiatric Hospital, University of Zurich, Lenggstrasse 31, Zurich 8032, Switzerland; Neuroscience Centre Zurich, University of Zurich, Winterthurerstrasse 190, Zürich 8057, Switzerland; Institute of Computer Science, University of Bern, Neubrückstrasse 10, Bern 3012, Switzerland
Benedikt A. Poser
Department of Cognitive Neuroscience, Faculty of Psychology and Neuroscience, Maastricht University, Oxfordlaan 55 EV 6299, Maastricht, the Netherlands
Antoine Lutti
Laboratory for Research in Neuroimaging, Department of Clinical Neuroscience, Lausanne University Hospital and University of Lausanne, Chemin de Mont-Paisible 16, Lausanne 1011, Switzerland
Dominik R. Bach
Computational Psychiatry Research, Department of Psychiatry, Psychotherapy and Psychosomatics, Psychiatric Hospital, University of Zurich, Lenggstrasse 31, Zurich 8032, Switzerland; Neuroscience Centre Zurich, University of Zurich, Winterthurerstrasse 190, Zürich 8057, Switzerland; Wellcome Centre for Human Neuroimaging and Max-Planck UCL Centre for Computational Psychiatry and Ageing Research, University College London, 10-12 Russell Square, London WC1B 5EH, United Kingdom; Corresponding authors at: Department of Psychiatry, Computational Psychiatry Research, Psychotherapy and Psychosomatics, Psychiatric Hospital, University of Zurich, Lenggstrasse 31, Zurich 8032, Switzerland.
Survival in biological environments requires learning associations between predictive sensory cues and threatening outcomes. Such aversive learning may be implemented through reinforcement learning algorithms that are driven by the signed difference between expected and encountered outcomes, termed prediction errors (PEs). While PE-based learning is well established for reward learning, the role of putative PE signals in aversive learning is less clear. Here, we used functional magnetic resonance imaging in humans (21 healthy men and women) to investigate the neural representation of PEs during maintenance of learned aversive associations. Four visual cues, each with a different probability (0, 33, 66, 100%) of being followed by an aversive outcome (electric shock), were repeatedly presented to participants. We found that neural activity at omission (US-) but not occurrence of the aversive outcome (US+) encoded PEs in the medial prefrontal cortex. More expected omission of aversive outcome was associated with lower neural activity. No neural signals fulfilled axiomatic criteria, which specify necessary and sufficient components of PE signals, for signed PE representation in a whole-brain search or in a-priori regions of interest. Our results might suggest that, different from reward learning, aversive learning does not involve signed PE signals that are represented within the same brain region for all conditions.
