title: Cognitive emotion regulation modulates the balance of competing influences on ventral striatal aversive prediction error signals.
abstract: Cognitive emotion regulation (CER) is a critical human ability to face aversive emotional stimuli in a flexible way, via recruitment of specific prefrontal brain circuits. Animal research reveals a central role of ventral striatum in emotional behavior, for both aversive conditioning, with striatum signaling aversive prediction errors (aPE), and for integrating competing influences of distinct striatal inputs from regions such as the prefrontal cortex (PFC), amygdala, hippocampus and ventral tegmental area (VTA). Translating these ventral striatal findings from animal research to human CER, we hypothesized that successful CER would affect the balance of competing influences of striatal afferents on striatal aPE signals, in a way favoring PFC as opposed to 'subcortical' (i.e., non-isocortical) striatal inputs. Using aversive Pavlovian conditioning with and without CER during fMRI, we found that during CER, superior regulators indeed reduced the modulatory impact of 'subcortical' striatal afferents (hippocampus, amygdala and VTA) on ventral striatal aPE signals, while keeping the PFC impact intact. In contrast, inferior regulators showed an opposite pattern. Our results demonstrate that ventral striatal aPE signals and associated competing modulatory inputs are critical mechanisms underlying successful cognitive regulation of aversive emotions in humans.
authors.affiliation: Klinikum rechts der Isar, Technische Universität München, Department of Neuroradiology, Munich 81675, Germany; Klinikum rechts der Isar, Technische Universität München, TUM-NIC Neuroimaging Center, Munich 81675, Germany; Ludwig-Maximilians-Universität München, Graduate School of Systemic Neurosciences, Planegg-Martinsried 82152, Germany.
authors.forename: Satja
authors.initials: S
authors.lastname: Mulej Bratec
authors.affiliation: Klinikum rechts der Isar, Technische Universität München, Department of Neuroradiology, Munich 81675, Germany; Klinikum rechts der Isar, Technische Universität München, TUM-NIC Neuroimaging Center, Munich 81675, Germany; Ludwig-Maximilians-Universität München, Department of Psychology, Munich 80802, Germany.
authors.forename: Xiyao
authors.initials: X
authors.lastname: Xie
authors.affiliation: Klinikum rechts der Isar, Technische Universität München, TUM-NIC Neuroimaging Center, Munich 81675, Germany; Duke-NUS Graduate Medical School Singapore, Singapore 169857, Singapore.
authors.forename: Yijun
authors.initials: Y
authors.lastname: Wang
authors.affiliation: Max Planck Institute of Psychiatry, Independent Max Planck Research Group Social Neuroscience, Munich 80804, Germany; University Hospital of Cologne, Department of Psychiatry, Cologne 50924, Germany.
authors.forename: Leonhard
authors.initials: L
authors.lastname: Schilbach
authors.affiliation: Klinikum rechts der Isar, Technische Universität München, Department of Neuroradiology, Munich 81675, Germany.
authors.forename: Claus
authors.initials: C
authors.lastname: Zimmer
authors.affiliation: Klinikum rechts der Isar, Technische Universität München, Department of Neuroradiology, Munich 81675, Germany; Klinikum rechts der Isar, Technische Universität München, TUM-NIC Neuroimaging Center, Munich 81675, Germany.
authors.forename: Afra M
authors.initials: AM
authors.lastname: Wohlschläger
authors.affiliation: Klinikum rechts der Isar, Technische Universität München, Department of Neuroradiology, Munich 81675, Germany; Klinikum rechts der Isar, Technische Universität München, TUM-NIC Neuroimaging Center, Munich 81675, Germany; Klinikum rechts der Isar, Technische Universität München, Department of Nuclear Medicine, Munich 81675, Germany.
authors.forename: Valentin
authors.initials: V
authors.lastname: Riedl
authors.affiliation: Klinikum rechts der Isar, Technische Universität München, Department of Neuroradiology, Munich 81675, Germany; Klinikum rechts der Isar, Technische Universität München, TUM-NIC Neuroimaging Center, Munich 81675, Germany; Klinikum rechts der Isar, Technische Universität München, Department of Psychiatry, Munich 81675, Germany. Electronic address: christian.sorg@tum.de.
authors.forename: Christian
authors.initials: C
authors.lastname: Sorg
mesh_terms: D000328:Adult; D000679:Amygdala / Q000000981:diagnostic imaging / Q000502:physiology*; D001931:Brain Mapping / Q000379:methods*; D003214:Conditioning, Classical / Q000502:physiology; D004644:Emotions / Q000502:physiology*; D056344:Executive Function / Q000502:physiology*; D005260:Female; D006624:Hippocampus / Q000000981:diagnostic imaging / Q000502:physiology*; D006801:Humans; D008279:Magnetic Resonance Imaging; D017397:Prefrontal Cortex / Q000000981:diagnostic imaging / Q000502:physiology*; D000068356:Self-Control; D066328:Ventral Striatum / Q000000981:diagnostic imaging / Q000502:physiology*; D055815:Young Adult
keywords: Aversive prediction error; Emotion regulation; Functional connectivity; Reappraisal ability; Ventral striatum; fMRI