Early life stress modulates oxytocin effects on limbic system during acute psychosocial stress

Simone Grimm; Karin Pestke; Melanie Feeser; Sabine Aust; Anne Weigand; Jue Wang; Katja Wingenfeld; Jens C Pruessner; Roberto La Marca; Heinz Böker; Malek Bajbouj

doi:10.1093/scan/nsu020

Early life stress modulates oxytocin effects on limbic system during acute psychosocial stress

Soc Cogn Affect Neurosci. 2014 Nov;9(11):1828-35. doi: 10.1093/scan/nsu020. Epub 2014 Jan 28.

Authors

Affiliations

¹ Cluster of Excellence 'Languages of Emotion', Freie Universitaet Berlin, 14195 Berlin, Germany, Department of Psychiatry, Campus Benjamin Franklin, Charité Berlin, 14050 Berlin, Germany, Dahlem Institute for Neuroimaging of Emotion, Freie Universitaet Berlin, 14195 Berlin, Germany, Clinic for Affective Disorders and General Psychiatry, Psychiatric University Hospital Zurich, 8032 Zurich, Switzerland, Center for Cognition and Brain Disorders and the Affiliated Hospital, Hangzhou Normal University, Hangzhou 310015, China, Douglas Mental Health Institute, Department of Psychiatry, McGill University, Montreal, Quebec H4H 1R3, Canada, Montreal Neurological Institute, McGill University, Montreal, Quebec H4H 1R3, Canada, and University of Zurich, Institute of Psychology, Department of Psychology Clinical Psychology and Psychotherapy, 8050 Zurich, Switzerland Cluster of Excellence 'Languages of Emotion', Freie Universitaet Berlin, 14195 Berlin, Germany, Department of Psychiatry, Campus Benjamin Franklin, Charité Berlin, 14050 Berlin, Germany, Dahlem Institute for Neuroimaging of Emotion, Freie Universitaet Berlin, 14195 Berlin, Germany, Clinic for Affective Disorders and General Psychiatry, Psychiatric University Hospital Zurich, 8032 Zurich, Switzerland, Center for Cognition and Brain Disorders and the Affiliated Hospital, Hangzhou Normal University, Hangzhou 310015, China, Douglas Mental Health Institute, Department of Psychiatry, McGill University, Montreal, Quebec H4H 1R3, Canada, Montreal Neurological Institute, McGill University, Montreal, Quebec H4H 1R3, Canada, and University of Zurich, Institute of Psychology, Department of Psychology Clinical Psychology and Psychotherapy, 8050 Zurich, Switzerland Cluster of Excellence 'Languages of Emotion', Freie Universitaet Berlin, 14195 Berlin, Germany, Department of Psychiatry, Campus Benjamin Franklin, Charité Berlin, 14050 Berlin, Germany, Dahlem Institute for Neuroimaging of Emotion, Freie Universitaet Berlin, 14195 Ber
² Cluster of Excellence 'Languages of Emotion', Freie Universitaet Berlin, 14195 Berlin, Germany, Department of Psychiatry, Campus Benjamin Franklin, Charité Berlin, 14050 Berlin, Germany, Dahlem Institute for Neuroimaging of Emotion, Freie Universitaet Berlin, 14195 Berlin, Germany, Clinic for Affective Disorders and General Psychiatry, Psychiatric University Hospital Zurich, 8032 Zurich, Switzerland, Center for Cognition and Brain Disorders and the Affiliated Hospital, Hangzhou Normal University, Hangzhou 310015, China, Douglas Mental Health Institute, Department of Psychiatry, McGill University, Montreal, Quebec H4H 1R3, Canada, Montreal Neurological Institute, McGill University, Montreal, Quebec H4H 1R3, Canada, and University of Zurich, Institute of Psychology, Department of Psychology Clinical Psychology and Psychotherapy, 8050 Zurich, Switzerland Cluster of Excellence 'Languages of Emotion', Freie Universitaet Berlin, 14195 Berlin, Germany, Department of Psychiatry, Campus Benjamin Franklin, Charité Berlin, 14050 Berlin, Germany, Dahlem Institute for Neuroimaging of Emotion, Freie Universitaet Berlin, 14195 Berlin, Germany, Clinic for Affective Disorders and General Psychiatry, Psychiatric University Hospital Zurich, 8032 Zurich, Switzerland, Center for Cognition and Brain Disorders and the Affiliated Hospital, Hangzhou Normal University, Hangzhou 310015, China, Douglas Mental Health Institute, Department of Psychiatry, McGill University, Montreal, Quebec H4H 1R3, Canada, Montreal Neurological Institute, McGill University, Montreal, Quebec H4H 1R3, Canada, and University of Zurich, Institute of Psychology, Department of Psychology Clinical Psychology and Psychotherapy, 8050 Zurich, Switzerland.
³ Cluster of Excellence 'Languages of Emotion', Freie Universitaet Berlin, 14195 Berlin, Germany, Department of Psychiatry, Campus Benjamin Franklin, Charité Berlin, 14050 Berlin, Germany, Dahlem Institute for Neuroimaging of Emotion, Freie Universitaet Berlin, 14195 Berlin, Germany, Clinic for Affective Disorders and General Psychiatry, Psychiatric University Hospital Zurich, 8032 Zurich, Switzerland, Center for Cognition and Brain Disorders and the Affiliated Hospital, Hangzhou Normal University, Hangzhou 310015, China, Douglas Mental Health Institute, Department of Psychiatry, McGill University, Montreal, Quebec H4H 1R3, Canada, Montreal Neurological Institute, McGill University, Montreal, Quebec H4H 1R3, Canada, and University of Zurich, Institute of Psychology, Department of Psychology Clinical Psychology and Psychotherapy, 8050 Zurich, Switzerland.

Abstract

Early life stress (ELS) is associated with altered stress responsivity, structural and functional brain changes and an increased risk for the development of psychopathological conditions in later life. Due to its behavioral and physiological effects, the neuropeptide oxytocin (OXT) is a useful tool to investigate stress responsivity, even though the neurobiological underpinnings of its effects are still unknown. Here we investigate the effects of OXT on cortisol stress response and neural activity during psychosocial stress. Using functional magnetic resonance imaging in healthy subjects with and without a history of ELS, we found attenuated hormonal reactivity and significantly reduced limbic deactivation after OXT administration in subjects without a history of ELS. Subjects who experienced ELS showed both blunted stress reactivity and limbic deactivation during stress. Furthermore, in these subjects OXT had opposite effects with increased hormonal reactivity and increased limbic deactivation. Our results might implicate that reduced limbic deactivation and hypothalamic-pituitary-adrenal axis responsivity during psychosocial stress are markers for biological resilience after ELS. Effects of OXT in subjects with a history of maltreatment could therefore be considered detrimental and suggest careful consideration of OXT administration in such individuals.

Keywords: early life stress; oxytocin; stress.

Publication types

Pragmatic Clinical Trial
Research Support, Non-U.S. Gov't

MeSH terms

Adult
Analysis of Variance
Child
Child Abuse / psychology*
Double-Blind Method
Female
Humans
Hydrocortisone / blood
Image Processing, Computer-Assisted
Limbic System / blood supply
Limbic System / drug effects*
Limbic System / pathology*
Magnetic Resonance Imaging
Male
Oxygen / blood
Oxytocin / administration & dosage*
Psychiatric Status Rating Scales
Psychological Tests
Saliva / metabolism
Stress, Psychological / blood
Stress, Psychological / pathology*
Young Adult

Substances

Oxytocin
Oxygen
Hydrocortisone