Oxytocin differentially alters resting state functional connectivity between amygdala subregions and emotional control networks: Inverse correlation with depressive traits

Monika Eckstein; Sebastian Markett; Keith M Kendrick; Beate Ditzen; Fang Liu; Rene Hurlemann; Benjamin Becker

doi:10.1016/j.neuroimage.2017.01.078

Oxytocin differentially alters resting state functional connectivity between amygdala subregions and emotional control networks: Inverse correlation with depressive traits

Neuroimage. 2017 Apr 1:149:458-467. doi: 10.1016/j.neuroimage.2017.01.078. Epub 2017 Feb 1.

Authors

Monika Eckstein¹, Sebastian Markett², Keith M Kendrick³, Beate Ditzen¹, Fang Liu⁴, Rene Hurlemann⁵, Benjamin Becker⁶

Affiliations

¹ Institute of Medical Psychology, Center for Psychosocial Medicine, University Hospital Heidelberg, D-69115 Heidelberg, Germany.
² Department of Psychology, University of Bonn, D-53127 Bonn, Germany; Center for Economics and Neuroscience, University of Bonn, D-53127 Bonn, Germany.
³ Key Laboratory for NeuroInformation of Ministry of Education, Center for Information in Medicine, University of Electronic Science and Technology of China, Chengdu, Sichuan 611731, China.
⁴ Department of Radiology, University of Wisconsin-Madison, Madison, WI 53705-2275, USA.
⁵ Department of Psychiatry and Division of Medical Psychology, University of Bonn, D-53127 Bonn, Germany.
⁶ Key Laboratory for NeuroInformation of Ministry of Education, Center for Information in Medicine, University of Electronic Science and Technology of China, Chengdu, Sichuan 611731, China. Electronic address: ben_becker@gmx.de.

PMID: 28161309
DOI: 10.1016/j.neuroimage.2017.01.078

Abstract

The hypothalamic neuropeptide oxytocin (OT) has received increasing attention for its role in modulating social-emotional processes across species. Previous studies on using intranasal-OT in humans point to a crucial engagement of the amygdala in the observed neuromodulatory effects of OT under task and rest conditions. However, the amygdala is not a single homogenous structure, but rather a set of structurally and functionally heterogeneous nuclei that show distinct patterns of connectivity with limbic and frontal emotion-processing regions. To determine potential differential effects of OT on functional connectivity of the amygdala subregions, 79 male participants underwent resting-state fMRI following randomized intranasal-OT or placebo administration. In line with previous studies OT increased the connectivity of the total amygdala with dorso-medial prefrontal regions engaged in emotion regulation. In addition, OT enhanced coupling of the total amygdala with cerebellar regions. Importantly, OT differentially altered the connectivity of amygdala subregions with distinct up-stream cortical nodes, particularly prefrontal/parietal, and cerebellar down-stream regions. OT-induced increased connectivity with cerebellar regions were largely driven by effects on the centromedial and basolateral subregions, whereas increased connectivity with prefrontal regions were largely mediated by right superficial and basolateral subregions. OT decreased connectivity of the centromedial subregions with core hubs of the emotional face processing network in temporal, occipital and parietal regions. Preliminary findings suggest that effects on the superficial amygdala-prefrontal pathway were inversely associated with levels of subclinical depression, possibly indicating that OT modulation may be blunted in the context of increased pathological load. Together, the present findings suggest a subregional-specific modulatory role of OT on amygdala-centered emotion processing networks in humans.

Keywords: Basolateral amygdala; Centromedial amygdala; Emotion; Oxytocin; Superficial amygdala.

Publication types

Randomized Controlled Trial
Research Support, Non-U.S. Gov't

MeSH terms

Administration, Intranasal
Adult
Amygdala / drug effects*
Depression / physiopathology
Emotions / drug effects*
Humans
Image Interpretation, Computer-Assisted
Magnetic Resonance Imaging
Male
Neural Pathways / drug effects
Oxytocics / pharmacology*
Oxytocin / pharmacology*
Rest
Young Adult

Substances

Oxytocics
Oxytocin