Mu-opioid receptor system modulates responses to vocal bonding and distress signals in humans

Author:

Sun Lihua12ORCID,Lukkarinen Lasse234,Putkinen Vesa2,Karlsson Henry K.2,Hirvonen Jussi5,Tiihonen Jari67,Lauerma Hannu34,Scott Sophie8ORCID,Nummenmaa Lauri29ORCID

Affiliation:

1. Department of Nuclear Medicine, Huashan Hospital, Fudan University, Shanghai, People’s Republic of China

2. Turku PET Centre, University of Turku, and Turku University Hospital, Turku, Finland

3. Department of Psychiatry, University of Turku, and Turku University Hospital, Turku, Finland

4. Psychiatric Hospital for Prisoners, Health Care Services for Prisoners, Turku, Finland

5. Department of Radiology, University of Turku, and Turku University Hospital, Turku, Finland

6. Department of Clinical Neuroscience, Karolinska Institute and Center for Psychiatry Research, Stockholm City Council, Stockholm, Sweden

7. Department of Forensic Psychiatry, University of Eastern Finland and Niuvanniemi Hospital, Kuopio, Finland

8. Institute of Cognitive Neuroscience, University College London, London, UK

9. Department of Psychology, University of Turku, Turku, Finland

Abstract

Laughter is a contagious prosocial signal that conveys bonding motivation; adult crying conversely communicates desire for social proximity by signalling distress. Endogenous mu-opioid receptors (MORs) modulate sociability in humans and non-human primates. In this combined PET–fMRI study ( n = 17), we tested whether central MOR tone is associated with regional brain responses to social signals of laughter and crying. MOR availability was measured with positron emission tomography (PET) using the high-affinity agonist radioligand [ 11 C]carfentanil. Haemodynamic responses to social laughter and crying vocalizations were measured using functional magnetic resonance imaging (fMRI). Social laughter evoked activation in the auditory cortex, insula, cingulate cortex, amygdala, primary and secondary somatosensory cortex, and primary and secondary motor cortex; crying sounds led to more restricted activation in the auditory cortex and nearby areas. MOR availability was negatively correlated with the haemodynamic responses to social laughter in the primary and secondary somatosensory cortex, primary and secondary motor cortex, posterior insula, posterior cingulate cortex, precuneus, cuneus, temporal gyri and lingual gyrus. For crying-evoked activations, MOR availability was negatively correlated with medial and lateral prefrontal haemodynamic responses. Altogether our findings highlight the role of the MOR system in modulating acute brain responses to both positive and negative social signals. This article is part of the theme issue ‘Cracking the laugh code: laughter through the lens of biology, psychology and neuroscience’.

Funder

Academy of Finland

Publisher

The Royal Society

Subject

General Agricultural and Biological Sciences,General Biochemistry, Genetics and Molecular Biology

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