Decoding brain basis of laughter and crying in natural scenes

Laughter and crying are universal signals of prosociality and distress, respectively. Here we investigated the functional brain basis of perceiving laughter and crying using naturalistic functional magnetic resonance imaging (fMRI) approach. We measured haemodynamic brain activity evoked by laughter...

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Main Authors: Lauri Nummenmaa, Tuulia Malèn, Sanaz Nazari-Farsani, Kerttu Seppälä, Lihua Sun, Severi Santavirta, Henry K. Karlsson, Matthew Hudson, Jussi Hirvonen, Mikko Sams, Sophie Scott, Vesa Putkinen
Format: Article
Language:English
Published: Elsevier 2023-06-01
Series:NeuroImage
Online Access:http://www.sciencedirect.com/science/article/pii/S1053811923002288
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author Lauri Nummenmaa
Tuulia Malèn
Sanaz Nazari-Farsani
Kerttu Seppälä
Lihua Sun
Severi Santavirta
Henry K. Karlsson
Matthew Hudson
Jussi Hirvonen
Mikko Sams
Sophie Scott
Vesa Putkinen
author_facet Lauri Nummenmaa
Tuulia Malèn
Sanaz Nazari-Farsani
Kerttu Seppälä
Lihua Sun
Severi Santavirta
Henry K. Karlsson
Matthew Hudson
Jussi Hirvonen
Mikko Sams
Sophie Scott
Vesa Putkinen
author_sort Lauri Nummenmaa
collection DOAJ
description Laughter and crying are universal signals of prosociality and distress, respectively. Here we investigated the functional brain basis of perceiving laughter and crying using naturalistic functional magnetic resonance imaging (fMRI) approach. We measured haemodynamic brain activity evoked by laughter and crying in three experiments with 100 subjects in each. The subjects i) viewed a 20-minute medley of short video clips, and ii) 30 min of a full-length feature film, and iii) listened to 13.5 min of a radio play that all contained bursts of laughter and crying. Intensity of laughing and crying in the videos and radio play was annotated by independent observes, and the resulting time series were used to predict hemodynamic activity to laughter and crying episodes. Multivariate pattern analysis (MVPA) was used to test for regional selectivity in laughter and crying evoked activations. Laughter induced widespread activity in ventral visual cortex and superior and middle temporal and motor cortices. Crying activated thalamus, cingulate cortex along the anterior-posterior axis, insula and orbitofrontal cortex. Both laughter and crying could be decoded accurately (66–77% depending on the experiment) from the BOLD signal, and the voxels contributing most significantly to classification were in superior temporal cortex. These results suggest that perceiving laughter and crying engage distinct neural networks, whose activity suppresses each other to manage appropriate behavioral responses to others’ bonding and distress signals.
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spelling doaj.art-fd1a649c16464b73a50a28a6cb8590402023-04-29T14:47:11ZengElsevierNeuroImage1095-95722023-06-01273120082Decoding brain basis of laughter and crying in natural scenesLauri Nummenmaa0Tuulia Malèn1Sanaz Nazari-Farsani2Kerttu Seppälä3Lihua Sun4Severi Santavirta5Henry K. Karlsson6Matthew Hudson7Jussi Hirvonen8Mikko Sams9Sophie Scott10Vesa Putkinen11Turku PET Centre, University of Turku, Finland; Turku University Hospital, University of Turku, Finland; Department of Psychology, University of Turku, Finland; Corresponding author.Turku PET Centre, University of Turku, Finland; Turku University Hospital, University of Turku, FinlandTurku PET Centre, University of Turku, Finland; Turku University Hospital, University of Turku, FinlandTurku PET Centre, University of Turku, Finland; Turku University Hospital, University of Turku, Finland; Department of Medical Physics, Turku University Hospital, University of Turku, FinlandTurku PET Centre, University of Turku, Finland; Turku University Hospital, University of Turku, FinlandTurku PET Centre, University of Turku, Finland; Turku University Hospital, University of Turku, FinlandTurku PET Centre, University of Turku, Finland; Turku University Hospital, University of Turku, FinlandTurku PET Centre, University of Turku, Finland; Turku University Hospital, University of Turku, Finland; School of Psychology, University of Plymouth, Plymouth, UK; Brain Research & Imaging Centre, Faculty of Health, University of Plymouth, Plymouth, UKDepartment of Radiology, University of Turku and Turku University Hospital, Turku, Finland; Medical Imaging Center, Department of Radiology, Tampere University and Tampere University Hospital, Tampere, FinlandDepartment of Biomedical Engineering and Computational Science, Aalto University, FinlandInstitute of Cognitive Neuroscience, University College London, United KingdomTurku PET Centre, University of Turku, Finland; Turku University Hospital, University of Turku, FinlandLaughter and crying are universal signals of prosociality and distress, respectively. Here we investigated the functional brain basis of perceiving laughter and crying using naturalistic functional magnetic resonance imaging (fMRI) approach. We measured haemodynamic brain activity evoked by laughter and crying in three experiments with 100 subjects in each. The subjects i) viewed a 20-minute medley of short video clips, and ii) 30 min of a full-length feature film, and iii) listened to 13.5 min of a radio play that all contained bursts of laughter and crying. Intensity of laughing and crying in the videos and radio play was annotated by independent observes, and the resulting time series were used to predict hemodynamic activity to laughter and crying episodes. Multivariate pattern analysis (MVPA) was used to test for regional selectivity in laughter and crying evoked activations. Laughter induced widespread activity in ventral visual cortex and superior and middle temporal and motor cortices. Crying activated thalamus, cingulate cortex along the anterior-posterior axis, insula and orbitofrontal cortex. Both laughter and crying could be decoded accurately (66–77% depending on the experiment) from the BOLD signal, and the voxels contributing most significantly to classification were in superior temporal cortex. These results suggest that perceiving laughter and crying engage distinct neural networks, whose activity suppresses each other to manage appropriate behavioral responses to others’ bonding and distress signals.http://www.sciencedirect.com/science/article/pii/S1053811923002288
spellingShingle Lauri Nummenmaa
Tuulia Malèn
Sanaz Nazari-Farsani
Kerttu Seppälä
Lihua Sun
Severi Santavirta
Henry K. Karlsson
Matthew Hudson
Jussi Hirvonen
Mikko Sams
Sophie Scott
Vesa Putkinen
Decoding brain basis of laughter and crying in natural scenes
NeuroImage
title Decoding brain basis of laughter and crying in natural scenes
title_full Decoding brain basis of laughter and crying in natural scenes
title_fullStr Decoding brain basis of laughter and crying in natural scenes
title_full_unstemmed Decoding brain basis of laughter and crying in natural scenes
title_short Decoding brain basis of laughter and crying in natural scenes
title_sort decoding brain basis of laughter and crying in natural scenes
url http://www.sciencedirect.com/science/article/pii/S1053811923002288
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