Motor and Limbic System Contribution to Emotional Laughter across the Lifespan
Abstract Laughter is a universal human behavior generated by the cooperation of different systems toward the construction of an expressive vocal pattern. Given the sensitivity of neuroimaging techniques to movements, the neural mechanisms underlying laughter expression remain unclear. Herein, we cha...
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| Published in | Cerebral cortex (New York, N.Y. 1991) Vol. 30; no. 5; pp. 3381 - 3391 |
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| Main Authors | , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Oxford University Press
14.05.2020
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| Subjects | |
| Online Access | Get full text |
| ISSN | 1047-3211 1460-2199 1460-2199 |
| DOI | 10.1093/cercor/bhz316 |
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| Abstract | Abstract
Laughter is a universal human behavior generated by the cooperation of different systems toward the construction of an expressive vocal pattern. Given the sensitivity of neuroimaging techniques to movements, the neural mechanisms underlying laughter expression remain unclear. Herein, we characterized the neural correlates of emotional laughter using the onsets and the duration of laughter bursts to inform functional magnetic resonance imaging. Laughter-related blood oxygen level-dependent (BOLD) increases involved both the motor (motor cortex, supplementary motor area, frontal operculum) and the emotional/limbic (anterior cingulate cortex, amygdala, n. accumbens, hippocampus) systems, as well as modulatory circuitries encompassing the basal ganglia, thalamus, and cerebellum. BOLD changes related to the 2 s preceding the laughter outbreak were selectively observed at the temporo-occipital junction and the periaqueductal gray matter, supporting the role of the former in the detection of incongruity and the gating role of the latter in the initiation of spontaneous laughter. Moreover, developmental changes were identified in laughter processing, consisting in a greater engagement of the reward circuitry in younger subjects; conversely, the default mode network appears more activated in older participants. Our findings contribute valuable information about the processing of real-life humorous materials and suggest a close link between laughter-related motor, affective, and cognitive elements, confirming its complex and multi-faceted nature. |
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| AbstractList | Laughter is a universal human behavior generated by the cooperation of different systems toward the construction of an expressive vocal pattern. Given the sensitivity of neuroimaging techniques to movements, the neural mechanisms underlying laughter expression remain unclear. Herein, we characterized the neural correlates of emotional laughter using the onsets and the duration of laughter bursts to inform functional magnetic resonance imaging. Laughter-related blood oxygen level-dependent (BOLD) increases involved both the motor (motor cortex, supplementary motor area, frontal operculum) and the emotional/limbic (anterior cingulate cortex, amygdala, n. accumbens, hippocampus) systems, as well as modulatory circuitries encompassing the basal ganglia, thalamus, and cerebellum. BOLD changes related to the 2 s preceding the laughter outbreak were selectively observed at the temporo-occipital junction and the periaqueductal gray matter, supporting the role of the former in the detection of incongruity and the gating role of the latter in the initiation of spontaneous laughter. Moreover, developmental changes were identified in laughter processing, consisting in a greater engagement of the reward circuitry in younger subjects; conversely, the default mode network appears more activated in older participants. Our findings contribute valuable information about the processing of real-life humorous materials and suggest a close link between laughter-related motor, affective, and cognitive elements, confirming its complex and multi-faceted nature. Abstract Laughter is a universal human behavior generated by the cooperation of different systems toward the construction of an expressive vocal pattern. Given the sensitivity of neuroimaging techniques to movements, the neural mechanisms underlying laughter expression remain unclear. Herein, we characterized the neural correlates of emotional laughter using the onsets and the duration of laughter bursts to inform functional magnetic resonance imaging. Laughter-related blood oxygen level-dependent (BOLD) increases involved both the motor (motor cortex, supplementary motor area, frontal operculum) and the emotional/limbic (anterior cingulate cortex, amygdala, n. accumbens, hippocampus) systems, as well as modulatory circuitries encompassing the basal ganglia, thalamus, and cerebellum. BOLD changes related to the 2 s preceding the laughter outbreak were selectively observed at the temporo-occipital junction and the periaqueductal gray matter, supporting the role of the former in the detection of incongruity and the gating role of the latter in the initiation of spontaneous laughter. Moreover, developmental changes were identified in laughter processing, consisting in a greater engagement of the reward circuitry in younger subjects; conversely, the default mode network appears more activated in older participants. Our findings contribute valuable information about the processing of real-life humorous materials and suggest a close link between laughter-related motor, affective, and cognitive elements, confirming its complex and multi-faceted nature. Laughter is a universal human behavior generated by the cooperation of different systems toward the construction of an expressive vocal pattern. Given the sensitivity of neuroimaging techniques to movements, the neural mechanisms underlying laughter expression remain unclear. Herein, we characterized the neural correlates of emotional laughter using the onsets and the duration of laughter bursts to inform functional magnetic resonance imaging. Laughter-related blood oxygen level-dependent (BOLD) increases involved both the motor (motor cortex, supplementary motor area, frontal operculum) and the emotional/limbic (anterior cingulate cortex, amygdala, n. accumbens, hippocampus) systems, as well as modulatory circuitries encompassing the basal ganglia, thalamus, and cerebellum. BOLD changes related to the 2 s preceding the laughter outbreak were selectively observed at the temporo-occipital junction and the periaqueductal gray matter, supporting the role of the former in the detection of incongruity and the gating role of the latter in the initiation of spontaneous laughter. Moreover, developmental changes were identified in laughter processing, consisting in a greater engagement of the reward circuitry in younger subjects; conversely, the default mode network appears more activated in older participants. Our findings contribute valuable information about the processing of real-life humorous materials and suggest a close link between laughter-related motor, affective, and cognitive elements, confirming its complex and multi-faceted nature.Laughter is a universal human behavior generated by the cooperation of different systems toward the construction of an expressive vocal pattern. Given the sensitivity of neuroimaging techniques to movements, the neural mechanisms underlying laughter expression remain unclear. Herein, we characterized the neural correlates of emotional laughter using the onsets and the duration of laughter bursts to inform functional magnetic resonance imaging. Laughter-related blood oxygen level-dependent (BOLD) increases involved both the motor (motor cortex, supplementary motor area, frontal operculum) and the emotional/limbic (anterior cingulate cortex, amygdala, n. accumbens, hippocampus) systems, as well as modulatory circuitries encompassing the basal ganglia, thalamus, and cerebellum. BOLD changes related to the 2 s preceding the laughter outbreak were selectively observed at the temporo-occipital junction and the periaqueductal gray matter, supporting the role of the former in the detection of incongruity and the gating role of the latter in the initiation of spontaneous laughter. Moreover, developmental changes were identified in laughter processing, consisting in a greater engagement of the reward circuitry in younger subjects; conversely, the default mode network appears more activated in older participants. Our findings contribute valuable information about the processing of real-life humorous materials and suggest a close link between laughter-related motor, affective, and cognitive elements, confirming its complex and multi-faceted nature. |
| Author | Talami, Francesca Meletti, Stefano Vaudano, Anna Elisabetta |
| Author_xml | – sequence: 1 givenname: Francesca orcidid: 0000-0002-9245-4792 surname: Talami fullname: Talami, Francesca organization: Department of Biomedical, Metabolic, and Neural Sciences, Center for Neuroscience and Neurotechnology, University of Modena and Reggio Emilia, 41121 Modena, Italy – sequence: 2 givenname: Anna Elisabetta orcidid: 0000-0002-6280-7526 surname: Vaudano fullname: Vaudano, Anna Elisabetta email: annavaudano@gmail.com organization: Department of Biomedical, Metabolic, and Neural Sciences, Center for Neuroscience and Neurotechnology, University of Modena and Reggio Emilia, 41121 Modena, Italy – sequence: 3 givenname: Stefano orcidid: 0000-0003-0334-539X surname: Meletti fullname: Meletti, Stefano organization: Department of Biomedical, Metabolic, and Neural Sciences, Center for Neuroscience and Neurotechnology, University of Modena and Reggio Emilia, 41121 Modena, Italy |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31848572$$D View this record in MEDLINE/PubMed |
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Laughter is a universal human behavior generated by the cooperation of different systems toward the construction of an expressive vocal pattern. Given... Laughter is a universal human behavior generated by the cooperation of different systems toward the construction of an expressive vocal pattern. Given the... |
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| Title | Motor and Limbic System Contribution to Emotional Laughter across the Lifespan |
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