Atypical Amygdala–Neocortex Interaction During Dynamic Facial Expression Processing in Autism Spectrum Disorder
Atypical reciprocal social interactions involving emotional facial expressions are a core clinical feature of autism spectrum disorder (ASD). Previous functional magnetic resonance imaging (fMRI) studies have demonstrated that some social brain regions, including subcortical (e.g., amygdala) and neo...
| Main Authors: | , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2019-10-01
|
| Series: | Frontiers in Human Neuroscience |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/article/10.3389/fnhum.2019.00351/full |
| _version_ | 1819226481505599488 |
|---|---|
| author | Wataru Sato Takanori Kochiyama Shota Uono Sayaka Yoshimura Yasutaka Kubota Reiko Sawada Reiko Sawada Morimitsu Sakihama Motomi Toichi Motomi Toichi |
| author_facet | Wataru Sato Takanori Kochiyama Shota Uono Sayaka Yoshimura Yasutaka Kubota Reiko Sawada Reiko Sawada Morimitsu Sakihama Motomi Toichi Motomi Toichi |
| author_sort | Wataru Sato |
| collection | DOAJ |
| description | Atypical reciprocal social interactions involving emotional facial expressions are a core clinical feature of autism spectrum disorder (ASD). Previous functional magnetic resonance imaging (fMRI) studies have demonstrated that some social brain regions, including subcortical (e.g., amygdala) and neocortical regions (e.g., fusiform gyrus, FG) are less activated during the processing of facial expression stimuli in individuals with ASD. However, the functional networking patterns between the subcortical and cortical regions in processing emotional facial expressions remain unclear. We investigated this issue in ASD (n = 31) and typically developing (TD; n = 31) individuals using fMRI. Participants viewed dynamic facial expressions of anger and happiness and their corresponding mosaic images. Regional brain activity analysis revealed reduced activation of several social brain regions, including the amygdala, in the ASD group compared with the TD group in response to dynamic facial expressions vs. dynamic mosaics (p < 0.05, ηp2 = 0.19). Dynamic causal modeling (DCM) analyses were then used to compare models with forward, backward, and bi-directional effective connectivity between the amygdala and neocortical networks. The results revealed that: (1) the model with effective connectivity from the amygdala to the neocortex best fit the data of both groups; and (2) the same model best accounted for group differences. Coupling parameter (i.e., effective connectivity) analyses showed that the modulatory effects of dynamic facial processing were substantially weaker in the ASD group than in the TD group. These findings suggest that atypical modulation from the amygdala to the neocortex underlies impairment in social interaction involving dynamic facial expressions in individuals with ASD. |
| first_indexed | 2024-12-23T10:26:11Z |
| format | Article |
| id | doaj.art-7226fe1e26a74850b940a31e86ffa4cd |
| institution | Directory Open Access Journal |
| issn | 1662-5161 |
| language | English |
| last_indexed | 2024-12-23T10:26:11Z |
| publishDate | 2019-10-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Human Neuroscience |
| spelling | doaj.art-7226fe1e26a74850b940a31e86ffa4cd2022-12-21T17:50:34ZengFrontiers Media S.A.Frontiers in Human Neuroscience1662-51612019-10-011310.3389/fnhum.2019.00351469436Atypical Amygdala–Neocortex Interaction During Dynamic Facial Expression Processing in Autism Spectrum DisorderWataru Sato0Takanori Kochiyama1Shota Uono2Sayaka Yoshimura3Yasutaka Kubota4Reiko Sawada5Reiko Sawada6Morimitsu Sakihama7Motomi Toichi8Motomi Toichi9Kokoro Research Center, Kyoto University, Kyoto, JapanBrain Activity Imaging Center, ATR-Promotions, Inc., Kyoto, JapanDepartment of Neurodevelopmental Psychiatry, Habilitation and Rehabilitation, Graduate School of Medicine, Kyoto University, Kyoto, JapanDepartment of Neurodevelopmental Psychiatry, Habilitation and Rehabilitation, Graduate School of Medicine, Kyoto University, Kyoto, JapanHealth and Medical Services Center, Shiga University, Hikone, JapanFaculty of Human Health Science, Graduate School of Medicine, Kyoto University, Kyoto, JapanThe Organization for Promoting Developmental Disorder Research, Kyoto, JapanRakuwa-kai Otowa Hospital, Kyoto, JapanFaculty of Human Health Science, Graduate School of Medicine, Kyoto University, Kyoto, JapanThe Organization for Promoting Developmental Disorder Research, Kyoto, JapanAtypical reciprocal social interactions involving emotional facial expressions are a core clinical feature of autism spectrum disorder (ASD). Previous functional magnetic resonance imaging (fMRI) studies have demonstrated that some social brain regions, including subcortical (e.g., amygdala) and neocortical regions (e.g., fusiform gyrus, FG) are less activated during the processing of facial expression stimuli in individuals with ASD. However, the functional networking patterns between the subcortical and cortical regions in processing emotional facial expressions remain unclear. We investigated this issue in ASD (n = 31) and typically developing (TD; n = 31) individuals using fMRI. Participants viewed dynamic facial expressions of anger and happiness and their corresponding mosaic images. Regional brain activity analysis revealed reduced activation of several social brain regions, including the amygdala, in the ASD group compared with the TD group in response to dynamic facial expressions vs. dynamic mosaics (p < 0.05, ηp2 = 0.19). Dynamic causal modeling (DCM) analyses were then used to compare models with forward, backward, and bi-directional effective connectivity between the amygdala and neocortical networks. The results revealed that: (1) the model with effective connectivity from the amygdala to the neocortex best fit the data of both groups; and (2) the same model best accounted for group differences. Coupling parameter (i.e., effective connectivity) analyses showed that the modulatory effects of dynamic facial processing were substantially weaker in the ASD group than in the TD group. These findings suggest that atypical modulation from the amygdala to the neocortex underlies impairment in social interaction involving dynamic facial expressions in individuals with ASD.https://www.frontiersin.org/article/10.3389/fnhum.2019.00351/fullamygdalaautism spectrum disorder (ASD)dynamic causal modeling (DCM)dynamic facial expressions of emotionfunctional magnetic resonance imaging (fMRI) |
| spellingShingle | Wataru Sato Takanori Kochiyama Shota Uono Sayaka Yoshimura Yasutaka Kubota Reiko Sawada Reiko Sawada Morimitsu Sakihama Motomi Toichi Motomi Toichi Atypical Amygdala–Neocortex Interaction During Dynamic Facial Expression Processing in Autism Spectrum Disorder Frontiers in Human Neuroscience amygdala autism spectrum disorder (ASD) dynamic causal modeling (DCM) dynamic facial expressions of emotion functional magnetic resonance imaging (fMRI) |
| title | Atypical Amygdala–Neocortex Interaction During Dynamic Facial Expression Processing in Autism Spectrum Disorder |
| title_full | Atypical Amygdala–Neocortex Interaction During Dynamic Facial Expression Processing in Autism Spectrum Disorder |
| title_fullStr | Atypical Amygdala–Neocortex Interaction During Dynamic Facial Expression Processing in Autism Spectrum Disorder |
| title_full_unstemmed | Atypical Amygdala–Neocortex Interaction During Dynamic Facial Expression Processing in Autism Spectrum Disorder |
| title_short | Atypical Amygdala–Neocortex Interaction During Dynamic Facial Expression Processing in Autism Spectrum Disorder |
| title_sort | atypical amygdala neocortex interaction during dynamic facial expression processing in autism spectrum disorder |
| topic | amygdala autism spectrum disorder (ASD) dynamic causal modeling (DCM) dynamic facial expressions of emotion functional magnetic resonance imaging (fMRI) |
| url | https://www.frontiersin.org/article/10.3389/fnhum.2019.00351/full |
| work_keys_str_mv | AT watarusato atypicalamygdalaneocortexinteractionduringdynamicfacialexpressionprocessinginautismspectrumdisorder AT takanorikochiyama atypicalamygdalaneocortexinteractionduringdynamicfacialexpressionprocessinginautismspectrumdisorder AT shotauono atypicalamygdalaneocortexinteractionduringdynamicfacialexpressionprocessinginautismspectrumdisorder AT sayakayoshimura atypicalamygdalaneocortexinteractionduringdynamicfacialexpressionprocessinginautismspectrumdisorder AT yasutakakubota atypicalamygdalaneocortexinteractionduringdynamicfacialexpressionprocessinginautismspectrumdisorder AT reikosawada atypicalamygdalaneocortexinteractionduringdynamicfacialexpressionprocessinginautismspectrumdisorder AT reikosawada atypicalamygdalaneocortexinteractionduringdynamicfacialexpressionprocessinginautismspectrumdisorder AT morimitsusakihama atypicalamygdalaneocortexinteractionduringdynamicfacialexpressionprocessinginautismspectrumdisorder AT motomitoichi atypicalamygdalaneocortexinteractionduringdynamicfacialexpressionprocessinginautismspectrumdisorder AT motomitoichi atypicalamygdalaneocortexinteractionduringdynamicfacialexpressionprocessinginautismspectrumdisorder |