Poststress social isolation exerts anxiolytic effects by activating the ventral dentate gyrus
After aversive stress, people either choose to return to their previously familiar social environment or tend to adopt temporary social withdrawal to buffer negative emotions. However, which behavior intervention is more appropriate and when remain elusive. Here, we unexpectedly found that stressed...
| Main Authors: | , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Elsevier
2023-05-01
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| Series: | Neurobiology of Stress |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S2352289523000255 |
| _version_ | 1797812036979130368 |
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| author | Huiyang Lei Huaqing Shu Rui Xiong Ting He Jingru Lv Jiale Liu Guilin Pi Dan Ke Qun Wang Xifei Yang Jian-Zhi Wang Ying Yang |
| author_facet | Huiyang Lei Huaqing Shu Rui Xiong Ting He Jingru Lv Jiale Liu Guilin Pi Dan Ke Qun Wang Xifei Yang Jian-Zhi Wang Ying Yang |
| author_sort | Huiyang Lei |
| collection | DOAJ |
| description | After aversive stress, people either choose to return to their previously familiar social environment or tend to adopt temporary social withdrawal to buffer negative emotions. However, which behavior intervention is more appropriate and when remain elusive. Here, we unexpectedly found that stressed mice experiencing social isolation exhibited less anxiety than those experiencing social contact. Within the first 24 h after returning to their previous social environment, mice experienced acute restraint stress (ARS) displayed low social interest but simultaneously received excessive social disturbance from their cage mates, indicating a critical time window for social isolation to balance the conflict. To screen brain regions that were differentially activated between the poststress social isolation and poststress social contact groups, we performed ΔFosB immunostaining and found that ΔFosB + signals were remarkably increased in the vDG of poststress social isolation group compared with poststress social contact group. There were no significant differences between the two groups in the other anxiety- and social-related brain regions, such as prelimbic cortex, infralimbic cortex, nucleus accumbens, etc. These data indicate that vDG is closely related to the differential phenotypes between the poststress social isolation and poststress social contact groups. Electrophysiological recording, further, revealed a higher activity of vDG in the poststress social isolation group than the poststress social contact group. Chemogenetically inhibiting vDG excitatory neurons within the first 24 h after ARS completely abolished the anxiolytic effects of poststress social isolation, while stimulating vDG excitatory neurons remarkably reduced anxiety-like behaviors in the poststress social contact group. Together, these data suggest that the activity of vDG excitatory neurons is essential and sufficient to govern the anxiolytic effect of poststress social isolation. To the best of our knowledge, this is the first report to uncover a beneficial role of temporal social isolation in acute stress-induced anxiety. In addition to the critical 24-h time window, activation of vDG is crucial for ameliorating anxiety through poststress social isolation. |
| first_indexed | 2024-03-13T07:32:36Z |
| format | Article |
| id | doaj.art-7d82b64fc32d4f8e944f452a1a892a3e |
| institution | Directory Open Access Journal |
| issn | 2352-2895 |
| language | English |
| last_indexed | 2024-03-13T07:32:36Z |
| publishDate | 2023-05-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Neurobiology of Stress |
| spelling | doaj.art-7d82b64fc32d4f8e944f452a1a892a3e2023-06-04T04:24:02ZengElsevierNeurobiology of Stress2352-28952023-05-0124100537Poststress social isolation exerts anxiolytic effects by activating the ventral dentate gyrusHuiyang Lei0Huaqing Shu1Rui Xiong2Ting He3Jingru Lv4Jiale Liu5Guilin Pi6Dan Ke7Qun Wang8Xifei Yang9Jian-Zhi Wang10Ying Yang11Department of Pathophysiology, School of Basic Medicine, Key Laboratory of Education Ministry of China/Hubei Province for Neurological Disorders, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430030, ChinaDepartment of Critical Care Medicine, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430022, China; Corresponding author.Department of Pathophysiology, School of Basic Medicine, Key Laboratory of Education Ministry of China/Hubei Province for Neurological Disorders, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430030, ChinaDepartment of Pathophysiology, School of Basic Medicine, Key Laboratory of Education Ministry of China/Hubei Province for Neurological Disorders, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430030, ChinaDepartment of Pathophysiology, School of Basic Medicine, Key Laboratory of Education Ministry of China/Hubei Province for Neurological Disorders, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430030, ChinaDepartment of Pathophysiology, School of Basic Medicine, Key Laboratory of Education Ministry of China/Hubei Province for Neurological Disorders, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430030, ChinaDepartment of Pathophysiology, School of Basic Medicine, Key Laboratory of Education Ministry of China/Hubei Province for Neurological Disorders, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430030, ChinaDepartment of Pathophysiology, School of Basic Medicine, Key Laboratory of Education Ministry of China/Hubei Province for Neurological Disorders, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430030, ChinaDepartment of Pathophysiology, School of Basic Medicine, Key Laboratory of Education Ministry of China/Hubei Province for Neurological Disorders, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430030, ChinaKey Laboratory of Modern Toxicology of Shenzhen, Shenzhen Center for Disease Control and Prevention, 8 Longyuan Road, Nanshan District, Shenzhen, 518055, ChinaDepartment of Pathophysiology, School of Basic Medicine, Key Laboratory of Education Ministry of China/Hubei Province for Neurological Disorders, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430030, China; Co-innovation Center of Neuroregeneration, Nantong University, Nantong, 226000, China; Corresponding author. Department of Pathophysiology, School of Basic Medicine, Key Laboratory of Education Ministry of China/Hubei Province for Neurological Disorders, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430030, ChinaDepartment of Pathophysiology, School of Basic Medicine, Key Laboratory of Education Ministry of China/Hubei Province for Neurological Disorders, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430030, China; Corresponding author.After aversive stress, people either choose to return to their previously familiar social environment or tend to adopt temporary social withdrawal to buffer negative emotions. However, which behavior intervention is more appropriate and when remain elusive. Here, we unexpectedly found that stressed mice experiencing social isolation exhibited less anxiety than those experiencing social contact. Within the first 24 h after returning to their previous social environment, mice experienced acute restraint stress (ARS) displayed low social interest but simultaneously received excessive social disturbance from their cage mates, indicating a critical time window for social isolation to balance the conflict. To screen brain regions that were differentially activated between the poststress social isolation and poststress social contact groups, we performed ΔFosB immunostaining and found that ΔFosB + signals were remarkably increased in the vDG of poststress social isolation group compared with poststress social contact group. There were no significant differences between the two groups in the other anxiety- and social-related brain regions, such as prelimbic cortex, infralimbic cortex, nucleus accumbens, etc. These data indicate that vDG is closely related to the differential phenotypes between the poststress social isolation and poststress social contact groups. Electrophysiological recording, further, revealed a higher activity of vDG in the poststress social isolation group than the poststress social contact group. Chemogenetically inhibiting vDG excitatory neurons within the first 24 h after ARS completely abolished the anxiolytic effects of poststress social isolation, while stimulating vDG excitatory neurons remarkably reduced anxiety-like behaviors in the poststress social contact group. Together, these data suggest that the activity of vDG excitatory neurons is essential and sufficient to govern the anxiolytic effect of poststress social isolation. To the best of our knowledge, this is the first report to uncover a beneficial role of temporal social isolation in acute stress-induced anxiety. In addition to the critical 24-h time window, activation of vDG is crucial for ameliorating anxiety through poststress social isolation.http://www.sciencedirect.com/science/article/pii/S2352289523000255Anxiolytic effectAcute stressSocial isolationSocial contactVentral dentate gyrus |
| spellingShingle | Huiyang Lei Huaqing Shu Rui Xiong Ting He Jingru Lv Jiale Liu Guilin Pi Dan Ke Qun Wang Xifei Yang Jian-Zhi Wang Ying Yang Poststress social isolation exerts anxiolytic effects by activating the ventral dentate gyrus Neurobiology of Stress Anxiolytic effect Acute stress Social isolation Social contact Ventral dentate gyrus |
| title | Poststress social isolation exerts anxiolytic effects by activating the ventral dentate gyrus |
| title_full | Poststress social isolation exerts anxiolytic effects by activating the ventral dentate gyrus |
| title_fullStr | Poststress social isolation exerts anxiolytic effects by activating the ventral dentate gyrus |
| title_full_unstemmed | Poststress social isolation exerts anxiolytic effects by activating the ventral dentate gyrus |
| title_short | Poststress social isolation exerts anxiolytic effects by activating the ventral dentate gyrus |
| title_sort | poststress social isolation exerts anxiolytic effects by activating the ventral dentate gyrus |
| topic | Anxiolytic effect Acute stress Social isolation Social contact Ventral dentate gyrus |
| url | http://www.sciencedirect.com/science/article/pii/S2352289523000255 |
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