Nucleus accumbens core single cell ensembles bidirectionally respond to experienced versus observed aversive events
Abstract Fear learning is a critical feature of survival skills among mammals. In rodents, fear learning manifests itself through direct experience of the aversive event or social transmission of aversive stimuli such as observing and acting on conspecifics’ distress. The neuronal network underlying...
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2023-12-01
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| Series: | Scientific Reports |
| Online Access: | https://doi.org/10.1038/s41598-023-49686-x |
| _version_ | 1797377069497188352 |
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| author | Oyku Dinckol Noah Harris Wenger Jennifer E. Zachry Munir Gunes Kutlu |
| author_facet | Oyku Dinckol Noah Harris Wenger Jennifer E. Zachry Munir Gunes Kutlu |
| author_sort | Oyku Dinckol |
| collection | DOAJ |
| description | Abstract Fear learning is a critical feature of survival skills among mammals. In rodents, fear learning manifests itself through direct experience of the aversive event or social transmission of aversive stimuli such as observing and acting on conspecifics’ distress. The neuronal network underlying the social transmission of information largely overlaps with the brain regions that mediate behavioral responses to aversive and rewarding stimuli. In this study, we recorded single cell activity patterns of nucleus accumbens (NAc) core neurons using in vivo optical imaging of calcium transients via miniature scopes. This cutting-edge imaging methodology not only allows us to record activity patterns of individual neurons but also lets us longitudinally follow these individual neurons across time and different behavioral states. Using this approach, we identified NAc core single cell ensembles that respond to experienced and/or observed aversive stimuli. Our results showed that experienced and observed aversive stimuli evoke NAc core ensemble activity that is largely positive, with a smaller subset of negative responses. The size of the NAc single cell ensemble response was greater for experienced aversive stimuli compared to observed aversive events. Our results also revealed sex differences in the NAc core single cell ensembles responses to experience aversive stimuli, where females showed a greater accumbal response. Importantly, we found a subpopulation within the NAc core single cell ensembles that show a bidirectional response to experienced aversive stimuli versus observed aversive stimuli (i.e., negative response to experienced and positive response to observed). Our results suggest that the NAc plays a role in differentiating somatosensory experience from social observation of aversion at a single cell level. These results have important implications for psychopathologies where social information processing is maladaptive, such as autism spectrum disorders. |
| first_indexed | 2024-03-08T19:48:40Z |
| format | Article |
| id | doaj.art-bf2c3817a35047fc89bacf5501fe5248 |
| institution | Directory Open Access Journal |
| issn | 2045-2322 |
| language | English |
| last_indexed | 2024-03-08T19:48:40Z |
| publishDate | 2023-12-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Scientific Reports |
| spelling | doaj.art-bf2c3817a35047fc89bacf5501fe52482023-12-24T12:14:48ZengNature PortfolioScientific Reports2045-23222023-12-0113111210.1038/s41598-023-49686-xNucleus accumbens core single cell ensembles bidirectionally respond to experienced versus observed aversive eventsOyku Dinckol0Noah Harris Wenger1Jennifer E. Zachry2Munir Gunes Kutlu3Department of Cell Biology and Neuroscience, Rowan-Virtua School of Translational Biomedical Engineering and Sciences, Rowan UniversityDepartment of Cell Biology and Neuroscience, Rowan-Virtua School of Translational Biomedical Engineering and Sciences, Rowan UniversityDepartment of Pharmacology, Vanderbilt UniversityDepartment of Cell Biology and Neuroscience, Rowan-Virtua School of Translational Biomedical Engineering and Sciences, Rowan UniversityAbstract Fear learning is a critical feature of survival skills among mammals. In rodents, fear learning manifests itself through direct experience of the aversive event or social transmission of aversive stimuli such as observing and acting on conspecifics’ distress. The neuronal network underlying the social transmission of information largely overlaps with the brain regions that mediate behavioral responses to aversive and rewarding stimuli. In this study, we recorded single cell activity patterns of nucleus accumbens (NAc) core neurons using in vivo optical imaging of calcium transients via miniature scopes. This cutting-edge imaging methodology not only allows us to record activity patterns of individual neurons but also lets us longitudinally follow these individual neurons across time and different behavioral states. Using this approach, we identified NAc core single cell ensembles that respond to experienced and/or observed aversive stimuli. Our results showed that experienced and observed aversive stimuli evoke NAc core ensemble activity that is largely positive, with a smaller subset of negative responses. The size of the NAc single cell ensemble response was greater for experienced aversive stimuli compared to observed aversive events. Our results also revealed sex differences in the NAc core single cell ensembles responses to experience aversive stimuli, where females showed a greater accumbal response. Importantly, we found a subpopulation within the NAc core single cell ensembles that show a bidirectional response to experienced aversive stimuli versus observed aversive stimuli (i.e., negative response to experienced and positive response to observed). Our results suggest that the NAc plays a role in differentiating somatosensory experience from social observation of aversion at a single cell level. These results have important implications for psychopathologies where social information processing is maladaptive, such as autism spectrum disorders.https://doi.org/10.1038/s41598-023-49686-x |
| spellingShingle | Oyku Dinckol Noah Harris Wenger Jennifer E. Zachry Munir Gunes Kutlu Nucleus accumbens core single cell ensembles bidirectionally respond to experienced versus observed aversive events Scientific Reports |
| title | Nucleus accumbens core single cell ensembles bidirectionally respond to experienced versus observed aversive events |
| title_full | Nucleus accumbens core single cell ensembles bidirectionally respond to experienced versus observed aversive events |
| title_fullStr | Nucleus accumbens core single cell ensembles bidirectionally respond to experienced versus observed aversive events |
| title_full_unstemmed | Nucleus accumbens core single cell ensembles bidirectionally respond to experienced versus observed aversive events |
| title_short | Nucleus accumbens core single cell ensembles bidirectionally respond to experienced versus observed aversive events |
| title_sort | nucleus accumbens core single cell ensembles bidirectionally respond to experienced versus observed aversive events |
| url | https://doi.org/10.1038/s41598-023-49686-x |
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