Childhood urbanicity is associated with emotional episodic memory-related striatal function and common variation in NTRK2
Abstract Background Childhoods in urban or rural environments may differentially affect the risk of neuropsychiatric disorders, possibly through memory processing and neural response to emotional stimuli. Genetic factors may not only influence individuals’ choices of residence but also modulate how...
| Main Authors: | , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
BMC
2024-04-01
|
| Series: | BMC Medicine |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s12916-024-03365-4 |
| _version_ | 1827291545481510912 |
|---|---|
| author | Xiao Zhang Yuyanan Zhang Hao Yan Hao Yu Dai Zhang Venkata S. Mattay Hao Yang Tan Weihua Yue |
| author_facet | Xiao Zhang Yuyanan Zhang Hao Yan Hao Yu Dai Zhang Venkata S. Mattay Hao Yang Tan Weihua Yue |
| author_sort | Xiao Zhang |
| collection | DOAJ |
| description | Abstract Background Childhoods in urban or rural environments may differentially affect the risk of neuropsychiatric disorders, possibly through memory processing and neural response to emotional stimuli. Genetic factors may not only influence individuals’ choices of residence but also modulate how the living environment affects responses to episodic memory. Methods We investigated the effects of childhood urbanicity on episodic memory in 410 adults (discovery sample) and 72 adults (replication sample) with comparable socioeconomic statuses in Beijing, China, distinguishing between those with rural backgrounds (resided in rural areas before age 12 and relocated to urban areas at or after age 12) and urban backgrounds (resided in cities before age 12). We examined the effect of childhood urbanicity on brain function across encoding and retrieval sessions using an fMRI episodic memory paradigm involving the processing of neutral or aversive pictures. Moreover, genetic association analyses were conducted to understand the potential genetic underpinnings that might contribute to memory processing and neural mechanisms influenced by early-life urban or rural environments. Results Episodic memory retrieval accuracy for more difficult neutral stimuli was similar between those with urban and rural childhoods, whereas aversive stimuli elicited higher retrieval accuracy in the urban group (P = 0.023). For aversive stimuli, subjects with urban childhood had relatively decreased engagement of the striatum at encoding and decreased engagement of the hippocampus at retrieval. This more efficient striatal encoding of aversive stimuli in those with urban childhoods was associated with common variation in neurotrophic tyrosine kinase receptor type 2 (NTRK2) (right striatum: P = 1.58×10−6). These findings were confirmed in the replication sample. Conclusions We suggest that this differential striatal processing of aversive stimuli observed in individuals with urban or rural childhoods may represent mechanisms by which childhood urbanicity may affect brain circuits, heightening behavioral responses to negative stressors associated with urban environments. NTRK2-associated neural processes in the striatum may play a role in these processes. |
| first_indexed | 2024-04-24T12:39:54Z |
| format | Article |
| id | doaj.art-e33a48ae4d294e68b74413f07eccdca0 |
| institution | Directory Open Access Journal |
| issn | 1741-7015 |
| language | English |
| last_indexed | 2024-04-24T12:39:54Z |
| publishDate | 2024-04-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Medicine |
| spelling | doaj.art-e33a48ae4d294e68b74413f07eccdca02024-04-07T11:21:09ZengBMCBMC Medicine1741-70152024-04-0122111410.1186/s12916-024-03365-4Childhood urbanicity is associated with emotional episodic memory-related striatal function and common variation in NTRK2Xiao Zhang0Yuyanan Zhang1Hao Yan2Hao Yu3Dai Zhang4Venkata S. Mattay5Hao Yang Tan6Weihua Yue7Institute of Mental Health, National Clinical Research Center for Mental Disorders, Peking University Sixth HospitalInstitute of Mental Health, National Clinical Research Center for Mental Disorders, Peking University Sixth HospitalInstitute of Mental Health, National Clinical Research Center for Mental Disorders, Peking University Sixth HospitalDepartment of Psychiatry, Jining Medical UniversityInstitute of Mental Health, National Clinical Research Center for Mental Disorders, Peking University Sixth HospitalLieber Institute for Brain DevelopmentLieber Institute for Brain DevelopmentInstitute of Mental Health, National Clinical Research Center for Mental Disorders, Peking University Sixth HospitalAbstract Background Childhoods in urban or rural environments may differentially affect the risk of neuropsychiatric disorders, possibly through memory processing and neural response to emotional stimuli. Genetic factors may not only influence individuals’ choices of residence but also modulate how the living environment affects responses to episodic memory. Methods We investigated the effects of childhood urbanicity on episodic memory in 410 adults (discovery sample) and 72 adults (replication sample) with comparable socioeconomic statuses in Beijing, China, distinguishing between those with rural backgrounds (resided in rural areas before age 12 and relocated to urban areas at or after age 12) and urban backgrounds (resided in cities before age 12). We examined the effect of childhood urbanicity on brain function across encoding and retrieval sessions using an fMRI episodic memory paradigm involving the processing of neutral or aversive pictures. Moreover, genetic association analyses were conducted to understand the potential genetic underpinnings that might contribute to memory processing and neural mechanisms influenced by early-life urban or rural environments. Results Episodic memory retrieval accuracy for more difficult neutral stimuli was similar between those with urban and rural childhoods, whereas aversive stimuli elicited higher retrieval accuracy in the urban group (P = 0.023). For aversive stimuli, subjects with urban childhood had relatively decreased engagement of the striatum at encoding and decreased engagement of the hippocampus at retrieval. This more efficient striatal encoding of aversive stimuli in those with urban childhoods was associated with common variation in neurotrophic tyrosine kinase receptor type 2 (NTRK2) (right striatum: P = 1.58×10−6). These findings were confirmed in the replication sample. Conclusions We suggest that this differential striatal processing of aversive stimuli observed in individuals with urban or rural childhoods may represent mechanisms by which childhood urbanicity may affect brain circuits, heightening behavioral responses to negative stressors associated with urban environments. NTRK2-associated neural processes in the striatum may play a role in these processes.https://doi.org/10.1186/s12916-024-03365-4UrbanicityEpisodic memoryStriatumHippocampusGenetic variant |
| spellingShingle | Xiao Zhang Yuyanan Zhang Hao Yan Hao Yu Dai Zhang Venkata S. Mattay Hao Yang Tan Weihua Yue Childhood urbanicity is associated with emotional episodic memory-related striatal function and common variation in NTRK2 BMC Medicine Urbanicity Episodic memory Striatum Hippocampus Genetic variant |
| title | Childhood urbanicity is associated with emotional episodic memory-related striatal function and common variation in NTRK2 |
| title_full | Childhood urbanicity is associated with emotional episodic memory-related striatal function and common variation in NTRK2 |
| title_fullStr | Childhood urbanicity is associated with emotional episodic memory-related striatal function and common variation in NTRK2 |
| title_full_unstemmed | Childhood urbanicity is associated with emotional episodic memory-related striatal function and common variation in NTRK2 |
| title_short | Childhood urbanicity is associated with emotional episodic memory-related striatal function and common variation in NTRK2 |
| title_sort | childhood urbanicity is associated with emotional episodic memory related striatal function and common variation in ntrk2 |
| topic | Urbanicity Episodic memory Striatum Hippocampus Genetic variant |
| url | https://doi.org/10.1186/s12916-024-03365-4 |
| work_keys_str_mv | AT xiaozhang childhoodurbanicityisassociatedwithemotionalepisodicmemoryrelatedstriatalfunctionandcommonvariationinntrk2 AT yuyananzhang childhoodurbanicityisassociatedwithemotionalepisodicmemoryrelatedstriatalfunctionandcommonvariationinntrk2 AT haoyan childhoodurbanicityisassociatedwithemotionalepisodicmemoryrelatedstriatalfunctionandcommonvariationinntrk2 AT haoyu childhoodurbanicityisassociatedwithemotionalepisodicmemoryrelatedstriatalfunctionandcommonvariationinntrk2 AT daizhang childhoodurbanicityisassociatedwithemotionalepisodicmemoryrelatedstriatalfunctionandcommonvariationinntrk2 AT venkatasmattay childhoodurbanicityisassociatedwithemotionalepisodicmemoryrelatedstriatalfunctionandcommonvariationinntrk2 AT haoyangtan childhoodurbanicityisassociatedwithemotionalepisodicmemoryrelatedstriatalfunctionandcommonvariationinntrk2 AT weihuayue childhoodurbanicityisassociatedwithemotionalepisodicmemoryrelatedstriatalfunctionandcommonvariationinntrk2 |