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Neighborhood Disadvantage and Neural Correlates of Threat and Reward Processing in Survivors of Recent Trauma

IMPORTANCE: Differences in neighborhood socioeconomic characteristics are important considerations in understanding differences in risk vs resilience in mental health. Neighborhood disadvantage is associated with alterations in the function and structure of threat neurocircuitry. OBJECTIVE: To inves...

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Autores principales: Webb, E. Kate, Ely, Timothy D., Rowland, Grace E., Lebois, Lauren A. M., van Rooij, Sanne J. H., Bruce, Steven E., Jovanovic, Tanja, House, Stacey L., Beaudoin, Francesca L., An, Xinming, Neylan, Thomas C., Clifford, Gari D., Linnstaedt, Sarah D., Germine, Laura T., Bollen, Kenneth A., Rauch, Scott L., Haran, John P., Storrow, Alan B., Lewandowski, Christopher, Musey, Paul I., Hendry, Phyllis L., Sheikh, Sophia, Jones, Christopher W., Punches, Brittany E., Swor, Robert A., Pascual, Jose L., Seamon, Mark J., Datner, Elizabeth M., Pearson, Claire, Peak, David A., Merchant, Roland C., Domeier, Robert M., Rathlev, Niels K., Sergot, Paulina, Sanchez, Leon D., Kessler, Ronald C., Koenen, Karestan C., McLean, Samuel A., Stevens, Jennifer S., Ressler, Kerry J., Harnett, Nathaniel G.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Medical Association 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10507487/
https://www.ncbi.nlm.nih.gov/pubmed/37721751
http://dx.doi.org/10.1001/jamanetworkopen.2023.34483
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author Webb, E. Kate
Ely, Timothy D.
Rowland, Grace E.
Lebois, Lauren A. M.
van Rooij, Sanne J. H.
Bruce, Steven E.
Jovanovic, Tanja
House, Stacey L.
Beaudoin, Francesca L.
An, Xinming
Neylan, Thomas C.
Clifford, Gari D.
Linnstaedt, Sarah D.
Germine, Laura T.
Bollen, Kenneth A.
Rauch, Scott L.
Haran, John P.
Storrow, Alan B.
Lewandowski, Christopher
Musey, Paul I.
Hendry, Phyllis L.
Sheikh, Sophia
Jones, Christopher W.
Punches, Brittany E.
Swor, Robert A.
Pascual, Jose L.
Seamon, Mark J.
Datner, Elizabeth M.
Pearson, Claire
Peak, David A.
Merchant, Roland C.
Domeier, Robert M.
Rathlev, Niels K.
Sergot, Paulina
Sanchez, Leon D.
Kessler, Ronald C.
Koenen, Karestan C.
McLean, Samuel A.
Stevens, Jennifer S.
Ressler, Kerry J.
Harnett, Nathaniel G.
author_facet Webb, E. Kate
Ely, Timothy D.
Rowland, Grace E.
Lebois, Lauren A. M.
van Rooij, Sanne J. H.
Bruce, Steven E.
Jovanovic, Tanja
House, Stacey L.
Beaudoin, Francesca L.
An, Xinming
Neylan, Thomas C.
Clifford, Gari D.
Linnstaedt, Sarah D.
Germine, Laura T.
Bollen, Kenneth A.
Rauch, Scott L.
Haran, John P.
Storrow, Alan B.
Lewandowski, Christopher
Musey, Paul I.
Hendry, Phyllis L.
Sheikh, Sophia
Jones, Christopher W.
Punches, Brittany E.
Swor, Robert A.
Pascual, Jose L.
Seamon, Mark J.
Datner, Elizabeth M.
Pearson, Claire
Peak, David A.
Merchant, Roland C.
Domeier, Robert M.
Rathlev, Niels K.
Sergot, Paulina
Sanchez, Leon D.
Kessler, Ronald C.
Koenen, Karestan C.
McLean, Samuel A.
Stevens, Jennifer S.
Ressler, Kerry J.
Harnett, Nathaniel G.
author_sort Webb, E. Kate
collection PubMed
description IMPORTANCE: Differences in neighborhood socioeconomic characteristics are important considerations in understanding differences in risk vs resilience in mental health. Neighborhood disadvantage is associated with alterations in the function and structure of threat neurocircuitry. OBJECTIVE: To investigate associations of neighborhood disadvantage with white and gray matter and neural reactivity to positive and negative stimuli in the context of trauma exposure. DESIGN, SETTING, AND PARTICIPANTS: In this cross-sectional study, survivors of trauma who completed sociodemographic and posttraumatic symptom assessments and neuroimaging were recruited as part of the Advancing Understanding of Recovery After Trauma (AURORA) study between September 2017 and June 2021. Data analysis was performed from October 25, 2022, to February 15, 2023. EXPOSURE: Neighborhood disadvantage was measured with the Area Deprivation Index (ADI) for each participant home address. MAIN OUTCOMES AND MEASURES: Participants completed separate threat and reward tasks during functional magnetic resonance imaging. Diffusion-weighted and high-resolution structural images were also collected. Linear models assessed the association of ADI with reactivity, microstructure, and macrostructure of a priori regions of interest after adjusting for income, lifetime trauma, sex at birth, and age. A moderated-mediation model tested whether ADI was associated with neural activity via microstructural changes and if this was modulated by PTSD symptoms. RESULTS: A total of 280 participants (183 females [65.4%]; mean [SD] age, 35.39 [13.29] years) completed the threat task and 244 participants (156 females [63.9%]; mean [SD] age, 35.10 [13.26] years) completed the reward task. Higher ADI (per 1-unit increase) was associated with greater insula (t(274) = 3.20; β = 0.20; corrected P = .008) and anterior cingulate cortex (ACC; t(274) = 2.56; β = 0.16; corrected P = .04) threat-related activity after considering covariates, but ADI was not associated with reward reactivity. Greater disadvantage was also associated with altered microstructure of the cingulum bundle (t(274) = 3.48; β = 0.21; corrected P = .001) and gray matter morphology of the ACC (cortical thickness: t(273) = −2.29; β = −0.13; corrected P = .02; surface area: t(273) = 2.53; β = 0.13; corrected P = .02). The moderated-mediation model revealed that ADI was associated with ACC threat reactivity via cingulum microstructural changes (index of moderated mediation = −0.02). However, this mediation was only present in individuals with greater PTSD symptom severity (at the mean: β = −0.17; standard error = 0.06, t= −2.28; P = .007; at 1 SD above the mean: β = −0.28; standard error = 0.08; t = −3.35; P < .001). CONCLUSIONS AND RELEVANCE: In this study, neighborhood disadvantage was associated with neurobiology that supports threat processing, revealing associations of neighborhood disadvantage with neural susceptibility for PTSD and suggesting how altered structure-function associations may complicate symptoms. Future work should investigate specific components of neighborhood disadvantage that may be associated with these outcomes.
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spelling pubmed-105074872023-09-20 Neighborhood Disadvantage and Neural Correlates of Threat and Reward Processing in Survivors of Recent Trauma Webb, E. Kate Ely, Timothy D. Rowland, Grace E. Lebois, Lauren A. M. van Rooij, Sanne J. H. Bruce, Steven E. Jovanovic, Tanja House, Stacey L. Beaudoin, Francesca L. An, Xinming Neylan, Thomas C. Clifford, Gari D. Linnstaedt, Sarah D. Germine, Laura T. Bollen, Kenneth A. Rauch, Scott L. Haran, John P. Storrow, Alan B. Lewandowski, Christopher Musey, Paul I. Hendry, Phyllis L. Sheikh, Sophia Jones, Christopher W. Punches, Brittany E. Swor, Robert A. Pascual, Jose L. Seamon, Mark J. Datner, Elizabeth M. Pearson, Claire Peak, David A. Merchant, Roland C. Domeier, Robert M. Rathlev, Niels K. Sergot, Paulina Sanchez, Leon D. Kessler, Ronald C. Koenen, Karestan C. McLean, Samuel A. Stevens, Jennifer S. Ressler, Kerry J. Harnett, Nathaniel G. JAMA Netw Open Original Investigation IMPORTANCE: Differences in neighborhood socioeconomic characteristics are important considerations in understanding differences in risk vs resilience in mental health. Neighborhood disadvantage is associated with alterations in the function and structure of threat neurocircuitry. OBJECTIVE: To investigate associations of neighborhood disadvantage with white and gray matter and neural reactivity to positive and negative stimuli in the context of trauma exposure. DESIGN, SETTING, AND PARTICIPANTS: In this cross-sectional study, survivors of trauma who completed sociodemographic and posttraumatic symptom assessments and neuroimaging were recruited as part of the Advancing Understanding of Recovery After Trauma (AURORA) study between September 2017 and June 2021. Data analysis was performed from October 25, 2022, to February 15, 2023. EXPOSURE: Neighborhood disadvantage was measured with the Area Deprivation Index (ADI) for each participant home address. MAIN OUTCOMES AND MEASURES: Participants completed separate threat and reward tasks during functional magnetic resonance imaging. Diffusion-weighted and high-resolution structural images were also collected. Linear models assessed the association of ADI with reactivity, microstructure, and macrostructure of a priori regions of interest after adjusting for income, lifetime trauma, sex at birth, and age. A moderated-mediation model tested whether ADI was associated with neural activity via microstructural changes and if this was modulated by PTSD symptoms. RESULTS: A total of 280 participants (183 females [65.4%]; mean [SD] age, 35.39 [13.29] years) completed the threat task and 244 participants (156 females [63.9%]; mean [SD] age, 35.10 [13.26] years) completed the reward task. Higher ADI (per 1-unit increase) was associated with greater insula (t(274) = 3.20; β = 0.20; corrected P = .008) and anterior cingulate cortex (ACC; t(274) = 2.56; β = 0.16; corrected P = .04) threat-related activity after considering covariates, but ADI was not associated with reward reactivity. Greater disadvantage was also associated with altered microstructure of the cingulum bundle (t(274) = 3.48; β = 0.21; corrected P = .001) and gray matter morphology of the ACC (cortical thickness: t(273) = −2.29; β = −0.13; corrected P = .02; surface area: t(273) = 2.53; β = 0.13; corrected P = .02). The moderated-mediation model revealed that ADI was associated with ACC threat reactivity via cingulum microstructural changes (index of moderated mediation = −0.02). However, this mediation was only present in individuals with greater PTSD symptom severity (at the mean: β = −0.17; standard error = 0.06, t= −2.28; P = .007; at 1 SD above the mean: β = −0.28; standard error = 0.08; t = −3.35; P < .001). CONCLUSIONS AND RELEVANCE: In this study, neighborhood disadvantage was associated with neurobiology that supports threat processing, revealing associations of neighborhood disadvantage with neural susceptibility for PTSD and suggesting how altered structure-function associations may complicate symptoms. Future work should investigate specific components of neighborhood disadvantage that may be associated with these outcomes. American Medical Association 2023-09-18 /pmc/articles/PMC10507487/ /pubmed/37721751 http://dx.doi.org/10.1001/jamanetworkopen.2023.34483 Text en Copyright 2023 Webb EK et al. JAMA Network Open. https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the CC-BY License.
spellingShingle Original Investigation
Webb, E. Kate
Ely, Timothy D.
Rowland, Grace E.
Lebois, Lauren A. M.
van Rooij, Sanne J. H.
Bruce, Steven E.
Jovanovic, Tanja
House, Stacey L.
Beaudoin, Francesca L.
An, Xinming
Neylan, Thomas C.
Clifford, Gari D.
Linnstaedt, Sarah D.
Germine, Laura T.
Bollen, Kenneth A.
Rauch, Scott L.
Haran, John P.
Storrow, Alan B.
Lewandowski, Christopher
Musey, Paul I.
Hendry, Phyllis L.
Sheikh, Sophia
Jones, Christopher W.
Punches, Brittany E.
Swor, Robert A.
Pascual, Jose L.
Seamon, Mark J.
Datner, Elizabeth M.
Pearson, Claire
Peak, David A.
Merchant, Roland C.
Domeier, Robert M.
Rathlev, Niels K.
Sergot, Paulina
Sanchez, Leon D.
Kessler, Ronald C.
Koenen, Karestan C.
McLean, Samuel A.
Stevens, Jennifer S.
Ressler, Kerry J.
Harnett, Nathaniel G.
Neighborhood Disadvantage and Neural Correlates of Threat and Reward Processing in Survivors of Recent Trauma
title Neighborhood Disadvantage and Neural Correlates of Threat and Reward Processing in Survivors of Recent Trauma
title_full Neighborhood Disadvantage and Neural Correlates of Threat and Reward Processing in Survivors of Recent Trauma
title_fullStr Neighborhood Disadvantage and Neural Correlates of Threat and Reward Processing in Survivors of Recent Trauma
title_full_unstemmed Neighborhood Disadvantage and Neural Correlates of Threat and Reward Processing in Survivors of Recent Trauma
title_short Neighborhood Disadvantage and Neural Correlates of Threat and Reward Processing in Survivors of Recent Trauma
title_sort neighborhood disadvantage and neural correlates of threat and reward processing in survivors of recent trauma
topic Original Investigation
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10507487/
https://www.ncbi.nlm.nih.gov/pubmed/37721751
http://dx.doi.org/10.1001/jamanetworkopen.2023.34483
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