Neighborhood Perceptions Are Associated With Intrinsic Amygdala Activity and Resting-State Connectivity With Salience Network Nodes Among Older Adults

Overview

Journal Psychosom Med

Specialty Psychiatry

Date 2023 Dec 27

PMID 38150567

Authors

Lola R Ortiz-Whittingham

Liang Zhan

Erika N Ortiz-Chaparro

Yvonne Baumer

Shannon Zenk

Melissa Lamar

Tiffany M Powell-Wiley

Affiliations

Soon will be listed here.

Abstract

Objective: Neighborhood perceptions are associated with physical and mental health outcomes; however, the biological associates of this relationship remain to be fully understood. Here, we evaluate the relationship between neighborhood perceptions and amygdala activity and connectivity with salience network (i.e., insula, anterior cingulate, thalamus) nodes.

Methods: Forty-eight older adults (mean age = 68 [7] years, 52% female, 47% non-Hispanic Black, 2% Hispanic) without dementia or depression completed the Perceptions of Neighborhood Environment Scale. Lower scores indicated less favorable perceptions of aesthetic quality, walking environment, availability of healthy food, safety, violence (i.e., more perceived violence), social cohesion, and participation in activities with neighbors. Participants separately underwent resting-state functional magnetic resonance imaging.

Results: Less favorable perceived safety ( β = -0.33, pFDR = .04) and participation in activities with neighbors ( β = -0.35, pFDR = .02) were associated with higher left amygdala activity, independent of covariates including psychosocial factors. Less favorable safety perceptions were also associated with enhanced left amygdala functional connectivity with the bilateral insular cortices and the left anterior insula ( β = -0.34, pFDR = .04). Less favorable perceived social cohesion was associated with enhanced left amygdala functional connectivity with the right thalamus ( β = -0.42, pFDR = .04), and less favorable perceptions about healthy food availability were associated with enhanced left amygdala functional connectivity with the bilateral anterior insula (right: β = -0.39, pFDR = .04; left: β = -0.42, pFDR = .02) and anterior cingulate gyrus ( β = -0.37, pFDR = .04).

Conclusions: Taken together, our findings document relationships between select neighborhood perceptions and amygdala activity as well as connectivity with salience network nodes; if confirmed, targeted community-level interventions and existing community strengths may promote brain-behavior relationships.

References

Graham A, Rasmussen J, Rudolph M, Heim C, Gilmore J, Styner M . Maternal Systemic Interleukin-6 During Pregnancy Is Associated With Newborn Amygdala Phenotypes and Subsequent Behavior at 2 Years of Age. Biol Psychiatry. 2017; 83(2):109-119. PMC: 5723539. DOI: 10.1016/j.biopsych.2017.05.027. View

Leschak C, Dutcher J, Byrne Haltom K, Breen E, Bower J, Eisenberger N . Associations between amygdala reactivity to social threat, perceived stress and C-reactive protein in breast cancer survivors. Soc Cogn Affect Neurosci. 2020; 15(10):1056-1063. PMC: 7657448. DOI: 10.1093/scan/nsz103. View

Barnett A, Zhang C, Johnston J, Cerin E . Relationships between the neighborhood environment and depression in older adults: a systematic review and meta-analysis. Int Psychogeriatr. 2017; 30(8):1153-1176. DOI: 10.1017/S104161021700271X. View

Huggins A, McTeague L, Davis M, Bustos N, Crum K, Polcyn R . Neighborhood Disadvantage Associated With Blunted Amygdala Reactivity to Predictable and Unpredictable Threat in a Community Sample of Youth. Biol Psychiatry Glob Open Sci. 2022; 2(3):242-252. PMC: 9348572. DOI: 10.1016/j.bpsgos.2022.03.006. View

Karstens A, Ajilore O, Rubin L, Yang S, Zhang A, Leow A . Investigating the separate and interactive associations of trauma and depression on brain structure: implications for cognition and aging. Int J Geriatr Psychiatry. 2017; 32(11):1190-1199. PMC: 5638677. DOI: 10.1002/gps.4755. View

Hamilton M . A rating scale for depression. J Neurol Neurosurg Psychiatry. 1960; 23:56-62. PMC: 495331. DOI: 10.1136/jnnp.23.1.56. View

Whitfield-Gabrieli S, Nieto-Castanon A . Conn: a functional connectivity toolbox for correlated and anticorrelated brain networks. Brain Connect. 2012; 2(3):125-41. DOI: 10.1089/brain.2012.0073. View

Suarez G, Burt S, Gard A, Burton J, Clark D, Klump K . The impact of neighborhood disadvantage on amygdala reactivity: Pathways through neighborhood social processes. Dev Cogn Neurosci. 2022; 54:101061. PMC: 8777301. DOI: 10.1016/j.dcn.2022.101061. View

Carvalho J, Tommet D, Crane P, Thomas M, Claxton A, Habeck C . Deconstructing racial differences: the effects of quality of education and cerebrovascular risk factors. J Gerontol B Psychol Sci Soc Sci. 2014; 70(4):545-56. PMC: 4542888. DOI: 10.1093/geronb/gbu086. View

10.

Powell-Wiley T, Baumer Y, Osei Baah F, Baez A, Farmer N, Mahlobo C . Social Determinants of Cardiovascular Disease. Circ Res. 2022; 130(5):782-799. PMC: 8893132. DOI: 10.1161/CIRCRESAHA.121.319811. View

11.

Boots E, Zhan L, Dion C, Karstens A, Peven J, Ajilore O . Cardiovascular disease risk factors, tract-based structural connectomics, and cognition in older adults. Neuroimage. 2019; 196:152-160. PMC: 6713222. DOI: 10.1016/j.neuroimage.2019.04.024. View

12.

Bronas U, Steffen A, Dion C, Boots E, Arfanakis K, Marquez D . Sedentary Time and White Matter Hyperintensity Volume in Older Adults. Med Sci Sports Exerc. 2019; 51(8):1613-1618. PMC: 7282192. DOI: 10.1249/MSS.0000000000001957. View

13.

Smith J, Zhao W, Wang X, Ratliff S, Mukherjee B, Kardia S . Neighborhood characteristics influence DNA methylation of genes involved in stress response and inflammation: The Multi-Ethnic Study of Atherosclerosis. Epigenetics. 2017; 12(8):662-673. PMC: 5687339. DOI: 10.1080/15592294.2017.1341026. View

14.

Heredia N, Xu T, Lee M, McNeill L, Reininger B . The Neighborhood Environment and Hispanic/Latino Health. Am J Health Promot. 2021; 36(1):38-45. PMC: 8671146. DOI: 10.1177/08901171211022677. View

15.

Muscatell K, Eisenberger N, Dutcher J, Cole S, Bower J . Links between inflammation, amygdala reactivity, and social support in breast cancer survivors. Brain Behav Immun. 2015; 53:34-38. PMC: 5784760. DOI: 10.1016/j.bbi.2015.09.008. View

16.

Folstein M, Folstein S, McHugh P . "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res. 1975; 12(3):189-98. DOI: 10.1016/0022-3956(75)90026-6. View

17.

Tawakol A, Osborne M, Wang Y, Hammed B, Tung B, Patrich T . Stress-Associated Neurobiological Pathway Linking Socioeconomic Disparities to Cardiovascular Disease. J Am Coll Cardiol. 2019; 73(25):3243-3255. PMC: 6767929. DOI: 10.1016/j.jacc.2019.04.042. View

18.

Miller G, White S, Chen E, Nusslock R . Association of Inflammatory Activity With Larger Neural Responses to Threat and Reward Among Children Living in Poverty. Am J Psychiatry. 2020; 178(4):313-320. PMC: 8016707. DOI: 10.1176/appi.ajp.2020.20050635. View

19.

Powell-Wiley T, Moore K, Allen N, Block R, Evenson K, Mujahid M . Associations of Neighborhood Crime and Safety and With Changes in Body Mass Index and Waist Circumference: The Multi-Ethnic Study of Atherosclerosis. Am J Epidemiol. 2017; 186(3):280-288. PMC: 5860351. DOI: 10.1093/aje/kwx082. View

20.

Bailey E, Malecki K, Engelman C, Walsh M, Bersch A, Martinez-Donate A . Predictors of discordance between perceived and objective neighborhood data. Ann Epidemiol. 2014; 24(3):214-21. PMC: 3947547. DOI: 10.1016/j.annepidem.2013.12.007. View