ArticlePublisher preview available

Differential Developmental Associations of Material Hardship Exposure and Adolescent Amygdala–Prefrontal Cortex White Matter Connectivity

Journal of Cognitive Neuroscience

September 2022
34(10):1866-1891

DOI:10.1162/jocn_a_01801

Authors:

Leigh Gayle Goetschius

The Hilltop Institute at University of Maryland, Baltimore County

Melissa K Peckins

St. John's University

Show all 10 authorsHide

Accumulating literature has linked poverty to brain structure and function, particularly in affective neural regions; however, few studies have examined associations with structural connections or the importance of developmental timing of exposure. Moreover, prior neuroimaging studies have not used a proximal measure of poverty (i.e., material hardship, which assesses food, housing, and medical insecurity) to capture the lived experience of growing up in harsh economic conditions. The present investigation addressed these gaps collectively by examining the associations between material hardship (ages 1, 3, 5, 9, and 15 years) and white matter connectivity of frontolimbic structures (age 15 years) in a low-income sample. We applied probabilistic tractography to diffusion imaging data collected from 194 adolescents. Results showed that material hardship related to amygdala–prefrontal, but not hippocampus–prefrontal or hippocampus–amygdala, white matter connectivity. Specifically, hardship during middle childhood (ages 5 and 9 years) was associated with greater connectivity between the amygdala and dorsomedial pFC, whereas hardship during adolescence (age 15 years) was related to reduced amygdala–orbitofrontal (OFC) and greater amygdala–subgenual ACC connectivity. Growth curve analyses showed that greater increases of hardship across time were associated with both greater (amygdala–subgenual ACC) and reduced (amygdala–OFC) white matter connectivity. Furthermore, these effects remained above and beyond other types of adversity, and greater hardship and decreased amygdala–OFC connectivity were related to increased anxiety and depressive symptoms. Results demonstrate that the associations between material hardship and white matter connections differ across key prefrontal regions and developmental periods, providing support for potential windows of plasticity for structural circuits that support emotion processing.

3-D renderings of amygdala to specific pFC targets. Seed amygdala targets in dark gray. pFC targets: left sgACC BA 25 (red); right dmPFC BA 10 (plum); right OFC BA 11 (blue); right sgACC BA 25 (green); right OFC BA 47 (yellow). White matter is illustrated in light gray. White matter in figure depicts all tracts originating from seed amygdala region for illustration purposes.

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Significant associations between material hardship at specific developmental stages and white matter connectivity after adjusting for other developmental stages. White matter connectivity and target on the left and zero-order plots on the right. (A) Increased material hardship at ages 5 and 9 years was related to increased right amygdala–dmPFC white matter connectivity, adjusting for other developmental stages. (B) Increased material hardship at age 15 years was related to increased left amygdala–sgACC white matter connectivity, adjusting for other developmental stages. (C) Increased material hardship at age 15 years was related to decreased right amygdala–OFC white matter connectivity, adjusting for other developmental stages.

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Covariates-adjusted model using structural equation modeling including all material hardship predictors and white matter connectivity targets. Model fit statistics indicate excellent fit: χ²[45] = 47.931, p = .355; RMSEA = .019 [.000, .053], CFI = .980, TLI = .965, SRMR = .047. Consistent with regression results, there were positive associations between material hardship at age 5 years with right amygdala–BA 10 (dmPFC) and hardship at age 15 years with left amygdala–BA 25 (sgACC). Furthermore, there were trending negative associations between material hardship at ages 9 and 15 years with right amygdala–BA 11 (OFC) white matter connectivity. Covariates included in the model: ethnoracial identity, sex, pubertal age, birth city, maternal education, family structure, violence exposure, social deprivation, and annual household income at baseline. ⁺p < .10. *p < .05. **p < .01. ***p < .001.

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Growth curve trajectory illustrating that material hardship increases with age. Figure shows linear estimated paths for each individual (black lines) as well as mean estimated group-level path trajectory (blue). Material hardship at age 1 year is set as point 0, where estimated mean [SE] for starting point (i.e., intercept) = 1.01 [.077], p < .001; variance [SE] = 0.91 [0.166], p < .001, and estimated mean [SE] change over time (slope) = 0.02 [0.008], p = .009; variance [SE] = 0.01 [0.002], p = .004.

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Structural equation path model showing path estimates between material hardship predictors and right amygdala–BA 10, right amygdala–BA 11, and left amygdala–BA 25 white matter connectivity. Material hardship at 1, 3, 5, 9, and 15 loadings estimating latent slope were fixed at 0, 2, 4, 8, and 14, respectively. Covariates included in the model: ethnoracial identity, sex, pubertal age, birth city, maternal education, family structure, violence exposure, social deprivation, and annual household income at baseline. *p < .05. **p < .01.

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Differential Developmental Associations of Material

Hardship Exposure and Adolescent Amygdala–Prefrontal

Cortex White Matter Connectivity

Felicia A. Hardi

, Leigh G. Goetschius

1,2

, Melissa K. Peckins

, Jeanne Brooks-Gunn

Sara S. McLanahan

, Vonnie McLoyd

, Nestor L. Lopez-Duran

, Colter Mitchell

Luke W. Hyde

, and Christopher S. Monk

Abstract

■Accumulating literature has linked poverty to brain structure

and function, particularly in affective neural regions; however,

few studies have examined associations with structural connec-

tions or the importance of developmental timing of exposure.

Moreover, prior neuroimaging studies have not used a proximal

measure of poverty (i.e., material hardship, which assesses food,

housing, and medical insecurity) to capture the lived experience

of growing up in harsh economic conditions. The present

investigation addressed these gaps collectively by examining

the associations between material hardship (ages 1, 3, 5, 9, and

15 years) and white matter connectivity of frontolimbic struc-

tures (age 15 years) in a low-income sample. We applied proba-

bilistic tractography to diffusion imaging data collected from 194

adolescents. Results showed that material hardship related to

amygdala–prefrontal, but not hippocampus–prefrontal or

hippocampus–amygdala, white matter connectivity. Specifically,

hardship during middle childhood (ages 5 and 9 years) was asso-

ciated with greater connectivity between the amygdala and

dorsomedial pFC, whereas hardship during adolescence (age

15 years) was related to reduced amygdala–orbitofrontal (OFC)

and greater amygdala–subgenual ACC connectivity. Growth

curve analyses showed that greater increases of hardship across

time were associated with both greater (amygdala–subgenual

ACC) and reduced (amygdala–OFC) white matter connectivity.

Furthermore, these effects remained above and beyond other

types of adversity, and greater hardship and decreased

amygdala–OFC connectivity were related to increased anxiety

and depressive symptoms. Results demonstrate that the associa-

tions between material hardship and white matter connections

differ across key prefrontal regions and developmental periods,

providing support for potential windows of plasticity for struc-

tural circuits that support emotion processing. ■

INTRODUCTION

In the United States, 16.2%, or approximately 11.9 million,

children and adolescents live below the poverty line, and

32% are near poor (within 200% of the poverty line;

Semega, Kollar, Creamer, & Mohanty, 2019). Children

who grow up in poverty are at an increased risk for adverse

outcomes, including behavioral problems, psychopathol-

ogy, and delayed cognitive development (Brooks-Gunn

& Duncan, 1997). Research has shown that neural regions

involved in emotion processing such as the pFC, amyg-

dala, and hippocampus are implicated in the effects of

poverty and adverse developmental outcomes (Merz,

Tottenham, & Noble, 2018; Kim et al., 2013; Luby et al.,

2013; Noble, Houston, Kan, & Sowell, 2012; Hanson,

Chandra, Wolfe, & Pollak, 2011). Despite evidence linking

poverty to brain function (e.g., functional activation and

connectivity) and structure (e.g., cortical volume and sur-

face area; Farah, 2017; Johnson, Riis, & Noble, 2016; Brito

& Noble, 2014), much less work has focused on its associ-

ation with structural connectivity (i.e., white matter tracts

that facilitate communication between distinct neural

structures) in adolescence. Moreover, although the effects

of economic hardship differ across development (Green,

Stritzel, Smith, Popham, & Crosnoe, 2018; Duncan, Yeung,

Brooks-Gunn, & Smith, 1998), most existing investigations

on neural correlates of poverty have not considered the

critical importance of developmental timing in the experi-

ence of economic hardship (Hyde et al., 2020). Thus, more

research is needed to examine how economic hardship

across development relates to adolescent white matter

tracts that link emotion processing regions.

Although most studies examining frontolimbic white

matter structures using diffusion MRI (dMRI) have focused

on density of major white matter tracts (e.g., fractional

anisotropy of the superior longitudinal fasciculus; Rosen,

Sheridan, Sambrook, Meltzoff, & McLaughlin, 2018; Noble,

This article is part of a Special Focus entitled Finances and Feel-

ings: The Affective Neuroscience of Poverty; deriving from a

symposium at the 2020 Annual Meeting of the Cognitive Neu-

roscience Society.

University of Michigan,

University of Maryland,

St. John’s

University, Queens, NY,

Columbia University,

Princeton

University

https://doi.org/10.1162/jocn_a_01801

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The amygdala is critically involved in processing emotion. Through bidirectional connections, the prefrontal cortex (PFC) is hypothesized to influence amygdala reactivity. However, research that elucidates the nature of amygdala-PFC interactions - through mapping amygdala-prefrontal tracts, quantifying variability among tracts, and linking this variability to amygdala activation - is lacking. Using probabilistic tractography to map amygdala-prefrontal white matter connectivity in 142 adolescents, the present study found that white matter connectivity was greater between the amygdala and the subgenual cingulate, orbitofrontal (OFC), and dorsomedial (dmPFC) prefrontal regions than with the dorsal cingulate and dorsolateral regions. Then, using a machine-learning regression, we found that greater amygdala-PFC white matter connectivity related to attenuated amygdala reactivity. This effect was driven by amygdala white matter connectivity with the dmPFC and OFC, supporting implicit emotion processing theories which highlight the critical role of these regions in amygdala regulation. This study is among the first to map and compare specific amygdala-prefrontal white matter tracts and to relate variability in connectivity to amygdala activation, particularly among a large sample of adolescents from a well-sampled study. By examining the association between specific amygdala-PFC tracts and amygdala activation, the present study provides novel insight into the nature of this emotion-based circuit.

Differential Developmental Associations of Material Hardship Exposure and Adolescent Amygdala–Prefrontal Cortex White Matter Connectivity

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