Approximately 40.6 million people live in poverty in the United States and of these, 7.3 million are children (Smega et al., 2017). Living in disadvantaged, poverty-stricken neighborhoods can have a profound impact on a child’s development, including his or her neural development (McLaughlin et al., 2013; Sheridan & McLaughlin, 2014). Neighborhood disadvantage and community violence exposure are common experiences in poor, urban areas (Benson et al., 2003; Friedson & Sharkey, 2015), and appear to affect neural development (Perkins & Graham-Bermann, 2012; Sheridan & McLaughlin, 2014). Atypical development of brain regions that control emotion processes can ultimately have a negative impact on mental health (Hill et al., 2005; McEwen & Gianaros, 2010; Ross & Mirowsky, 2001). The prefrontal cortex (PFC), hippocampus, amygdala, and hypothalamus control emotional function and are connected by large white matter pathways (i.e., cingulum bundle, uncinate fasciculus, stria terminalis, and fornix) that carry signals between these brain regions. Changes in the microstructure of these white matter pathways alter emotional function (Fields, 2008). Therefore, the impact neighborhood disadvantage and violence exposure have on emotional function may be mediated, in part, by changes in the microstructure of these white matter pathways. Determining the relationship neighborhood disadvantage and violence exposure have with the white matter that connects these brain regions may provide novel insights into neural processes that may explain the relationships neighborhood disadvantage and violence exposure have with emotional function.

Neighborhood disadvantage shows a robust association with the emotional development of children. Specifically, children raised in disadvantaged neighborhoods are more susceptible to internalizing (e.g., anxiety and depression) and externalizing (e.g., conduct problems) disorders (Goodnight et al., 2012; Hackman et al., 2012; Susman et al., 1997; Xue et al., 2005). Although little is known about the neural mechanisms through which neighborhood disadvantage affects the emotional development of children, prior work has linked the PFC, hippocampus, and amygdala to the internalizing symptoms that are associated with anxiety and depression (Burghy et al., 2012; MacMillan et al., 2003). Further, the hippocampus and amygdala have been linked to externalizing behaviors that are often observed in conduct and other behavioral disorders (Davidson et al., 2000; Hanson et al., 2015; Hill et al., 2005). These findings suggest that the PFC, hippocampus, and amygdala play a fundamental role in emotion expression and regulation processes that are important for healthy emotional function.

Similar to neighborhood disadvantage, exposure to violence during adolescence affects emotional development. Violence exposure during childhood and adolescence increases stress levels, which, in turn, may alter brain development and lead to emotional dysfunction (Mead et al., 2010). Further, repeated exposure to violence increases stress, leading to the disproportionate use of neural pathways that underlie the stress response, which alters emotion expression and regulation processes (Perry & Pollard, 1998). Thus, elevated stress linked to violence exposure may lead to the disproportionate use of these white matter pathways, altering their microstructure and resulting in long term changes in emotional function. In fact, prior research has linked childhood experiences of parental verbal abuse to decreased white matter microstructure of the cingulum bundle and fornix, which connect brain regions that are associated with depression and anxiety (e.g., dorsomedial PFC, ventromedial PFC, hippocampus, and hypothalamus) (Choi et al., 2009).

The PFC, hippocampus, amygdala, and hypothalamus are connected by large white matter fibers (i.e., bundles of myelinated axons) that support communication between these brain regions. The anterior portion of the cingulum bundle connects medial regions of the PFC, including the dorsomedial PFC and ventromedial PFC (Bubb et al., 2018; Catani & Thiebaut de Schotten, 2008). In turn, the uncinate fasciculus extends from the ventromedial PFC to the anterior temporal lobe (Catani & Thiebaut de Schotten, 2008; Von Der Heide et al., 2013). Finally, the stria terminalis and fornix connect the amygdala and hippocampus to the hypothalamus (Catani & Thiebaut de Schotten, 2008; Kamali et al., 2015; Kwon et al., 2011; Mori et al., 2008). Reductions in the microstructure of the cingulum bundle, uncinate fasciculus, stria terminalis, and fornix have been linked to impaired emotional control (e.g., bipolar disorder, generalized anxiety disorder, major depressive disorder, and posttraumatic stress disorder) (Bae et al., 2006; Barysheva et al., 2013; Benedetti et al., 2011; Harnett et al., 2018; Harris et al., 2008; Korgaonkar et al., 2011; Lin et al., 2011; Phan et al., 2009). Further, reductions of stria terminalis and fornix microstructure have also been found among adolescents who engage in high risk behaviors (McQueeny et al., 2009). This prior work suggests that the microstructure of the white matter tracts that connect the PFC and limbic system plays an important role in emotional health.

Prior research has demonstrated that the brain matures in stages, with the most growth between 7 and 11 years of age (Epstein, 1986). However, white matter pathways continue to develop throughout childhood, adolescence, and young adulthood (Paus et al., 2001; Schmithorst et al., 2005). While the maturation of some white matter pathways (e.g., superior longitudinal fasciculus, inferior longitudinal fasciculus) is largely completed by adolescence, the white matter pathways that support emotion processes (e.g., cingulum bundle, uncinate fasciculus, stria terminalis, fornix) continue to develop into young adulthood (Asato et al., 2010; Steinberg, 2005). This longer developmental timeline may leave these white matter pathways and the brain regions they connect vulnerable to the disruptive effects of neighborhood disadvantage and violence exposure during adolescence. Disadvantaged neighborhoods and exposure to violence may alter the development of the white matter that connects the PFC, hippocampus, amygdala, and hypothalamus during adolescence, thereby increasing the risk of emotional dysfunction.

The current study investigated the relationship between neighborhood disadvantage and violence exposure during adolescence and QA of the cingulum bundle, uncinate fasciculus, stria terminalis/fornix in young adulthood. We hypothesized that the QA of these white matter pathways would vary negatively with neighborhood disadvantage and violence exposure. Determining the relationship that neighborhood disadvantage and violence exposure have with the QA of the cingulum bundle, uncinate fasciculus, stria terminalis, and fornix will provide new insights into the impact adolescent experiences have on brain development.

Adolescence is a pivotal period of neural development during which the white matter tracts that connect the PFC, hippocampus, amygdala, and hypothalamus continue to mature (Asato et al., 2010; Bava et al., 2010). These white matter tracts support important emotional processes (Zheng et al., 2018). In fact, prior research has demonstrated that the development of healthy emotional function parallels the maturation of these white matter pathways (Bolhuis et al., 2019; Nagy et al., 2004). Therefore, adverse environmental conditions during adolescence may disrupt the typical neurodevelopment of white matter in these areas, which may ultimately alter emotional function. The present study investigated the relationship that adolescent neighborhood disadvantage and violence exposure have with the QA of white matter pathways that are important for healthy emotional function (i.e., cingulum bundle, uncinate fasciculus, stria terminalis, and fornix). The present results demonstrate that greater neighborhood disadvantage during adolescence (i.e., assessed at age 11) is associated with reduced QA of the cingulum bundle, uncinate fasciculus, and stria terminalis/fornix in young adulthood (i.e., assessed at age 20). These findings suggest that the neighborhood environment in which children live may play an important role in the development of white matter pathways that are linked to emotion expression and regulation. However, neighborhood disadvantage was closely related to family income. Both neighborhood disadvantage and family income demonstrated similar relationships with QA, suggesting that these relationships apply to the broader socioeconomic context during development and adolescence – as experienced within the family and neighborhood.

The PFC, hippocampus, amygdala, and hypothalamus are important components of a neural circuit that supports emotion expression and regulation. These brain regions are connected by white matter pathways that include the cingulum bundle, uncinate fasciculus, stria terminalis, and fornix. Reduced microstructure within these white matter pathways has been previously linked to emotion dysregulation. Specifically, reduced microstructure of the cingulum bundle has been implicated in depression, anxiety, and posttraumatic stress disorder (Bubb et al., 2018; Davis et al., 1997; Harnett et al., 2018; Tröstl et al., 2011). Furthermore, decreased microstructure of the uncinate fasciculus has been implicated in social anxiety disorder and childhood major depressive disorder (Adluru et al., 2017; LeWinn et al., 2014; Tröstl et al., 2011). Similarly, reduced microstructure of the stria terminalis/fornix appears to play an important role in depression (Korgaonkar et al., 2011). Therefore, disruption of the microstructure of these white matter pathways may impair neural communication between the PFC, hippocampus, amygdala, and hypothalamus, resulting in maladaptive emotion expression and regulation and ultimately long-term emotional dysfunction. The disruption of these pathways may help to explain the higher prevalence of psychiatric disorders in individuals growing up in economically disadvantaged contexts (Johnson et al., 2011; McLaughlin et al., 2011) Thus, the current findings have important implications regarding the neural impact of the larger socioeconomic environment in which a child is raised. Our findings suggest that growing up in disadvantaged families and neighborhoods may alter the development of white matter pathways that are important for the neural communication that supports emotional processes.

Prior work that has investigated the relationship between family income and white matter structure support the present findings. This prior research examined family income as an income-to-needs ratio and found that as family income decreased, microstructure of the cingulum bundle and uncinate fasciculus decreased (Dufford & Kim, 2017). However, family income is only one of many variables that factor into neighborhood disadvantage (Finch et al., 2010; Santiago et al., 2011). Therefore, the current study focused on a broader range of integrated environmental factors that comprise neighborhood disadvantage, rather than on family income alone. Our findings suggest that both family income and the neighborhood in which a child is raised (or factors associated with these socioeconomic indicators) may have a significant impact on white matter development. In fact, low family income and high neighborhood disadvantage constitute environmental deprivation, as conceptualized in McLaughlin and Sheridan’s model of childhood adversity (McLaughlin et al., 2014; McLaughlin & Sheridan, 2016). According to this framework, childhood adversity that is characterized by significant deprivation (e.g., lack of caregiver support and impoverished environment) may negatively affect neurodevelopmental processes, such as synaptic pruning and myelination (McLaughlin et al., 2017). The present findings are consistent with the expected outcomes of deprivation. Specifically, we observed that as neighborhood disadvantage increased and family income decreased, the QA of the cingulum bundle, uncinate fasciculus, and stria terminalis/fornix decreased. The decreased QA of these white matter pathways may affect emotional function and may ultimately influence susceptibility to psychopathology.

In contrast to the findings with neighborhood disadvantage and family income, QA did not vary with violence exposure in any tract (i.e., cingulum bundle, uncinate fasciculus, and stria terminalis/fornix). Although previous research suggests that violence exposure may have deleterious effects on white matter tracts that include the cingulum bundle and fornix (Choi et al., 2009; Lu et al., 2013), we were not able to replicate these prior findings in the present study. Differences between the findings of the present study and prior work (Choi et al., 2009; Lu et al., 2013) may be due to differences in the conceptualization of violence exposure. Prior work examined the impact of childhood trauma (i.e., emotional abuse, physical abuse, sexual abuse, emotional neglect, and physical neglect; Choi et al., 2009; Lu et al., 2013), while the current study examined the impact of community-based violence exposure (i.e., threatened with or without a weapon, physical attacks, or witnessing others being threatened or physically attacked). Thus, these differences in the conceptualization of violence exposure may account for inconsistencies between the present study and prior research.

Results of the present investigation should be interpreted with several considerations. First, the assessment of neighborhood disadvantage took place when participants were approximately 11 years of age, while neuroimaging was completed when participants were around 20 years of age. Thus, there was a relatively long period of time between the collection of neighborhood disadvantage and neuroimaging data. The larger study from which these data were drawn did not have resources to geocode addresses after T1 of data collection. Therefore, addresses were updated so participants could be contacted, but were not systematically maintained. Thus, we were unable to determine whether participants’ exposure to neighborhood disadvantage changed across adolescence. Tracking the impact of neighborhood disadvantage across adolescence is an important area for future exploration. Longitudinal evaluation of neighborhood disadvantage would provide further information regarding how changing levels of neighborhood disadvantage might impact the development of white matter across time. Additionally, participants did not complete any cognitive assessments as part of the present investigation. Thus, we were unable to evaluate the relationship our findings have with cognitive ability. Further, the present study used an average QA value for each participant across each tract of interest, consistent the with procedures used in prior work (Acheson, Wijtenburg, Rowland, Bray, et al., 2014; Acheson, Wijtenburg, Rowland, Winkler, et al., 2014; Harnett et al., 2018; Squeglia et al., 2015). Thus, the full microstructural complexity of each tract was not examined. Although this does not directly limit the findings of the current work, a more complete characterization of the tracts examined in the present study may be a fruitful avenue for future investigation. Finally, results pertaining to the stria terminalis/fornix should be interpreted with caution. The parameters of the diffusion weighted imaging may not have had adequate resolution to accurately reconstruct very small tracts, such as the stria terminalis and fornix, due to crossing fibers and partial volume effects. Although prior work suggests that QA is better able to resolve crossing fibers and manage partial volume effects than other diffusion metrics, (Yeh et al., 2013), results for the stria terminalis/fornix should be interpreted with caution.

The present study found that neighborhood disadvantage and low family income in adolescence (i.e., assessed at age 11) varied with the QA of the cingulum bundle, uncinate fasciculus, and stria terminalis/fornix in young adulthood (i.e., assessed at age 20). These findings suggest that a developing child’s socioeconomic context can have a meaningful impact on the QA of white matter tracts that are important for emotional function. Reductions in the QA of these white matter tracts could interfere with normal, healthy emotion processes. The disruption of healthy neural function may, in turn, interfere with neural maturation during key development stages, and ultimately lead to the dysfunction of important emotional processes during adulthood (e.g., mood and anxiety disorders).