Neighborhood Disadvantage Associated With Blunted Amygdala Reactivity to Predictable and Unpredictable Threat in a Community Sample of Youth

Abstract

Background: Childhood socioeconomic disadvantage is a form of adversity associated with alterations in critical frontolimbic circuits involved in the pathophysiology of psychiatric disorders. Most work has focused on individual-level socioeconomic position, yet individuals living in deprived communities typically encounter additional environmental stressors that have unique effects on the brain and health outcomes. Notably, chronic and unpredictable stressors experienced in the everyday lives of youth living in disadvantaged neighborhoods may impact neural responsivity to uncertain threat.

Methods: A community sample of children (N = 254) ages 8 to 15 years (mean = 12.15) completed a picture anticipation task during a functional magnetic resonance imaging scan, during which neutral and negatively valenced photos were presented in a temporally predictable or unpredictable manner. Area Deprivation Index (ADI) scores were derived from participants' home addresses as an index of relative neighborhood disadvantage. Voxelwise analyses examined interactions of ADI, valence, and predictability on neural response to picture presentation.

Results: There was a significant ADI × valence interaction in the middle temporal gyrus, anterior cingulate cortex, hippocampus, and amygdala. Higher ADI was associated with less amygdala activation to negatively valenced images. ADI also interacted with predictability. Higher ADI was associated with greater activation of lingual and calcarine gyri for unpredictably presented stimuli. There was no three-way interaction of ADI, valence, and predictability.

Conclusions: Neighborhood disadvantage may impact how the brain perceives and responds to potential threats. Future longitudinal work is critical for delineating how such effects may persist across the life span and how health outcomes may be modifiable with community-based interventions and policies.

Figure 1

Depiction of example blocks in experimental paradigm. In predictable blocks, a clock ticks until the clock hand reaches the 12 o’clock position and the clock face is filled with red. Then, a picture that is either neutral or negative in valence is presented. In unpredictable blocks, the clock hand changes position randomly and does not indicate when the picture will be presented. Rows A and B depict predictable neutral and unpredictable negative blocks, respectively.

Figure 2

Frequency of Area Deprivation Index (ADI) scores in sample (N = 254). Dotted line represents sample mean of 40.57 (SD = 25.59).

Figure 3

Box plot depicts Area Deprivation Index (ADI) frequency by racial group. White participants (n = 138) lived in significantly less disadvantaged neighborhoods (mean = 29.612, SD = 19.95) compared with Black participants (n = 71, mean = 59.51, SD = 23.11). Other racial groups were excluded due to small cell sizes.

Figure 4

Clusters depict significant interactions of Area Deprivation Index with task conditions (valence, predictability), adjusted for age and gender with voxelwise p < .001 and cluster threshold p < .05. (A) Greater neighborhood disadvantage was associated with greater activation in the middle temporal gyrus (62, −24, −16) and less activation in the parahippocampal gyrus (36, –28, −18) for negative versus neutral images. (B) Greater neighborhood disadvantage was associated with greater activation in the lingual gyrus (−22, −88, −16) and parahippocampal gyrus (34, −32, −12) for unpredictable versus predictable images.

Figure 5

Neighborhood disadvantage associated with blunted amygdala response to negatively valenced stimuli (k = 70 voxels [18, −4, −16] and k = 58 voxels [−18, −4, −18]). Scatterplot depicts association between Area Deprivation Index (ADI) and activation in the right amygdala cluster.