Abstract Facets of the post-natal environment including the type and complexity of environmental stimuli, the quality of parenting behaviors, and the amount and type of stress experienced by a child affects brain and behavioral functioning. Poverty is a type of pervasive experience that is likely to influence biobehavioral processes because children developing in such environments often encounter high levels of stress and reduced environmental stimulation. This study explores the association between socioeconomic status and the hippocampus, a brain region involved in learning and memory that is known to be affected by stress. We employ a voxel-based morphometry analytic framework with region of interest drawing for structural brain images acquired from participants across the socioeconomic spectrum (n = 317). Children from lower income backgrounds had lower hippocampal gray matter density, a measure of volume. This finding is discussed in terms of disparities in education and health that are observed across the socioeconomic spectrum.

Citation: Hanson JL, Chandra A, Wolfe BL, Pollak SD (2011) Association between Income and the Hippocampus. PLoS ONE 6(5): e18712. https://doi.org/10.1371/journal.pone.0018712 Editor: Monica Uddin, University of Michigan, United States of America Received: September 15, 2010; Accepted: March 16, 2011; Published: May 4, 2011 Copyright: © 2011 Hanson et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: This work was supported by the US National Institute on Drug Abuse (Grant DA028087 to JLH), the US National Institute of Mental Health (Grants MH61285 and MH68858 to SDP) and the Children's Bureau of the Administration on Children, Youth and Families as part of the Child Neglect Research Consortium. This project was also supported by the Russell Sage Foundation and the University of Wisconsin-Madison Graduate School grants to BLW. The authors also thank the Russell Sage Foundation for their support of Health and SES working group. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist.

Introduction A growing body of research, conducted mainly in rodents, has found that factors such as the complexity of stimuli present in the post-natal environment, the quality of parenting behaviors, and the amount of stress that occurs during the lifespan can affect neural, emotional and cognitive functioning (for review, see [1], [2]). These findings raise complex questions about how variations in the environment can shape neural development in humans [3]. In particular, an increasing interest is being paid to the effects of socioeconomic status and poverty on brain and behavior, since living in poverty is often characterized by heightened amounts of stress and reductions in environmental stimulation [4]. This study focuses on associations between household income and the hippocampus. The hippocampus is located in the medial temporal lobe of the brain. This region is known to be affected by stress and is tied to cognitive functions such as learning, memory, and behavioral regulation (for review, see [5]). It is difficult to quantify the many facets of an individual's environment; for this reason, we use income as a proxy for a multitude of factors including enriched cultural environment, better schools and neighborhoods, and access to stimulating materials in early childhood. Non-human animal research has found environmental enrichment is related to greater dendritic branching and wider dendritic fields [6], [7], increased astrocyte number and size [8], and improved synaptic transmission [9] in portions of the hippocampus. Environmental enrichment, in addition, appears to bolster neurobiological resiliency. For example, enriched environments result in increases in neuronal precursor cells in portions of the hippocampus [10] and greater recovery after a lesion in the hippocampus [11]. Stress also exerts long-lasting negative effects on the hippocampus. For example, research has found prolonged maternal separation and brief handling impacts the hippocampus and affects stress regulation and memory ability later in life [12]. Similar effects have been noted in humans. These studies suggest that parental nurturance and environmental stimulation, including both resources such as the number of books in a child's home and parental time spend reading to a child, predict neurocognitive performance on tests related to the hippocampus such as long-term memory [13], [14]. Prior research has linked poverty with a myriad of deleterious outcomes from poor health to lower educational achievement [15], [16], [17], [18]. Yet little is currently understood about the neurobiological mechanisms leading to these socioeconomic disparities. We hypothesized that the morphometric properties of hippocampus would be related to gradients in income. We focus on this brain region both because of its known sensitivity to environmental stress and its role in core adaptive processes such as learning.

Discussion This study was designed to examine the possible association between household family income and the hippocampus, a brain region central to many important cognitive and emotional processes. We identified an association with the hippocampus and income, as hypothesized. The hippocampus has previously been found to be associated with quality of environmental input and stress. Taken together, these findings suggest that differences in the hippocampus, perhaps due to stress tied to growing up in poverty, might partially explain differences in long-tern memory, learning, control of neuroendocrine functions, and modulation of emotional behavior. These results are consistent with research on neuropsychological differences across the SES gradient (for review, see [31]). Farah and colleagues [13], [32] along with Rao et al. [14] found environmental stimulation and parental nurturance was related to memory functioning in childhood. Such long-term memory functions are mediated by the hippocampus [33]. Variations in hippocampal size have been associated with memory performance with larger hippocampal volumes being related to better memory performance [34]. In addition, higher levels of chronic life stress appear to be associated with smaller hippocampal volumes in adults [35]. These results add to the modest body of research examining neurobiological associations with socioeconomic status, providing one potential neurobiological mechanism through which the early environment may convey risk for a host of deleterious outcomes. In contrast to previous research linking amygdala volume and stress [36], we did not observe associations for the amygdala and income. Amygdala quantification is very challenging and even with such a large sample size, automated methods may not be appropriate. Follow-up analyses using a different method of automated segmentation however yielded similar results (see Supplemental Materials S1). In addition, associations between the amygdala and early life stress effects may vary by age of measurement (for discussion, see [37]). For example, increases in amygdala volume may be seen early in development after the experience of stress, while small amygdala volume may occur later in development. The structural imaging project presented here does not address issues of causation: poverty carries multiple components of environmetal risk and many factors may affect the development of brain structure. Future research should longitudinally assay both brain structure and function, as understanding both factors are likely central to truly understanding associations between neurobiological outcomes and income. Additional work should also include a variety of neuropsychological assessment, as the cognitive tests employed in this study were predominantly “prefrontal-dependent”: tapping rule acquisition and working memory. Subsequent studies must also aim to delineate the effects of household income, environmental stimulation, stress, and other variables such as possible nutritional differences related to poverty with large samples of children living in poverty. Such research designs will further increase understanding the neurobiological correlates of poverty and socioeconomic status. This study examined a large group of children and adolescents from 5 different research sites around the United States. Although issues of race and ethnicity were not the focus of our study, these factors may be associated with variations in neural development. Preliminary analyses suggested that our effects held for Caucasian and non-Caucasian participants. Future research should focus on exploring ethnic diversity with appropriately sized samples across income categories. Of important note, the NIH data set was also designed with a plan to screenout individuals with mental health issues or very low intelligence. This design skews the sample because psychopathology and learning disorders are disproportionately represented among impoverished children. The present results therefore reflect so-called “normal” children living in poverty. This suggests that the present results likely under-represent the true effects of poverty. Alternatively one could argue that the exclusionary criteria may strengthen the implications of our results as psychopathology or learning disorders as possible explanations of the association can largely be ruled out as factors lying behind the correlation. Understanding how environmental variations can affect neural, emotional and cognitive functioning in humans has major implications for both basic scientific questions and public policy initiatives. Such knowledge about the neural embedding of socioeconomic status, specifically poverty, may aid in the design and implementation of intervention programs addressing SES-related disparities in a cognitive and health outcomes. We found variations in socioeconomic status were associated with hippocampal volumes (as measured by gray matter probability). This finding suggests a potential neurobiological mechanism through which the early environment may convey risk for a host of deleterious outcomes from poor health to lower educational achievement. In addition to SES-related disparities, such results add to our understanding of human brain development, as we aim to further delineate how post-natal experiences may uniquely shape the brain and change behavior.

Acknowledgments We thank Jay Bhattacharya, Ed Moss, and the Health & SES working book group at the Russell Sage Foundation for helpful discussions.

Author Contributions Conceived and designed the experiments: JLH AC BLW SDP. Analyzed the data: JLH SDP. Contributed reagents/materials/analysis tools: JLH AC BLW SDP. Wrote the paper: JLH AC BLW SDP.