Abstract
Human neuroimaging studies have shown that people living in poverty tend to suffer hippocampal atrophy, which leads to impaired memory and learning throughout life. However, behavioral studies demonstrate that poor people with high self‐esteem are often exempt from the deleterious effect of poverty and instead possess a happy and successful life. Here we investigated whether high self‐esteem can buffer against the deleterious effects of poverty, as indicated by low subjective socioeconomic status (SSS), on the hippocampal gray matter volume (GMV) in a large cohort of young participants (N = 280). As expected, findings revealed that although low (vs. high) SSS was linked with a smaller hippocampal GMV, the deleterious effect of low SSS on hippocampal GMV was alleviated when the participants have high self‐esteem. Commonality analyses further confirmed this observation. The current study suggests that positive psychological resources such as self‐esteem may provide protection for the hippocampal atrophy in adversity. Hum Brain Mapp 37:3757–3766, 2016. © 2016 Wiley Periodicals, Inc.
Keywords: socioeconomic status, self‐esteem, hippocampus, resilience
Abbreviations
- FWHM
Full width at half maximum
- GLM
General linear model
- GM
Gray matter
- GMV
Gray matter volume
- IQR
Interquartiles
- MP‐RAGE
Magnetization prepared rapid gradient echo
- MRI
Magnetic resonance imaging
- SES
Socioeconomic status
- SSS
Subjective socioeconomic status
INTRODUCTION
In 2012, nearly one billion children, or every second child in the world, lived in poverty (cf. The Human Development Report, 2012), suffering various stressful life events, such as violence, hunger, poor health and abuse [Baum et al., 1999]. It has long been recognized that poverty has a deleterious effect not only on physical health but also on mental health and cognitive abilities [Adler et al., 1994; Conger and Donnellan, 2007]. Indeed, prior studies have revealed that the hippocampus, a critical neural substrate for regulating responses under stress, is adversely affected by chronic stress [Avishai‐Eliner et al., 2001; Fenoglio et al., 2006; Gianaros et al., 2007; Plotsky and Meaney, 1993]. Given that poverty and low socioeconomic status (SES) may be chronic sources of stress and adversity [Baum et al., 1999], it has also been implicated as a risk factor for problems with hippocampal structure and function. Structural magnetic resonance imaging (MRI) studies have revealed smaller hippocampus in children from low‐income families [Hanson et al., 2011; Jednorog et al., 2012], and such association remains detectable even more than 50 years later [Staff et al., 2012]. Higher SES, as reflected by educational attainment, may also serve as a buffer against age‐related reductions in hippocampal volume [Noble et al., 2012]). Because accumulating evidence from meta‐analyses converges to demonstrate the pivotal role of the hippocampus in memory and learning [Kühn and Gallinat, 2014; Martinelli et al., 2013], atrophy of the hippocampus may consequently further prevent children in low‐income families from higher achievement that could help them escape the cycle of poverty.
Previous studies have demonstrated that psychosocial resources can greatly buffer the deleterious effect of poverty [Creswell et al., 2005]. One such psychological resource is self‐esteem, which refers to one's overall subjective emotional evaluation of his or her own worth [Pan et al., 2016; Rosenberg, 1965]. That is, self‐esteem can either be positive (i.e., high self‐esteem) or negative (i.e., low self‐esteem). In the Kauai longitudinal Study, researchers tracked the development of 698 children born in 1955 on the island of Kauai in Hawaii. They found that children who lived in poverty but had high levels of self‐esteem developed into stable, competent, confident, and productive adults [Werner, 1995]. A similar result was observed in successful youth who grew up in London's high‐crime neighborhoods in the Longitudinal Cambridge Study [Werner, 1997]. Interestingly, individuals with high self‐esteem tend to have larger hippocampal volumes [Kubarych et al., 2012; Pruessner et al., 2005]. Given the protective role of self‐esteem against poverty in previous studies, we hypothesized that high self‐esteem promotes hippocampal resilience, especially in individuals in poverty.
To test this hypothesis, a large population of college students was recruited (N = 280), and voxel‐based morphometry (VBM) was used to examine whether the hippocampus of low SES participants was modulated by self‐esteem. Specifically, we first replicated the relationship between participants' hippocampal gray matter volume (GMV) and their social economic status, such that a higher SES would be linked with larger hippocampal GMV. Second, we measured participants' self‐esteem with the Rosenberg Self‐Esteem Scale [Rosenberg, 1965] and tested our prediction that high self‐esteem can buffer the deleterious effects of poverty on hippocampal GMV.
MATERIALS AND METHODS
Participants
Two hundred and eighty college students (138 males; mean age = 22.68 years, SD = 1.07 years) from Beijing Normal University, China, participated in this study as a part of an ongoing project investigating relation among genes, environment, brain and behavior [Kong et al., 2016; Song et al., 2014; Wang et al., in press]. Data that are irrelevant to the scope of this study were not reported in this study. The participants reported no past or current psychiatric illness or history of neurological disorders (e.g., epilepsy, traumatic brain injury, neurodegenerative disorders and cerebro‐vascular disease), mental retardation or significant systemic medical illness. Both the behavioral and MRI protocols were approved by the Institutional Review Board of Beijing Normal University. Written informed consents were obtained from all participants prior to the experiment.
Behavioral Measures
Socioeconomic Status (SES)
Participants' SES was assessed by the MacArthur Scale (youth version) of Subjective Social Status [Goodman et al., 2001], which measures individuals' subjective perception of their families' place on the social ladder. The subjective socioeconomic status (SSS) was selected because perceived social standing is more closely associated with stress‐related mental and physical health than objective SES (e.g., education, income and occupation) [Adler et al., 2000; Singh‐Manoux et al., 2005]. In this study, participants were presented a ten‐rung “social ladder” and asked to indicate the point that “best represents where your family was” during their development (i.e., childhood [6–12 years old], adolescent [12–18 years old] and youth [18–22 years old]) compared with other families in China. The participants were informed that at the top of the ladder was the most well‐to‐do family, with the most money, education and respected jobs, whereas families at the bottom were the worst off.
Self‐Esteem
Participants' self‐esteem was assessed in Chinese with an established and validated Chinese version of Rosenberg Self‐Esteem Scale [Wang et al., 2010; Yang and Wang, 2007], which contains ten items to assess one's global self‐worth, incorporating both positive and negative feelings about the self (e.g., “On the whole, I am satisfied with myself”). The participants were instructed to report the extent to which they agreed or disagreed with each statement using a 6‐point Likert‐type scale (1 = strongly disagree, 6 = strongly agree). The total score of self‐esteem was calculated by summing the scores of each item, and a higher score indicated a more positive evaluation of self‐worth and value.
MRI Acquisition
Participants were scanned using a Siemens 3T scanner (MAGENTOM Trio with a Tim system) with a 12‐channel phased‐array head coil at the BNU Imaging Center for Brain Research, Beijing, China. MRI structural images were acquired using a 3D magnetization prepared rapid gradient echo (MP‐RAGE) T1‐weighted sequence (TR/TE/TI = 2530/3.39/1100 ms, flip angle = 7 degrees, FOV = 256 × 256 mm2). One hundred and twenty‐eight contiguous sagittal slices were imaged with 1 × 1‐mm in‐plane resolution and 1.33‐mm slab thickness for whole brain coverage.
Image Processing for Voxel‐Based Morphometry
VBM was employed to characterize the neuroanatomical differences in GMV and neuroanatomical correlates of behavioral performance across participants [Ashburner and Friston, 2000]. Specifically, VBM was performed using SPM8 (Statistical Parametric Mapping, Wellcome Department of Imaging Neuroscience, London, UK) and Diffeomorphic Anatomical Registration through Exponentiated Lie Algebra (DARTEL, Wellcome Department of Imaging Neuroscience). First, image quality was assessed by visual examination. Second, the origin of each brain was manually set to the anterior commissure for each participant. Third, the images were segmented into four distinct tissue classes: gray matter (GM), white matter, cerebrospinal fluid and everything else (e.g., skull and scalp) using a unified segmentation approach [Ashburner and Friston, 2005]. Fourth, the GM images for each participant were rigidly aligned and resampled to 2 × 2 × 2 mm. Fifth, the images were nonlinearly registered with DARTEL, which involves iteratively computing a study‐specific template based on the tissue maps from all participants and then warping all participants' GM images into the generated template to increasingly improve the alignment [Ashburner, 2007]. Sixth, the GM images were normalized to standard MNI space, and the GM voxel values were modulated by multiplying the Jacobian determinants derived from the registration to preserve the volume of tissue from each structure [Good et al., 2002]. The modulated GM images were then smoothed with an 8‐mm full width at half maximum (FWHM) isotropic Gaussian kernel. Finally, to exclude noisy voxels, the modulated images were masked using an absolute masking with a threshold of 0.2. The masked modulated GM images were used for further statistical analyses.
Exclusion Criteria
In the measurement of self‐esteem, outliers were defined as two interquartiles (IQR) below the first quartile or two IQR above the third quartile. One participant (male) was excluded because his self‐esteem score was two IQRs below the first quartile. Another participant (male) was excluded from further analysis because of missing items in the questionnaire. In the measurement of neural substrate, another 6 participants (male, 2% of the sample) whose images had excessive scanner artifacts or showed gross anatomical abnormalities were excluded. Therefore, among all 280 participants tested, 272 participants (male: 130, age mean = 22.64, SD = 1.03 years) were include in the VBM analysis.
Statistical Analysis of VBM
Because the GM images were normalized to the standard MNI space, we defined the whole hippocampus using probabilistic maps from the Harvard‐Oxford Subcortical Structural Atlas implemented in FSL [the FMRIB Software Library, http://www.fmrib.ox.ac.uk/fsl (Smith et al., 2004)], and only included voxels that have 25% or greater probability of being labeled as the hippocampus. The total GMV of the right/left hippocampus was calculated by summarizing the probability values (or GMV) of all voxels within the right/left hippocampal mask from the modulated images. We also obtained the total hippocampal GMV by adding hippocampal GMVs of both hemispheres together.
To examine the deleterious effect of poverty on hippocampal GMV, an independent two‐sample t‐test was conducted to compare hippocampal GMV between the participants with high SSS (i.e., above the median) and the participants with low SSS (i.e., below the median). Because the disputed nature of the definition of poverty, the result found in the low SSS group was used to infer the deleterious effect of poverty on the hippocampus. Sex and the total GMV of the whole brain were treated as confounding covariates, which were regressed out from the variance of hippocampal GMV. Similar analyses were also conducted on hippocampal GMV in the right and left hemispheres separately to confirm the correlation between SSS and hippocampal GMV. Considering the participants tested were college students, who had a narrow range of ages (mean age = 22.64 years, SD = 1.03 years); therefore, we did not regress out the confounding factor of age.
To further examine whether the hippocampus was the primary and major brain region dampened by poverty, a whole‐brain t‐test analysis was performed by comparing the GMV of each voxel between low SSS and high SSS group. Sex and the total GMV of the whole brain were also treated as confounding covariates. Correction for multiple comparisons was applied using a non‐stationary whole‐brain cluster‐level correction (min t > 3.29, cluster significance: P < 0.01) [Hayasaka et al., 2004].
Finally, we explored whether high self‐esteem could buffer against the deleterious effect of poverty on hippocampal GMV. To this end, a general linear model (GLM) was performed to test the effects of SSS, self‐esteem, and their interaction on participants' hippocampal GMV, while controlling participants' sex and their total GMV of the whole brain. The participants' self‐esteem scores were mean‐centered before entering into the GLM. In addition, commonality analyses [Nimon, 2010] were used to assess the predictive contributions of SSS and self‐esteem to explain individual differences in hippocampal GMV in high and low SSS groups, respectively. In each commonality analysis, there were two predictor variables: SSS and self‐esteem. Thus there were two unique variance contributors (U SSS, U self‐esteem) and one common variance contributor (C SSS, self‐esteem). To calculate the variance contributions, three regression models were built. In the three models, SSS, self‐esteem, and the combination of SSS and self‐esteem were set as the independent variables, respectively. Consistently, the dependent variable in all three models was the residual of hippocampal GMV after regressing out the variance of sex and the GMV of the whole brain. The total variance explained in each regression model was labeled R1, R2, or R12, respectively. Thus, the unique variance contribution of SSS (U SSS) was calculated by subtracting R2 from R12, while the unique variance contribution of self‐esteem (U self‐esteem) was computed by subtracting R1 from R12. The common variance contribution of SSS and self‐esteem (C SSS, self‐esteem) was calculated as (R1+ R2 – R12). To evaluate the relative influence of SSS and self‐esteem, the proportion of each contributor in the total explained variance was calculated. To further investigate whether the self‐esteem interacted with SSS specifically to predict hippocampal GMV, we examined if the association between SSS and GMV in other regions that were smaller for low SSS participants also interacted with self‐esteem.
RESULTS
Relationship Between SSS and Hippocampal GMV
Because the SSS values in the three periods (i.e., childhood, adolescent, and youth) were highly correlated (r childhood & adolescent = 0.82; r adolescent & youth = 0.87; r childhood & youth = 0.67, all ps < 0.001), the SSS values of the three periods were averaged to simplify the analysis and comprehensively represent participants' SSS during their course of growth, with a lower score of SSS indicating a more impoverished upbringing. There SSS scores ranged from 1 to 8.67 (mean = 4.21, median = 4, SD = 1.64) (Fig. 1A).
Figure 1.
The distribution of SSS and the effect of SSS on hippocampal GMV. (A) The histogram shows the distribution of participants' SSS. High‐SSS (dark gray) and low‐SSS (light gray) were identified as those individuals who scored above or below the median, respectively. (B) The graph shows the effect of SSS on the hippocampal GMV. Participants in low‐SSS had significantly less hippocampal GMV than the high‐SSS group. The y axis indicates the residual of hippocampal GMV after regressing out the variance of gender and the total GMV of the whole brain. Asterisks indicate a significant difference between groups (**P < 0.001).
Furthermore, we validated the measurement of SSS using participants' objective SES index by their household wealth. Participants were asked whether their families possess following items (landline telephone, refrigerator, washing machine, air conditioner, kitchen, DVD player, internet, the classics, poetry, artwork, private car, bathroom, computer, mobile phone, TV) in their childhood, adolescent and youth. Participants responded either yes or no, and the yes responses were summed so that a higher score indicated higher socioeconomic circumstances in that period. There were significant correlations between participants' SSS scores and their objective SES at different periods (childhood: r = 0.655, P < 0.001; adolescent: r = 0.641, P < 0.001; youth: r = 0.635, P < 0.001), confirming the participants with lower SSS scores did come from more impoverished families.
To replicate the previous finding that the hippocampus was impaired by poverty [Hanson et al., 2011; Jednorog et al., 2012; Staff et al., 2012], we explored the relationship between SSS and hippocampal GMV. To balance the number of participants between high and low SSS groups, participants whose SSS scores were equal or below the median were categorized as the low SSS group (N = 144, males: 72; mean age = 22.89 years; mean SSS = 2.96, SD = 0.87), whereas those with the scores higher than the median were classified as the high SSS group (N = 128, males: 50; mean age = 22.38 years; mean SSS = 5.63, SD = 1.03). The hippocampus was defined using probabilistic maps from the Harvard‐Oxford Subcortical Structural Atlas available for FSL, including only voxels that had 25% or greater probability of being labeled as the hippocampus. We compared hippocampal GMV between the participants with high SSS and the participants with low SSS, with sex and GMV of the whole brain treated as covariates of confounding factors, and we found that the low SSS group had significantly less hippocampal GMV than the high SSS group [t (270) = 3.77, P < 0.001, Cohen' d = 0.46; Fig. 1B].
To examine whether the pattern was present in the hippocampus of each hemisphere, we performed the same analysis on each hippocampus respectively. A similar pattern was observed in both the right [t (270) = 3.31, P = 0.001, Cohen' d = 0.40] and left [t (270) = 3.70, P < 0.001, Cohen' d = 0.45] hippocampus. After controlling for age, as well as sex and whole‐brain GMV, the regression coefficient of hippocampal GMV and SSS remained significant (β= 0.15, P < 0.001), which was similar to the results without controlling for age.
In addition, a whole‐brain regression analysis where SSS was treated as a continuous variable also revealed a significant correlation between SSS and hippocampal GMV (Z = 3.29, P = 0.01; peak coordinates: x = 24, y = −14, z = −18), similar to the result with the analysis based on the contrast of high versus low SSS groups. Thus, our results replicate previous findings that poverty is associated with smaller GMV of the hippocampus.
To further explore whether the rest of the brain is affected by SSS, a whole‐brain t‐test was performed by comparing the GMV of each voxel between low SSS and high SSS group, with sex and the total GMV of the whole brain as confounding covariates. We found that the high SSS participants had greater GMV in bilateral hippocampus (see Fig. 2 and Table 1) and superior parietal lobule (SPL), and smaller GMV in medial prefrontal cortex and precentral gyrus than low SSS participants.
Figure 2.
The whole‐brain analysis based on the contrast between high versus low SSS group. The whole‐brain analysis revealed two clusters in the bilateral hippocampus where the high SSS group possessed a larger GMV than the low SSS group. Also shown in the figure is that the high SSS group possessed less GMV than the low SSS group in the medial prefrontal cortex. The color bar indicates Z values. [Color figure can be viewed at http://wileyonlinelibrary.com.]
Table 1.
Regions that showed significantly differences in GMV between low SSS and high SSS participants
Regions | Cluster size | t‐max | MNI coordinate | ||
---|---|---|---|---|---|
x | y | z | |||
Right hippocampus | 3352 | 4.87 | −24 | −28 | −6 |
Left hippocampus | 2552 | 4.65 | 26 | −14 | −16 |
Superior parietal lobule | 992 | 4.5 | 16 | −46 | 74 |
Medial prefrontal cortex * | 20968 | −6.00 | −12 | 56 | −10 |
Precentral gyrus * | 1608 | −4.57 | −4 | −16 | 50 |
Note: t > 3.29, cluster significance: P < 0.01; “*”: low SSS group had a larger GMV in this region.
Interaction Effect of SSS and Self‐Esteem on Hippocampal GMV
Previous behavioral studies have shown that high self‐esteem provides protection against the deleterious effect of low SES [Werner, 1995, 1997]; here we further investigated whether high self‐esteem enhances the resilience of the hippocampus to poverty. To this end, we conducted a General Liner Model (GLM) to predict participants' hippocampal GMV using SSS and self‐esteem and their interaction term as predictors, and sex and the total GMV of the whole brain as covariates. Participants' self‐esteem was measured by the Rosenberg Self‐esteem Scale [Rosenberg, 1965]. The coefficient alpha for the sample was 0.88, showing reasonably high reliability in assessment of the participants' self‐esteem. The kurtosis and skewness of all scores ranged from −1 and +1, indicating the normality of the data [Marcoulides and Hershberger, 1997]. Meanwhile, the total score for the ten items on the scale ranged from 29 to 60 (mean = 44.70, SD = 6.45), showing considerable individual differences.
Results revealed that the main effect of SSS was significant [t (266) = 3.36, P = 0.001, η p 2 = 0.04], which is consistent with the t‐test we reported above. The main effect of self‐esteem was also significant [t (266) = 2.25, P < 0.05, η p 2 = 0.02], showing that participants with higher self‐esteem had larger hippocampal GMV. Importantly, the predicted SSS × self‐esteem interaction effect was marginally significant [t (266) = −1.93, P = 0.055, η p 2 = 0.01]. To unpack the interaction effect, we calculated the partial correlations between self‐esteem and hippocampal GMV after controlling for participants' sex and the total GMV of the whole brain for the low and high SSS group, respectively. As predicted, the partial correlation between self‐esteem and hippocampal GMV was significant only for the low SSS participants (r = 0.24, P < 0.01, Fig. 3), but not for the high SSS participants (r = 0.002, P = 0.99). Meanwhile, the effect of self‐esteem on the hippocampus of the low SSS group was significant larger than that of the high SSS group (Steiger's Z = 1.98, P < 0.05, one tail), suggesting that self‐esteem especially buffers the deleterious effect of poverty on the hippocampus of individuals with low SSS.
Figure 3.
Self‐esteem was associated with hippocampal GMV only for the low SSS participants, but not for the high SSS participants.
To further examine the effects of SSS and self‐esteem had hippocampal GMV, commonality analyses were used to assess the predictive contributions of SSS and self‐esteem in explaining the variance in hippocampal GMV of participants from high and low SSS groups. The results of the commonality analyses are shown in Table 2. In the low SSS group, the variance observed in hippocampal GMV was best explained by the unique variance of self‐esteem (R 2 = 0.055, 85.9% of total variance explained by the SSS and self‐esteem together), followed by the shared variance of SSS and self‐esteem (R 2 = 0.005, 7.8%) and the unique variance of SSS (R 2 = 0.004, 6.3%). In contrast, the variance of hippocampal GMV of the participants from high SSS families was best explained by the unique variance of SSS (R 2 = 0.0016, 89.2%, Fig. 4), followed by the shared contribution of SSS and self‐esteem (R 2 = 0.00015, 8.5%) and the unique variance of self‐esteem (R 2 = 0.000042, 2.3%). That suggests that material resources from families (i.e., SSS) play a dominant role in shaping hippocampal GMV when individuals live in an advantaged environment, whereas hippocampal GMV is largely modulated by psychological resources (i.e., self‐esteem) if individuals are in an improvised environment.
Table 2.
Results of commonality analyses
Variance contributor | Variance explained (R 2) | Proportion in the total explained Variance (%) |
---|---|---|
Low SSS group | ||
U SSS | 0.0040 | 6.3 |
U self‐esteem | 0.055 | 85.9 |
C SSS,self‐esteem | 0.0050 | 7.8 |
Total | 0.064 | 100 |
High SSS group | ||
U SSS | 0.0016 | 89.2 |
U self‐esteem | 0.000042 | 2.3 |
C SSS,self‐esteem | 0.00015 | 8.5 |
Total | 0.0018 | 100 |
Figure 4.
The contributions of SSS and self‐esteem toward explaining the variance of hippocampal GMV in low SSS and high SSS participants. The pie charts show the proportions of variance explained by SSS and self‐esteem in the total explained variance of hippocampal GMV in low SSS and high SSS group, respectively. The area indicates the effect from different variance contributors.
Finally, to investigate whether self‐esteem interacted with SSS specifically to predict hippocampal GMV, we examined whether the association between SSS and GMV in the SPL, another region associated with SSS, also interacted with self‐esteem. We only observed a significant main effect of SSS on SPL GMV [t (266) = 4.30, P < 0.001], not the main effect of self‐esteem [t (266) = −0.32, P = 0.75]. Meanwhile, the interaction effect of SSS by self‐esteem in the hippocampus was significantly different from that in the SPL (Steiger's Z = −1.98, P < 0.05), suggesting that the interaction was specific to hippocampal GMV.
DISCUSSION
The present study investigated the role of self‐esteem in the resilience of the hippocampus to the deleterious effects of poverty during development in a large cohort of young adult participants. As expected, participants with relatively low SSS had smaller hippocampal GMV than those with relatively high SSS. More importantly, self‐esteem played a buffering role, such that the effect of SSS on hippocampal GMV depended on the participant's level of self‐esteem. In the low SSS group, participants with high self‐esteem showed larger hippocampal GMV than did their counterparts with similar SSS but low self‐esteem. In contrast, self‐esteem had no effect on hippocampal GMV of participants from the high SSS group. Further, the variance of hippocampal GMV was mainly explained by self‐esteem among low SSS participants, whereas SSS played a dominant role among the high SSS participants. In addition, the finding that self‐esteem did not interact with SSS to predict GMV in other cortical regions is consistent with this stress‐related hypothesis. Therefore, self‐esteem likely provides protection for the hippocampus, specifically for those growing up in a disadvantaged environment.
The finding that participants' SSS level was positively correlated with hippocampal GMV is consistent with previous studies [Jednorog et al., 2012; Staff et al., 2012]. The deleterious effect of low SSS likely comes from chronic stress [Baum et al., 1999], which leads to excessive secretion of stress hormones such as neurotoxic glucocorticoids [Hackman et al., 2010; McEwen and Gianaros, 2010]. Because the hippocampus contains a high density of glucocorticoids receptors, it appears particularly susceptible to the deleterious effect of low SSS [Avishai‐Eliner et al., 2001; McEwen, 2012; Plotsky and Meaney, 1993]. Indeed, prior studies have revealed that the hippocampus, a critical neural substrate for regulating responses under stress, is adversely affected by chronic stress [Avishai‐Eliner et al., 2001; Fenoglio et al., 2006; Gianaros et al., 2007; Plotsky and Meaney, 1993].
Importantly, our study demonstrates for the first time that self‐esteem can improve the resilience of the hippocampus to low SSS. The underlying mechanism of this protection is unclear, but one possibility is that self‐esteem may protect the hippocampus by reducing sensitivity to stress and thus decreasing the secretion of neurotoxic stress hormones [Blum, 1998; Creswell et al., 2005; Goldenberg et al., 2001]. Indeed, high self‐esteem can lead to ‘positive illusion,’ or positive self‐evaluation, which is an exaggerated perception of control and unrealistic optimism [Taylor and Brown, 1994]. Previous neuroimaging work shows that self‐esteem may modulate neural responses to social feedbacks in brain regions such as dorsal anterior cingulate cortex, dorsal medial prefrontal cortex [Eisenberger et al., 2011], and the ventral anterior cingulate cortex [Somerville et al., 2010]. Recently, self‐esteem is also found to be related to brain network properties between the medial prefrontal cortex and the ventral striatum [Chavez and Heatherton, 2015]. Therefore, self‐esteem likely emerges from neural systems integrating information about the self with positive reward and self‐perception. Such positive perception and expectation may help lowering susceptibility to perceived stress and thus reducing physiological responses to stress [Bonanno et al., 2005; Crocker and Park, 2004; Hostinar et al., 2014; Mantzicopoulos, 1990]. As a result, the hippocampus is less likely to be exposed to excessive levels of neurotoxic glucocorticoids in individuals because of the protection of self‐esteem [Pruessner et al., 2005]. Importantly, the finding that self‐esteem didn't interact with SSS to predict GMV in other regions that were smaller for low SSS participants strengthened our stress‐related hypothesis. For future study, only with serial longitudinal assessments of self‐esteem and structural brain images along with concurrent reports of perceived stress, we can identify whether self‐esteem provides protection for hippocampus through modifying the expression of stress‐related variations in hippocampal and cortical morphology [Feder et al., 2009; Fenoglio et al., 2006].
The finding that self‐esteem promotes hippocampal resilience to poverty has important practical implications. First, our study suggests potential solutions to help individuals suffering poverty. For example, the hippocampus may maintain normal development if people of low SES can maintain positive self‐regard through exercise, setting realistic expectations, or spending time with friends [Mruk, 2006]. In addition to self‐esteem, other external protective factors, such as parenthood relationships, social support, sense of control, and positive thinking style, have been found to provide protection for individuals from low SES families [Chen and Miller, 2013; Hostinar et al., 2014]. It would be interesting to explore whether these factors also promote hippocampal resilience to poverty, and, if they do, how both internal and external factors work in concert to resist the deleterious effects poverty has on the brain.
Besides the association between SSS and the hippocampus, we also observed a significant negative correlation between SSS and the GMV of the mPFC, suggesting that lower SSS individuals had a larger GMV of the mPFC. This finding is in principle consistent with previous studies that have linked childhood SES with adult PFC volume [Cohen et al., 2006; Gianaros et al., 2007; Lawson et al., 2013; Noble et al., 2015] and PFC activity in both cognitive [Sheridan et al., 2012] and emotional tasks [Javanbakht et al., 2015]. This association may be accounted for by the role of the mPFC in emotional processing, especially emotional regulation [Etkin et al., 2011]. Indeed, chronic stress during childhood is found to mediate the relationship between childhood poverty and the activity of prefrontal cortical region [Kim et al., 2013; Sheridan et al., 2012]. Therefore, it is possible that children from low‐SES family need to employ more emotional regulation to handle with the stress from poverty, which might lead to a larger mPFC volume. In other words, individuals with lower SSS are likely to possess larger mPFC volume as we observed here.
In summary, this study demonstrates that self‐esteem protects the hippocampus against the deleterious effects of poverty, which suggests practical implications for professional intervention policies. In addition, this study provides a neurobiological framework for investigating the association between psychophysiological development and self‐esteem in adverse environments. In our study, several issues remained unaddressed and are important topics for future research. First, given the correlational nature of the results in our study, the cause‐and‐effect relationship between SES, self‐esteem and hippocampal GMV remains unclear. Therefore, our stress‐related hypothesis is proposed simply based on previous studies [Hanson et al., 2011; Jednorog et al., 2012; Noble et al., 2012; Werner, 1995, 1997]. Future longitudinal studies are needed to directly illustrate how self‐esteem modulates the association between SES and hippocampal GMV, and to uncover the critical period of psychophysiological development during which the effect of self‐esteem is most pronounced [Chen and Miller, 2013; Curtis and Cicchetti, 2003; Werner, 1995]. One possible experiment is to compare individuals' stress levels and hippocampal volumes before and after intervention aimed at improving their self‐esteem levels so that we can directly test whether self‐esteem protects the hippocampus through stress‐related pathway. Second, we focused on the hippocampus as the primary region of interest in our study. Since several regions such as medial prefrontal cortex are also modulated by SES, further studies are expected to examine the relationship between the SES, GMV of these regions and other psychological variables.
The first two authors contributed equally to this work.
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