Higher socioeconomic status strengthens confidence facing the COVID-19 pandemic for the males rather than females: the predictive role of left hippocampus

doi:10.21203/rs.3.rs-2003812/v1

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Higher socioeconomic status strengthens confidence facing the COVID-19 pandemic for the males rather than females: the predictive role of left hippocampus

https://doi.org/10.21203/rs.3.rs-2003812/v1

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Socioeconomic status (SES) has a large impact on the way individuals respond to environmental threats. However, less is known about how SES links to personal confidence in confronting COVID-19 and its underlying neural mechanisms. To this end, we assessed self-confidence in coping with pandemic on 606 participants during its peak in China from 21th, February, 2020 to 28th, February, 2020, who underwent magnetic resonance imaging (MRI) scanning before the outbreak from 17th, September, 2019 to 11th, January, 2020. We found that males, rather than females, showed heightened confidence levels as SES increased. Similarly, greater gray matter volumes (GMV) in the left hippocampus, which were identified as SES-related brain correlates using whole-brain voxel-based morphometry (VBM) method, predicted higher confidence level for males, whilst such association was not found among females. Moreover, an independent moderation analysis replicated the predictive role of GMV based on the pre-defined anatomical structure (i.e., left hippocampus). These findings suggested that relative to females, a less threat-biased evaluation style shaped by greater hippocampal volumes might account for the males’ adequate psychological resources for coping with the pandemic. Overall, evidence highlighted the importance to focus on specific populations like females, and people from lower SES in the era of pandemic.

COVID-19

confidence

gender difference

socioeconomic status

voxel-based morphometry

An unprecedented pandemic, which was officially designated as Corona Virus Disease 2019 (COVID-19) on 11th, February, 2020 (Anand et al., 2020), swept across China, and sooner the world. At the beginning of its outbreak, not only the increasing number of confirmed and death cases owing to the contagious and fatal virus per se but also being lack of effective vaccine undoubtedly exacerbated sense of uncertainty and threats among the human beings, such as fear of being infected, inadequate supplies, and financial losses (Pfefferbaum & North, 2020). A series of strict measures (e.g., lockdown of Wuhan and home quarantine) were subsequently taken by the Chinese government (Park et al., 2020; Pfefferbaum & North, 2020), which prevented the viruses from fast and extensive transmission effectively. For the public, the confidence reflects people’s belief in holding ability to cope with challenges, and its high level in the aspects like policies and health care system are favorable for winning the battel against the COVID-19 (Chan et al., 2020; Guglielmi et al., 2020). Moreover, personal confidence in pandemic control can significantly decrease the influence of COVID-19 stressors, such as less anxious experience (Keller et al., 2011; X. Liu et al., 2020; Pramukti et al., 2020). However, the psychological response to such large-scale ongoing life threat may vary from people in the different socioeconomic status (SES). To date, less is known about how SES impacts personal confidence facing the COVID-19 and its underlying neural correlates.

SES, which is conceptualized as a combination in terms of social factors including individuals’ (or parents’) income and educational attainment (Farah, 2017), largely determines how individuals respond to the threats. For example, facing the same disasters such as the economic uncertainty (Griskevicius et al., 2011a; Mittal & Griskevicius, 2014), human-caused disaster (Jiang et al., 2020), and natural threat (Fothergill & Peek, 2004), individuals from lower SES perceive higher levels of uncertainty, and exhibit lower sense of control compared to the peers from higher SES backgrounds. Findings like these imply that the perceived psychological resources disposing of environmental threats may be enhanced as SES increases. Likewise, SES serves as a critical environmental factor to shape the vulnerability of the COVID-19-related threat in the era. Specifically, the socioeconomic disadvantaged contexts often pose individuals in poorer housing conditions and lower accessible to the necessary resources (e.g., medical cares), which increases the possibility of transmission of COVID-19 (Rollston & Galea, 2020). In line with this connotation, researchers find the rates of COVID-19 cases and mortality are higher among those from the lower SES backgrounds in both Western and Asian countries (Hawkins et al., 2020; Yoshikawa & Kawachi, 2021). These findings indicate that the adversities the poor have been encountering may amplify their burden for coping with the pandemic and sense of threats, and thereby lower their confidence to manage it. In this vein, people with sufficient financial support report higher confidence to overcome the COVID-19 (Li et al., 2020), which suggests the crucial role of SES in the perception of COVID-19-related confidence. Nevertheless, the situation may differ in males and females. As is known, the COVID-19 crisis confers less psychological impact on males than females, with lower threat perception concerning the pandemic (Galasso et al., 2020; Perrotta et al., 2021; Song et al., 2020). It is likely that the males are found to report higher personal control over their lives (Ross & Mirowsky, 2002), and such controllability is enhanced as SES increases (Slagsvold & SØrensen, 2008). Thus, it is reasonable that the males, compared to the females, exhibit higher confidence level in coping with the pandemic (Li et al., 2020). Collectively, it is assumed that higher SES backgrounds may enhance the confidence levels for males than females.

Furthermore, the estimation of confidence in coping with the COVID-19 may rely on the ability of mental simulation, which creates the way of delivering episodic information for evaluating future threats concerning the pandemic. The medial temporal lobes, including hippocampus and parahippocampal gyrus, are preferentially identified as the hubs engaging in such future-oriented thoughts (Schacter et al., 2017; Yagi & Galea, 2019). These sectors are especially susceptible to the disadvantaged environments (i.e., lower SES), in which causes the structural atrophy in hippocampus among both humans and rodents (Aksic et al., 2013; Brito & Noble, 2014; Cavanagh et al., 2013; Yu et al., 2018). Such SES-related brain correlates will in turn influence the socio-emotional processing (Blair, 2010; Blair et al., 2011; Ursache & Noble, 2016). For instance, the reduced hippocampal volumes in children from lower SES backgrounds are related to the dysfunctional stress response, with higher attentional bias to threats (Dufford et al., 2019), and higher diurnal cortisol (Dahmen et al., 2018). In a similar vein, researchers suggest that individuals with a threat dysregulation brain style may show biased evaluation towards the stimuli in the era of pandemic, increasing the propensity to deem them as stressors (e.g., signs of illness symptoms) (Hagerty & Williams, 2020). Collectively, the brain correlates, especially volumetric reduction in hippocampus, shaped in the lower SES contexts may incur a threat-biased prediction, which may attenuate individuals’ confidence to cope with the pandemic. Besides, the hippocampal volume reduction is confirmed to link to the stress-related disorders (e.g., anxiety disorders) (Hillerer et al., 2019). However, when faced with the stress-eliciting stimuli, women show excessively stronger activation in the emotion-processing brain regions like hippocampus and insula, whilst men are detected to exhibit a higher cerebral blood flow in the regulatory regions (i.e., prefrontal cortex) (Filkowski et al., 2017; J. Wang et al., 2007), which indicates a greater difficulty for women in regulating the stress. Taken together, it is assumed that greater hippocampal volumes may promote males to show higher levels of confidence confronting with the COVID-19.

Here, we probed whether SES was associated with confidence to cope with the overwhelmed threats like COVID-19 for males and females respectively, and whether SES-related brain anatomy played a predictive role in it. To address these issues, we conducted the correlation analyses to figure out the association between SES and confidence ratings. Then, a moderation analysis was tested to verify the moderating role of gender in the relationship between SES and confidence ratings (see Fig. 1A). Moreover, together with the whole-brain level voxel-based morphometry (VBM) method (Mechelli et al., 2005), we investigated whether SES-related morphologic variations could predict the gender-specific confidence levels to cope with the pandemic (see Fig. 1B). Besides, to confirm the reliability of findings, we predefined the medial temporal gyrus including the bilateral hippocampus and parahippocampus as regions of interest (ROI) based on the hypothesis (Tzourio-Mazoyer et al., 2002). The parallel moderation analyses were subsequently conducted to test the predictive role of the ROI-predefined GMV in confidence level for males and females.

Participants

Data for current study came from the project aligning with prior researches called the Behavior-Brain Research Project for Chinese personality traits (BBP) (Chen et al., 2021; Feng et al., 2021; He et al., 2021). Inclusion criteria for all participants were: history of chronic psychiatric (i.e., depression), current or history of medical (i.e., hypertension) or infectious diseases, taking prescription during the past 3 months, alcohol drinking or smoking per day, having an operation in the past one year, and in pregnancy (Table 1). The subjects were required to provide the written informed consents and the Institutional Review Board of Southwest University approved the research protocols, which were adhered to recently updated version of the Declaration of Helsinki.

Before the outbreak, we launched a large-scale longitudinal cohort project for magnetic resonance imaging (MRI) acquisition from 17th, September, 2019 to 11th, January, 2020. To track the mental states influenced by COVID-19, a total of 901 participants from the same cohort were required to report their confidence level using a 5-point Likert scale facing COVID-19 via an online survey during its peak which lasted from 21th, February, 2020 to 28th, February, 2020. A subsample set of 606 subjects (males, 179; age, 19.36 ± 0.82 y.o.) who finished the follow-up ratings were finally included in the current study (see Table 1; more information concerning participants selection could be seen in Supplemental Material – Participants for details).

Table 1

The demographic information.
Variable	Male	Female	p value
Variable	(n = 179)	(n = 427)	p value
Demographics
% Gender	70%	30%	NA
% Nationality (Minority)	15%	10%	0.06
% Family type (One-parent family)	7%	9%	0.36
% Number of children (The only child)	55%	63%	0.1
Age (M, SD)	19.46 (0.99)	19.31(0.79)	0.07

Gender differences were checked with respect to the distributions of minority, family type and number of children with Chi-square analyses. An independent sample T test was performed to testify whether there were gender differences in age among different groups. Notes: NA, the statistical tests were not performed.

Socioeconomic status (SES)

Family income and educational attainment of their parents, were combined to create a composite measurement as SES in the present study (Farah, 2017). The family annual income data were coded as follows: 1, annual income < RMB 5,000; 2, annual income RMB 5,001-25,000; 3, annual income RMB 25,001-45,000; 4, annual income RMB 45,001-65,000; 5, annual income RMB 65,001-85,000; 6, annual income RMB 85,001-105,000; 7, annual income > RMB 105,000 (Takeuchi et al., 2019). Besides, the educational qualification of both parents were coded: 1, elementary school graduate or below; 2, junior high school graduate; 3, high school graduate; 4, graduate of a short term school completed after high school (such as a junior college); 5, university graduate; 6, master degree; 7, doctorate (Takeuchi et al., 2019). The education level was acquired via calculating the averaged values of education attained by each parent (Takeuchi et al., 2014). In line with prior researches (Gianaros et al., 2007; J. Yang et al., 2016), SES was estimated by averaging the degree of income and education for further analyses.

Confidence ratings

To estimate the COVID-19-related confidence for individuals, a self-edited confidence scale composing of 2 descriptive items was developed in a follow-up survey. The items were depicted as follows (Li et al., 2020; Pramukti et al., 2020; P.-W. Wang et al., 2020): (A) how confident are you that you can cope well with your personal life during the outbreak of COVID-19 pandemic; (B) how confident are you that the government can cope well with economics of China during the outbreak of COVID-19. The subjects endorsed their agreement on the scale utilizing the 5-point Likert scale (1, not at all; 5, extremely). Eventually, the score on each item for participants was separately calculated, and the higher scores indicated the corresponding higher level of confidence to face the environmental threat, namely COVID-19.

MRI image acquisition

The structural MRI data were acquired on a SIMENS MAGNETOM PRISMA 3T MRI system (Siemens Medical Department, Erlangen, Germany). The high-resolution anatomical MRI data were acquired using the T1-weighted magnetization prepared rapid gradient echo (MPRGE) sequence (TR = 2530 ms, FOV = 256 mm, slice per slab = 192, voxel size = 0.5 × 0.5 × 1 mm, flip angle = 7^°). As usual, we utilized the foam pads for the sake of avoiding excessive head motion during scanning.

Notably, 606 structural images were subjected to quality control to ensure high data quality. More specifically, brain imaging data were displayed in sequence to check data quality and no findings of distortions, ghosting, or gross anatomical abnormalities (Yan et al., 2016). Meanwhile, normalization for each participant’s image was also visually checked (Yan et al., 2016).

Pre-processing of structural data

The current study adopted the Statistical Parametric Mapping software (SPM 12; Wellcome Department of Cognitive Neurology, London, United Kingdom) to preprocess the MRI data (http://www.fil.ion.ucl.ac.uk/spm/software/spm12/), which was implemented in Matlab (Mathworks Inc., Natick, MA, United States). We first manually reoriented the T1 images by setting the anterior commissure as origin. Subsequently, the adjusted image of each participant was segmented into different tissues including gray matter (GM), white matter (WM), and cerebral spinal fluid (CSF), to acquire the maps with the voxel-wise probability of gray matter (Ashburner & Friston, 2005). These images were then normalized to the MNI space using the Diffeomorphic Anatomical Registration Through Exponentiated Lie Algebra (DARTEL). The normalized images were modulated using the Jacobean determinants, and smoothed through convolving them with a Gaussian kernel of 8 mm full width at half maximum (FWHM) to improve the signal-to-noise ratio.

Statistical analyses

Whole brain analysis. We explored the association between SES and the localized GMV adopting whole-brain VBM method in the SPM 12 toolkit. To this end, SES was entered as a variable of interest, whilst age, gender and global GMV were included as covariates of no interest in the model to rule out the potential effects on brain morphology (Good et al., 2001; Kulynych et al., 1994; Peelle et al., 2012). The global GMV were obtained through the Matlab script ‘get_totals’ (http://www.cs.ucl.ac.uk/staff/g.ridgway/vbm/get_totals.m). The absolute mask (threshold= 0.2) was used to restrict the search volume of grey matter. Afterwards, the T contrast was thresholded by the Gaussian Random Field theory (GRF, voxel p < 0.001; cluster p < 0.05). As was mentioned before, lower SES backgrounds were demonstrated to be associated with hippocampal reductions, and consequently the shaped brain morphology might impact on the response to stressors (Farah, 2017; Frodl & O’Keane, 2013). If the whole brain analyses searched any volumes in the hippocampus that were significantly correlated with SES, the regions might be saved as ROI for extracting their GMV, which was used for subsequent moderation analyses.

ROI-level analysis. To further testify the role of medial temporal lobes in SES, we defined the bilateral hippocampus and parahippocampus as ROI using parcellations from the Automated Anatomical Labelling Atlas (AAL) (Tzourio-Mazoyer et al., 2002). Specifically, we performed the replication analyses to calculate the associations between SES and GMV extracted from the pre-defined ROI (Bonferroni corrected p < 0.05).

Moderation analysis. We firstly conducted a moderation analysis to explore whether gender moderated the relationship between SES and confidence to cope with COVID-19. Moreover, to testify whether the SES-related brain morphology could predict gender-specific COVID-19-related confidence, the moderation analyses were also conducted in parallel. Based on the hypothesis, the SES-related brain correlates were defined as the GMV in the medial temporal lobes (i.e., hippocampus and parahippocampus) derived from the whole-brain VBM and ROI-level analyses, which were extracted via the script of ‘get_totals’ for the moderation analyses, respectively.

Relationship between SES/ Gender and COVID-19-related confidence

To reveal the relationship between SES and confidence facing the COVID-19, we performed a bivariate Spearman’s rank correlation analysis and found higher SES was related to higher confidence to cope with personal life during the COVID-19 [r = 0.099, p = 0.015; 95% CIs (confidence interval), 0.018 - 0.174], whilst no significant relationship was found between SES and confidence in economics (r = 0.055, p = 0.177; 95% CI, -0.022 – 0.138; see Supplemental Material – Correlation analyses for details).

To test whether there were gender differences in COVID-19-related confidence ratings, the independent sample T tests found that compared to males, females showed less confidence to cope with personal life during the COVID-19 [t₍₆₀₄₎ = 2.950, p = 0.003; males = 2.990 ± 1.185, females = 2.690 ± 1.112], but not on economics [t₍₆₀₄₎ = 0.710, p = 0.480; males = 1.930 ± 0.848, females = 1.880 ± 0.690]. These results suggest that people, who are from higher SES and men, may hold higher confidence for managing their personal life during this pandemic.

The modulatory effect of gender on SES and COVID-19-related confidence

We conducted the hierarchical regression analyses to investigate whether SES related to the confidence to cope with personal life during the COVID-19 as a function of gender. It was found that the model predicting the confidence level was significant [adjusted R²= 0.008; F_{(1, 602)} = 6.826, p = 0.028]. The results revealed significant main effects of SES (β = 0.243, t₍₆₀₂₎ = 3.257, p = 0.001), but not for gender (β = 0.098, t₍₆₀₂₎ = 0.891, p = 0.373) in predicting confidence. As predicted, the results showed a significant two-way interaction effect between the relationship of SES and gender (β = -0.287, t₍₆₀₂₎ = -2.200, p = 0.028). To clarify such effect more clearly, the simple slope tests were conducted (Aiken et al., 1991), and revealed that SES significantly predicted confidence to cope with personal life during the COVID-19 for males [β = 0.243, t₍₆₀₂₎ = 3.257, p = 0.001], but such effect was not found for females [β = 0.048, t₍₆₀₂₎ = 1.014, p = 0.311; see Table 2, Figure 4A]. Overall, these findings indicate that men, but not women, with high SES tend to hold high level of confidence on managing their personal life despite the impacts of COVID-19 pandemic.

Table 2. The moderation effect of gender.

Variables	R²-change	β	p
Confidence to cope with personal life during the COVID-19	R²-change	β	p
Step 1
SES	0.025***	0.105	0.010
Gender	0.025***	-0.127	0.002
Step 2
SES	0.008*	0.243	0.001
Gender		0.098	0.373
SES*Gender		-0.287	0.028

Notes: *, p < 0.05; ***, p < 0.001.

The brain anatomy underlying SES

To identify the specific brain regions related to SES, the whole brain analyses were conducted to regress SES scores on GMV in each voxel of the brain. The VBM results showed that higher SES was related to less GMV in the left middle prefrontal cortex (MPFC; MNI coordinates: 0, 50, 30; voxels = 1598), and left precuneus (MNI coordinates: -29, -29, 62; voxels = 551). Besides, higher SES was correlated with greater GMV in the left cerebellum (MNI coordinates: -23, -57, -48; voxels = 12046), right medial temporal gyrus extending to the hippocampus (MTG; MNI coordinates: 51, 2, -27; voxels = 1738), and left hippocampus extending to parahippocampus (MNI coordinates: -30, -26, -12; voxels = 894; see Figure 2; see Supplementary material – The anatomical correlates of SES for details).

Besides, to verify robustness of the findings, we also explored the relationships between SES and GMV in anatomically defined ROI. The correlation analyses showed that higher SES were related to greater GMV in the left hippocampus [r = 0.169, Bonferroni corrected p < 0.05; 95% CIs, 0.091 – 0.248], left parahippocampus [r = 0.134, Bonferroni corrected p < 0.05; 95% CIs, 0.060 – 0.208], right hippocampus [r = 0.172, Bonferroni corrected p < 0.05; 95% CIs, 0.091 – 0.252] and right parahippocampus [r = 0.148, Bonferroni corrected p < 0.05; 95% CIs, 0.067 – 0.224; see Figure 3], with regressing out the covariates of no interest including age, gender and GMV. Taken together, these findings further indicate that the medial temporal lobes may be the crucial anatomical basis of SES.

The modulatory effect of gender on SES-related brain morphology and confidence

Based on the hypothesis, we performed the moderation analyses to testify the moderation effect between SES-related morphologic difference, namely the medial temporal lobes, and gender on confidence to cope with personal life during the COVID-19 (Aiken et al., 1991). The model in predicting confidence level was significant [adjusted R²= 0.009; F_{(1, 602)} = 5.148, p < 0.05]. More precisely, it was found the significant main effects of GMV in the left hippocampus [β = 0.214, t₍₆₀₂₎ = 2.545, p = 0.011], and gender [β = 0.981, t₍₆₀₂₎ = 2.155, p = 0.032]. Notably, gender significantly moderated the relationship between the GMV in the left hippocampus and the confidence [β = -1.019, t₍₆₀₂₎ = -2.384, Bonferroni corrected p < 0.05]. To depict the interaction effect in a clearer way, we conducted a simple slope test (Aiken, West andReno, 1991), and it revealed that the GMV in the left hippocampus predicted confidence concerning the effect of COVID-19 on personal life for males [β = 0.214, t₍₆₀₂₎ = 2.545, p = 0.011], but not for females [β = -0.024, t₍₆₀₂₎ = -0.443, p = 0.658; see Table 3, Figure 4B]. Moreover, the parallel analyses were conducted in the region revealed by the VBM analyses including the right MTG to verify the specificity of such effect (see Supplemental Material – The moderating analyses for details). The findings suggest that only GMV in the left hippocampus significantly predicts the gender-specific confidence level.

Furthermore, to verify the reliable role of medial temporal lobes in predicting COVID-19-related confidence, we performed a replication analysis to investigate the relationship between predefined ROI-level GMV in left hippocampus, gender and confidence (Aiken et al., 1991). We found the model could significantly predict the confidence level [adjusted R²= 0.008; F_{(1, 602)} = 5.246, p < 0.05]. In detail, there were significant main effects of the GMV in left hippocampus [β = 0.237, t₍₆₀₂₎ = 2.639, p = 0.009], and gender [β = 1.235, t₍₆₀₂₎ = 2.089, p = 0.037]. More importantly, in line with the prior findings, gender moderated the association between GMV in left hippocampus and confidence level [β = -1.241, t₍₆₀₂₎ = -2.239, uncorrected p = 0.025]. The simple slope tests indicated that greater GMV in the left hippocampus enhanced the males’ confidence level [β = 0.237, t₍₆₀₂₎ = 2.639, p = 0.009], whilst such relationship was not found for females [β = 0.000, t₍₆₀₂₎ = 0.007, p = 0.994; see Table 3, Figure 4B]. In addition, the parallel analyses showed that such relationship was specific for the left hippocampus (see Supplemental Material – The moderating analyses for details). Taken together, the results replicate what we have reported before, and indicate that greater GMV in the left hippocampus predicts the confidence level confronted with the COVID-19 for males rather than females.

Table 3. The moderating effect analyses.

Variables	R²-change	β	Uncorrected p
Confidence to cope with personal life during the COVID-19	R²-change	β	Uncorrected p
Whole-Brain level
Step 1
Whole-brain level GMV	0.016**	0.045	0.322
Gender	0.016**	-0.099	0.029
Step 2
Whole-brain level GMV	0.009*	0.214	0.011
Gender		0.981	0.032
Whole-brain level GMV*Gender		-1.019	0.017
ROI-level
Step 1
ROI-level GMV	0.017**	0.066	0.165
Gender	0.017**	-0.084	0.076
Step 2
ROI-level GMV	0.008*	0.237	0.009
Gender		1.235	0.037
ROI-level GMV*Gender		-1.241	0.025

Results showed that gender significantly moderated the relationship between GMV in the left hippocampus, which were derived from whole-brain level and ROI-level analyses respectively, and confidence to cope with personal life during the COVID-19. Notes: *, p < 0.05; **, p < 0.01.

The findings in present study revealed that males, rather than females, showed heightened confidence levels as SES increased. Furthermore, the GMV in the left hippocampus, which were identified no matter from the whole-brain and ROI-predefined level, predicted more adequate COVID-19-related confidence for males, whilst females did not show such association. The current work revealed that compared to females, the SES-related brain correlates (i.e., hippocampal volumes) served as a protective role for males to show greater confidence level confronting the COVID-19 crisis. Collectively, these findings shed lights on the deficient psychological resources for women to cope with the pandemic.

The moderating analysis showed that higher SES could enhance higher level of confidence for males rather than females. Generally speaking, individuals with greater socioeconomic advantage were less impacted by the threats, perceiving lower sense of uncertainty (Fothergill & Peek, 2004; Jiang et al., 2020; Mittal & Griskevicius, 2014). Likewise, higher SES also served as a protective role in coping with the COVID-19 pandemic. For example, the advantaged contexts provided the accessibility to necessary resources, such as masks and healthy foods (Rollston & Galea, 2020), which might increase people’s confidence to confront this pandemic. Moreover, the stress-related disorders often highlighted the importance of gender disparities (Oyola & Handa, 2017; Verma et al., 2011; J. Wang et al., 2007). More specifically, researchers posited that stress would exert stronger proximal effects on women, including an increased risk or even prevalence of developing mental conditions (i.e., anxiety) (Hodes & Epperson, 2019). The higher susceptibility to threats among women might be owing to the over-reaction to the stressors. For instance, the gender-specific stress response in HPA axis was uncovered in animal studies (Verma et al., 2011), with uniformly higher cortisol level at the basal level among females relative to males (Roelfsema et al., 1993). In a similar vein, the long-term consequences of COVID-19-related threats disproportionately impacted women than men (Zamarro et al., 2020, p. 19). Evidence showed that relative to men, women were more sensitive to the stressors that related to the pandemic, internalizing higher rates of mental conditions like anxiety during this specific period (N. Liu et al., 2020). In line with these findings, some evolutionary theories provided insights into why the increased sensitivity of threatening stimuli among females had been kept across human history (Glover & Hill, 2012; Oldehinkel & Bouma, 2011). Traditionally, women mostly engaged in taking care of offspring rather than being the providers of material resources (i.e., food) like men. It was thereby adaptive for them to be highly sensitive to, or vigilant about not only the environmental dangers, but also children’s signals of need (i.e., crying), which in turn brought overreaction to stress (Glover & Hill, 2012; McLean & Anderson, 2009; Oldehinkel & Bouma, 2011). As researchers suggested, human beings during the period of pandemic were exposed to the stressors, such as fear of illness of ourselves and our loved ones, physical distancing, and inadequate medical supplies (Goldfarb, 2020; Pfefferbaum & North, 2020). This indicated that irrespective of socioeconomic status a family dwelled, the inherent and instinctive response pattern in the history determined females’ overreaction to the COVID-19-related stressors, and might incur greater worry about how to care the family for safety. The females were consequently susceptible to the potent stressor COVID-19 regardless of the socioeconomic contexts, showing lower COVID-19-related confidence. Taken together, the results showed that only socioeconomically advantaged men showed higher confidence level confronting the COVID-19 pandemic.

Moreover, the results showed that the increased GMV in the left hippocampus predicted higher COVID-19-related confidence for males, whilst such association was not significant for females. As was known, the hippocampi damage would in turn fail to regulate the feedback inhibition of HPA axis, thereby leading to excessive cortisol secretion (Sapolsky et al., 1986). For instance, evidence demonstrated a robust negative correlation between GMV in hippocampus and cortisol secretion during the day (Frodl & O’Keane, 2013). The hippocampus was highly connected with a spectrum of brain regions including the frontal (i.e., the MFG) and parietal cortices (Aminoff et al., 2013; Suzuki, 2009). This segment served critical functions in the associative threat learning, facilitating generalization to novel threatening stimuli (Corchs & Schiller, 2019). Coupled with the evidence, it suggested that those with the structural reductions in hippocampus might be accompanied by the dysregulation response to the life threats COVID-19, with higher possibility to associate neutral stimuli (i.e., crowed places) as threatening cues (i.e., the infected zones) after the outbreak of the pandemic. Moreover, hippocampus was also identified as a hub region in episodic prospection (Allen & Fortin, 2013; Aminoff et al., 2013), and evidence showed that greater hippocampal volumes was associated with better ability to simulate the future events (Yang et al., 2020). Together, it could be proposed that the structural atrophy in hippocampus would engender more negative mental simulation of threats via the biased contextual associative processing (McEwen & Gianaros, 2011), which might account for why individuals with less GMV in the hippocampus showed less confidence facing with this pandemic irrespective of gender.

Moreover, the individual difference in personal confidence level varied from gender when the hippocampal volumes were increased. Just as mentioned before, females tended to activate stress response, and be alert to the threats because of their traditional role in taking care of offspring, whereas males were prone to inhibit the processing of fear for exploring the new environment (Glover & Hill, 2012). Importantly, the researchers held that the limbic system, especially hippocampus and parahippocampus, were identified as guiding behaviors for self-preservation and preservation of species (MacLean, 1985; Ploog, 2003). These viewpoints from evolutionary perspectives might intriguingly suggest that gender disparities were in a way rooted in the bottom-up emotional systems shaped by adaptation in the evolutionary process that predisposed females and males to react to environmental threats in different way. Likewise, the meta-analysis pointed out that relative to males, females exhibited greater activation in the subcortical regions including hippocampus for processing the negative stimuli (Stevens & Hamann, 2012). Based on these accounts, it implied that COVID-19 would activate more inherent fear for women concerning the safety after the outbreak of pandemic, which resulted in their lower levels of confidence despite high GMV in the hippocampus. Such morphological features of the brain, however, provided a favorable premise for males to act on the same threats, leading to higher confidence level confronted with the COVID-19. Taken together, the SES-related brain correlates worked together with gender to predict the inter-differences in humans’ confidence towards the environmental threats.

Current study had limitations. Firstly, the findings reveled by current study would be cautious to be generalized to other cultures. For ascertaining the robustness of results, a large-scale epidemiological investigation in a cross-cultural sample would be much more desirable. Besides, the stress response disparities in SES and gender could shape the development of neurocognitive functioning for human beings (Ursache & Noble, 2016; Verma et al., 2011). We thus attached great significance to building the neurobiological basis underlying how SES linked to COVID-19-related confidence, which provided novel insights into such relationship. The biological factor, including the cortisol level before the COVID-19 virus, was thus suggested to be added in the model.

The current work, for the first time, provided the evidence that the psychological resources at disposal of environmental threats (i.e., COVID-19) depended on joint interaction effect of SES and gender. Moreover, greater hippocampal volumes predicted higher confidence level for males but not for females. The results suggested that greater GMV in the left hippocampus might protect the males rather than females from the impact of the threat-biased appraisal, and thereby they tended to show higher confidence level. Overall, our work highlights the necessity of providing psychological aid for specific populations, particularly the females and people from lower SES. Urgent action is needed to mitigate the devastating impacts of this pandemic on them, including ensuring the employment, providing social support and so on.

Acknowledgements

We express our sincere appreciation to those who contribute to data collection of this project, especially Junye Xu, Yaqi Zhang, Junyu Wang, Xu Wang.

Funding

This work was supported by the National Natural Science Foundation of China [31971026] and the Fundamental Research Funds for the Central Universities [SWU2009104].

Data availability statement

The data that support the findings of this study are available from the corresponding author upon reasonable request.

Author Contributions

Rong Zhang: Formal analysis, Methodology, Visualization, Writing original draft;

Zhiyi Chen: Investigation, Methodology, Resources, Editing original draft;

Weihua Zhao: Methodology, Editing original draft;

Pan Feng: Investigation, Resources, Editing original draft;

Feng Zhou: Methodology, Editing original draft;

Tingyong Feng: Conceptualization, Data curation, Funding acquisition, Supervision, Writing& Editing original draft.

Conflicts of interest

None.

Ethical approval

The authors confirm that all procedures contributing to this work comply with the ethical standards of the relevant national and institutional committees on human experimentation and with the Helsinki Declaration of 1975, as revised in 2008.

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No competing interests reported.

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Higher socioeconomic status strengthens confidence facing the COVID-19 pandemic for the males rather than females: the predictive role of left hippocampus

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Socioeconomic status (SES)

Confidence ratings

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