Sex Differences in Brain Structure Account for the Sexual Distinction on Balanced Time Perspective


 Sex differences in behaviour and cognition have been widely observed, however, little is known about such differences in maintaining a balanced time perspective or their potential underlying neural substrates. To answer the above questions, two studies were conducted. In Study 1, time perspective was assessed in 1,913 college students, including 771 males and 1,092 females, and demonstrated that females had a significantly more balanced time perspective than males. In Study 2, 58 males and 47 females underwent assessment of time perspective and structural brain imaging. Voxel-based morphometry analysis and cortical thickness analysis were used to analyse the structural imaging data. Results showed that compared with males, females demonstrated a more balanced time perspective, which primarily related to lower grey matter volume in left precuneus, right cerebellum, right putamen and left supplementary motor area. Analysis of cortical thickness failed to reveal any significant sex differences. Furthermore, the sex difference in grey matter volume of left precuneus, right cerebellum, right putamen and left supplementary motor area could account for the difference in balanced time perspective between males and females. The findings deepen our understanding of sex differences in human cognition and their potential neural signature, and may inform tailored interventions to support a balanced time perspective in daily life.


Introduction
Mounting evidence points to the importance of studying human subjective temporality and its implications for adaptive and maladaptive thoughts and behaviours in everyday life (for a review, see Stolarski, Zajenkowski, Jankowski, & Szymaniak, 2020). Time perspective (TP) refers to the "nonconscious process whereby the continual ows of personal and social experiences are assigned to temporal categories, or time frames, that help to give order, coherence, and meaning to those events" (p.1271) (Zimbardo & Boyd, 1999). According to this original de nition, TP is posited to included ve dimensions: Future, Past-Negative, Past-Positive, Present-Fatalistic and Present-Hedonistic.
A balanced time perspective is de ned as "the mental ability to switch exibly among TPs depending on task features, situational considerations, and personal resources rather than be biased toward a speci c TP that is not adaptive across situations" (Boniwell & Zimbardo, 2004). Proposed as a central ingredient of positive psychology (Boniwell & Zimbardo, 2004), the bene cial effects of a balanced time perspective have been observed across a many aspects of subjective well-being (T. Chen Proverbio, 2021) and personality traits (Costa, Terracciano, & McCrae, 2001). In general, males are generally overshadowed by females on tests of nonverbal reasoning and emotion identi cation, however the converse pro le is typically observed on tests of motor and spatial cognition (Satterthwaite et al., 2014). At present, sex was generally controlled as a covariate in studies exploring balanced time perspective (Stolarski et al., 2020), which makes the sex difference on balanced time perspective unclear.
Little is known about sex differences in balanced time perspective and the available evidence to date is mixed. Two studies have reported that females are more balanced in time perspective than males with a level, however effects have ranged from signi cant to marginal (T. Chen, Liu, Cui, Chen, & Wang, 2016; Guo, Chen, & Feng, 2017). In contrast, a separate study showed females were signi cantly less balanced in time perspective than males (N =140, p = 0.032) (Wu, Zhou, Zhao, Qiu, & Guo, 2019). Given these con icting ndings, it is important to explore this question using a large sample. In this context, it is important to understand whether the sex difference in balanced time perspective re ects underlying sex differences at the neural level. Mounting evidence converges to suggest considerable sex differences in brain anatomy and function (Gur & Gur, 2017). Compared with females, males are reported to have larger grey matter volume in subcortical temporal structures (including hippocampus) and motor areas (Lotze et al., 2019). In contrast, males have been shown to display thinner cortical thickness and less gyri cation in frontal, parietal regions (Luders et al., 2004;Lv et al., 2010) as well as weaker structural connectivity in the inter-hemispheric connections (Tunç et al., 2016). As such, while there appears to be signi cant sex differences in terms of underlying brain structure, it remains unclear how such differences relate to the sex difference observed in studies of balanced time perspective.
To address these questions, we designed two studies. Study 1 aimed to con rm that females showed more a balanced time perspective than males with a large sample. As an extension to Study 1, Study 2 explored how potential sex differences in brain anatomy, indexed by grey matter volume and cortex thickness, might account for a more balanced time perspective in females relative to males.

Study 1
Study 1 was designed to test the hypothesis that females manifested a more balanced time perspective than males within a large sample.

Method Participants
A total of 1913 college students were recruited from Beijing by advertisement to complete a questionnaire measuring time perspective. The sample included 796 males (mean age = 20.07 years, SD = 1.16) and 1117 females (mean age= 19.75 years, SD= 1.11), in which age information of 24 males and 25 females was missing. Participants were required to complete the questionnaire after a brief introduction to the study. Written informed consent was provided by participants before the commencement of the study. This study was approved by the ethics committee of the Institute of Psychology, Chinese Academy of Sciences.

Measures
The  MA, USA). T1-weighted structural images were initially reoriented to the same spatial orientation and the point of the anterior commissure, and followed by pre-processing with standard settings of the CAT12 toolbox: skull-stripping, bias corrections for magnetic eld inhomogeneity, precise segmentation into grey matter, white matter, and cerebrospinal uid, followed by spatial normalization to the DARTEL template in the Montreal Neurological Institute (MNI) space (voxel size: 1.5mm × 1.5mm × 1.5mm). Finally, spatial smoothing was performed with an 8-mm full-width at half maximum isotropic Gaussian kernel. The VBM data was applied with a 0.2 absolute masking threshold. Automated measures of quality control implemented in the CAT12 toolbox and careful visual inspection of the data were applied to ensure data quality.
Surface-based morphometry (SBM) analysis Cortical thickness analysis was performed with SPM12 and the CAT12 running in MatLab R2013b (The MathWorks, Inc., Natick, MA, USA). Cortical thickness was estimated using a projection-based methodology, implemented in the CAT12 toolbox, by calculating the distance between the inner and outer cortical surface (Dahnke, Yotter, & Gaser, 2013). Projection-based thickness can deal well with partial volume information, sulcal blurring, and sulcal asymmetries. Topological correction, spherical mapping, and spherical registration were conducted to derive a cortical thickness index. The merged surface of both hemispheres were then resampled and spatially smoothed with 15-mm full-width at half maximum isotropic Gaussian kernel. To ensure the SBM data quality, automated measures of quality control implemented in the CAT12 toolbox and careful visual inspection of the data were applied.

Data analysis
Independent t tests were performed with CAT12/SPM12 to examine potential sex differences in grey matter volume and cortical thickness controlling for age. Total intracranial volume (TIV) was additionally controlled for in the VBM analysis. Voxel-level thresholds (p < 0.001 without correction) and cluster-level thresholds (p < 0.05 with FWE cluster correction for multiple comparisons) were further applied to guard against false positive results. To examine whether sex differences in brain anatomy underlie sex difference in balanced time perspective, we derived the mean values of each signi cant cluster for brain regions showing a signi cant sex difference. Those mean grey matter volumes, and cortical thickness values in each signi cant cluster were separately controlled as covariates in a series of ANCOVAs comparing the sex difference in DBTP.

Results
There was no sex difference in terms of age (p = 0.587). On structural neuroimaging, males were found to have signi cantly higher TIV relative to females (p < 0.001) (see Table 1). VBM analysis showed that, compared with females, males had signi cantly larger grey matter volume in the right cerebellum (Crus I), left precuneus, left supplementary motor area and right putamen (p < 0.05, FWE cluster-level correction) (see Table 2 and Fig. 2). SBM analysis revealed no sex difference in cortical thickness (p < 0.05, FWE cluster-level correction).

DBTP was normally distributed in males (
A series of ANCOVA demonstrated that the signi cant sex difference in DBTP disappeared when any of the grey matter volumes of the above regions (i.e., left precuneus, right cerebellum (Crus I), right putamen, left supplementary motor) were included as a covariate in the analyses (see Table 3).

General Discussion
This study sought to explore sex differences in the maintenance of a balanced time perspective and to identify potential neuroanatomical correlates of such differences using structural brain imaging. Across two independent studies, we found evidence of a more balanced time perspective in females compared to males, which related to smaller grey matter volumes in the left precuneus, right cerebellum Crus I, right putamen and left supplementary motor area. Furthermore, controlling for any of the above grey matter volumes was found to ameliorate the signi cant sex difference in balanced time perspective. Our ndings suggest that distinct structural neuroanatomical regions may underlie sex-based differences in the maintenance of a balanced time perspective.
Despite mounting interest in the adaptive utility of maintaining a balanced time perspective, little is known regarding potential sex differences. Notably, our ndings of a more balanced time perspective in females relative to their male counterparts are in line with a previous study in an independent sample (T. Chen et al., 2016). The cognitive processes that support this sex-based difference, however, remain unclear. Maintenance of a balanced time perspective is posited to rely on cognitive control processes (e.g., working memory, inhibition), which enable the exible switching between different temporal orientations ( (Gur et al., 2012). We tentatively suggest that sex differences in cognitive control may drive the differences in maintaining a balanced time perspective, although future studies directly testing this proposal will be required.
The second major aim of our study was to elucidate potential neuroanatomical sex-based differences that could potentially account for the optimal time perspective exhibited by females as compared to males. Our VBM analysis revealed that males had larger TIV, and higher grey matter volumes in left precuneus, right cerebellum (Crus I), right putamen and left supplementary motor area than females when controlling for TIV. In contrast, we did not nd sex difference in cortical thickness.
We found that the sex difference in grey matter , the precuneus supports a number of complex cognitive functions that are essential for self-referential processing and episodic past and future thinking (Cavanna & Trimble, 2006). The precise role of the precuneus in modulating a balanced time perspective remains unclear. As such, it will be important to delineate how DMN integrity supports the capacity for exible switching between different time perspectives, and how sex differences impact these switching processes.
Our results further implicated regions traditionally viewed as motor-related regions, including the cerebellum and supplementary motor area, in the origin of sex difference in balance time perspective. At rst glance, regions typically associated with motor function might not be expected to support a cognitively demanding process such as a balanced time perspective. However, accumulating evidence from neuroimaging and clinical studies indicates that these regions serve a number of cognitive control functions, such as inhibition (Nachev, (Segarra et al., 2008). Apart from executive control, the cerebellum is increasingly understood to serve an emotion regulation function (Schutter & Van Honk, 2005). As such, cerebellar involvement may re ect emotion regulation processes which are positively associated with balanced time perspective (Stolarski et al., 2011).
Finally, we found evidence for sex differences in subcortical structures in the origin of sex differences in balanced time perspective. Of note, the putamen emerged as the only subcortical region implicated in sex differences in this study. As a key region of the basal ganglia, the putamen is reliably implicated in the brain's reward pathways (Haber & Knutson, 2010) as well as motor and cognitive function. Neuroimaging and lesion studies converge to suggest that the putamen contributes to higher cognitive functions implicated in a balanced time perspective including working memory (Voytek & Knight, 2010), inhibition (Rubia et al., 2006) Taking our ndings together, our results can be interpreted in favour of sex differences in a corticosubcortical-cerebellar network that contributes to sex differences in the maintenance of a balanced time perspective (Bostan & Strick, 2018;Habas et al., 2009). Our ndings of an inverse relationship between brain structure and performance warrant further exploration. We tentatively propose that these associations may re ect synaptic or neuronal pruning processes during brain maturation (Kanai & Rees, 2011). Brain grey matter development has been shown to follow an inverted U-shape with peak total brain volume and grey matter volume in females emerging on average 2 years earlier than males, and decreasing along a steeper slope than males until early adulthood (Lenroot et al., 2007), suggesting earlier neuronal pruning in females. Whether sex-based differences in cortical pruning (e.g., cortical thickness) account for greater e ciencies in balanced time perspective remain unknown, and future studies adopting a longitudinal approach may offer some clarity on this matter.

Conclusions
In summary, our ndings offer preliminary evidence to suggest sex differences in the maintenance of a balanced time perspective can be linked to underlying differences in brain structure. Future research is now required to build on these ndings to determine the functional implications of differences in time perspective in terms of subjective wellbeing in males versus females (T. Chen et al., 2020; Zhang et al., 2013). Moreover, given the correlational nature of our study, longitudinal approaches incorporating multiple time points across the lifespan are warranted to determine the precise origin of sex differences in the neural correlates of time perspective. These approaches may lend themselves to novel interventions to improve time perspective in males, which in turn may impact positively on other aspects of subjective wellbeing including mental health.

Declarations
Author contributions included conception and study design (TC, MI and YW), data collection or acquisition (ZL, JH, YW and RCK), statistical analysis (TC, JH, MI), interpretation of results (TC, MI and YW), drafting the manuscript work or revising it critically for important intellectual content (TC, JFC, MI,YW and RCK) and approval of nal version to be published and agreement to be accountable for the integrity and accuracy of all aspects of the work (All authors). Data availability The datasets are available from the corresponding author upon request.
Code availability Not applicable.
Ethical approval This study was approved by the ethics committee of the Institute of Psychology, Chinese Academy of Sciences.
Informed consent Informed consent was collected from all participants, who were paid for their participation.
Consent for publication Participants approved the data to be published.
Con ict of interest All the authors declared that they have no con ict of interest.