Elsevier

NeuroImage

Volume 32, Issue 1, 1 August 2006, Pages 445-456
NeuroImage

Sex differences in mental rotation: Top–down versus bottom–up processing

https://doi.org/10.1016/j.neuroimage.2006.03.030Get rights and content

Abstract

Functional MRI during performance of a validated mental rotation task was used to assess a neurobiological basis for sex differences in visuospatial processing. Between-sex group analysis demonstrated greater activity in women than in men in dorsalmedial prefrontal and other high-order heteromodal association cortices, suggesting women performed mental rotation in an effortful, “top–down” fashion. In contrast, men activated primary sensory cortices as well as regions involved in implicit learning (basal ganglia) and mental imagery (precuneus), consistent with a more automatic, “bottom–up” strategy. Functional connectivity analysis in association with a measure of behavioral performance showed that, in men (but not women), accurate performance was associated with deactivation of parieto-insular vestibular cortex (PIVC) as part of a visual–vestibular network. Automatic evocation by men to a greater extent than women of this network during mental rotation may represent an effective, unconscious, bottom–up neural strategy which could reasonably account for men's traditional visuospatial performance advantage.

Introduction

The biological basis for possible cognitive differences between men and women remains a topic of great interest and controversy. Mental rotation is a visuospatial task which gives rise to robust sex-based differences in performance, with men performing more accurately than women on average (Voyer et al., 1995). It therefore serves as a valuable probe for investigating the neurobiological underpinnings of sex differences in cognition. Several prior studies aimed at determining the neural basis for this male advantage have shown that men and women both activate regions of prefrontal, parietal, and temporal–occipital regions during mental rotation, with no (Dietrich et al., 2001, Tagaris et al., 1996, Unterrainer et al., 2000) or variable (Fink et al., 2003, Jordan et al., 2002, Seurinck et al., 2004, Thomsen et al., 2000) between-sex differences, though greater activity in frontal brain regions has been detected in women in a majority of studies (Seurinck et al., 2004, Thomsen et al., 2000, Weiss et al., 2003). One limitation of these prior studies, likely to account in part for discrepant results, is the use of variable, study-specific mental rotation paradigms created by each set of investigators for use during fMRI scanning. None of these study-specific tasks gave rise to significant male behavioral performance advantages in scanned subjects (perhaps due to small sample sizes typical of neuroimaging studies), and none were known to do so in larger populations, calling into question the usefulness of results in explaining a neural basis for this advantage. We therefore utilized a computerized mental rotation task optimized for use during fMRI scanning, which we have previously shown to be a valid measure of mental rotation abilities and to produce the expected pattern of sex-based performance in a large sample of normal subjects (Voyer et al., 2006), to investigate the neural basis for sex differences in mental rotation performance. In addition to standard between-sex group analysis of imaging data, we incorporated performance accuracy at each level of task difficulty into correlational analyses in order to assess contributions of sex, level of behavioral performance, and interaction effects to fMRI results, in accordance with studies emphasizing the importance of this approach (Seurinck et al., 2004, Shelton and Gabrieli, 2004, Tagaris et al., 1996, Unterrainer et al., 2000). Functional connectivity analyses were performed in order to explore brain networks engaged during accurate mental rotation, and how they might differ by sex.

Section snippets

Subjects

32 healthy subjects underwent fMRI scanning as part of the present study, which was approved by the New York Presbyterian Hospital–Weill/Cornell Institutional Review Board. Acceptable data were obtained from 25 subjects: 13 women (mean age 28.6, std 7.5) and 12 men (mean age 30.1, std 5.9). All subjects were strongly right-handed according to the Edinburgh Handedness Inventory, free from medical, neurological and psychiatric disease, and taking no medications. Reasons for excluding subjects

Behavioral results

For both accuracy and RT, there was an expected main effect of degree of rotation, with greater degree of rotation associated with lower accuracy [F(4,92) = 29.10, P < 0.0001] and longer RT [F(4,92) = 240.5, P < 0.0001] in both men and women. There was a weak trend towards a main effect of sex on performance accuracy, with men performing non-significantly better than women [F(1,23) = 2.04, P = 0.17], though this trend was not apparent when omitted trials were counted as incorrect and included

Behavioral findings

Behavioral results show the expected increasing reaction time and decreasing accuracy with increasing angle of rotation originally described by Shepard and Metzler (1971), confirming that subjects were appropriately engaged in the task. Despite slightly better mental rotation performance by men (men: average 83% correct; women: average 75% correct), there were no significant sex differences in accuracy or reaction time. Thus, the sex-specific neural profiles identified using fMRI were detected

Conclusion

In sum, using a validated mental rotation task in association with fMRI, we have demonstrated distinct, sex-based patterns of neural activity during mental rotation. Between-sex group analysis revealed greater activity in females of heteromodal cortical regions involved in top–down, effortful maintenance in working memory of visuospatial transformations and calculations, including dorsal medial prefrontal cortex. In contrast, men appear to take a more bottom–up approach, demonstrating greater

Acknowledgments

We are grateful to Danny Q. Chen, Oliver Tuescher, Wolfgang Engelien, Cristina Sison and Xun Liu for their help with this project. We thank Michael Peters for sharing his re-drawn figures with us.

This research was supported by NIH RO1 MH0646 and by the General Clinical Research Center at the Weill Medical College of Cornell University, NIH/NCRR M01 RR00047.

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