666 Clinical neuroscience
Sex differences in the association between gray matter
volume and verbal creativity
Baoguo Shia, Li Xua, Qunlin Chenb,c and Jiang Qiub,c
The explanation for why significant sex differences are
found in creativity has become an increasingly important
topic. The current study applied a cognitive neuroscience
perspective and voxel-based morphometry to investigate
the sex differences for the association between verbal
creativity and gray matter volume (GMV) in a large sample
of healthy adults from the Chinese Mainland (163 men and
193 women). Furthermore, we sought to determine which
brain regions are responsible for these differences. Our
behavioral results showed a significant sex difference.
Specifically, women scored higher than men on originality.
The voxel-based morphometry results indicated that the
relationship between originality and GMV differed between
men and women in the left temporo-occipital junction.
Higher originality scores in women were associated with
more GMV. In contrast, higher originality scores in men were
related to less GMV. These findings suggest the left
temporo-occipital junction GMV plays a unique role in the
Introduction
Creativity is generally accepted as a core element of
social interaction, and it is of great importance to the
progression and innovation of society. According to
Guilford [1], divergent thinking (DT) is the basis of
creativity. It refers to the ability to produce many answers
to one question. As a result, tests of DT have long been
the most commonly used tools in research to assess an
individual’s creativity [2]. Of these tools, the Torrance
Test of Creative Thinking (TTCT) is one of the most
well-established measures of creativity [3]. Typically,
responses to DT tests are assessed according to their
originality (i.e. the statistical frequency of the answer),
fluency (i.e. number of answers), and flexibility (i.e.
number of response categories). Among these, originality
is vital for creativity [4] and it reflects creativity more
strongly than fluency in the real world [5]. On the basis of
this knowledge, we used originality as measured by the
verbal TTCT as the creativity index in the current study.
Sex differences in cognitive abilities are a relatively
popular topic that has been studied across various
domains including creativity. Most previous behavioral
studies have focused on determining whether females
differ from males in terms of creative personality [6], the
creative process [7], and creative potential [8].
Furthermore, they have sought to identify the factors that
contribute toward sex differences as well as when and
how long these differences play a role in the relationship
0959-4965 Copyright © 2017 Wolters Kluwer Health, Inc. All rights reserved.
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sex differences in verbal creativity because women usually
surpass men in semantic processing, which is the major
function of the left temporal region. NeuroReport
28:666–670 Copyright © 2017 Wolters Kluwer Health, Inc.
All rights reserved.
NeuroReport 2017, 28:666–670
Keywords: gray matter volume, originality, sex differences, verbal creativity,
voxel-based morphometry
a
Beijing Key Laboratory of Learning and Cognition, Department of Psychology,
Capital Normal University, Beijing, bKey Laboratory of Cognition and Personality
(SWU), Ministry of Education and cSchool of Psychology, Southwest University,
Chongqing, China
Correspondence to Baoguo Shi, PhD, Beijing Key Laboratory of Learning and
Cognition, Department of Psychology, Capital Normal University, Beijing 100048,
China
Tel: + 86 138 1083 9083; fax: + 86 105 890 8389;
e-mail: baoguoshi@cnu.edu.cn
Received 2 April 2017 accepted 11 May 2017
between sex and creativity. Since some studies have
found significant sex differences in cognitive aspects,
including creativity (e.g. [9,10]), explanations for the
existence of these differences have become increasingly
important. Generally, individuals may suggest that bio-
logical, cultural and historical, and social and environ-
mental factors as well as interactions among various
factors play important roles. To gain a deeper under-
standing of this issue, studies on sex differences have
been extended to cognitive neuroscience. Increasing
neurophysiological evidence supports the existence of
sex differences in the structural and functional organi-
zation of the brain [11,12]. However, among all of the
neuroscience investigations, sex and creativity studies are
quite few. Razumnikova and Vol’f [13] examined sex
differences in creativity related to global/local hemi-
spheric selective processing. Their results indicated that
verbal activity originality was more associated with the
success of selective processes in the left hemisphere
among males. However, this activity was more associated
with the selective functions of both hemispheres in
females. Ryman et al. [14] carried out a structural neuroi-
maging study with young adults from Mexico to explore
the association between white matter connectivity and
creative cognition. Significant inverse relationships were
observed between global connectivity (i.e. total connec-
tions of each region to all other regions), efficiency (i.e.
path lengths from each region to all other regions),
DOI: 10.1097/WNR.0000000000000820

clustering (i.e. number of connections among all adjacent
nodes of the region), and creative cognition in women,
whereas no significant relationship was noted in men.
Abraham et al. [15] carried out a functional neuroimaging
study with German undergraduates to investigate the sex
differences in conceptual expansion. The results indicated
that males showed significantly stronger activation in the
left inferior frontal gyrus, the inferior parietal lobule, and
the orbitofrontal cortex, whereas females showed stronger
activation in the anterior and posterior superior temporal
gyri, and the superior parietal cortex.
Taken together, no clear picture has emerged on the
relationship between sex and creativity. In addition, the
current research is needed for two major reasons. First,
most previous studies of sex and creativity have been
broad behavioral studies and not neuroscience investi-
gations. Even in the existing neuroscience investigations,
sex was considered an unimportant factor in creativity in
the whole study, which was not sufficient to fully
recognize the reasons for sex differences in creativity.
Second, most investigations have focused primarily on
the results in children and adolescents, whereas findings
in adults are rare. For a complete understanding of the
relationship between sex and creativity, it is imperative
to collect data from different age groups, cultural con-
texts, and research perspectives.
Because gray matter (GM) is considered to be respon-
sible for high-level mental functions studied by cognitive
neuroscientists, the current study investigated whether
sex differences exist in the relationship between GM
morphology and verbal creativity among adults from
Mainland China. Specifically, we used psychological
creativity tests for DT and voxel-based morphometry
(VBM) to measure gray matter volume (GMV) and
sought to determine the brain regions responsible for
these differences.
Methods
Participants
A total of 356 college students recruiting from Southwest
University participated in the current study, including
163 men (mean age = 20.20 years, SD = 1.35) and 193
women (mean age = 19.68 years, SD = 1.03). All partici-
pants were right-handed, and had no history of mental
health illness or neurological disorders. They were first
asked to sign a written informed consent document (for
the two 17-year-old participants, we obtained informed
written consent from their guardians), and then under-
took a set of psychological tests and MRI scans. This
study was part of an ongoing project to examine the link
between brain imaging, creativity, and personality [16].
The Institutional Review Board of the Southwest
University Brain Imaging Center approved this project.
Copyright r 2017 Wolters Kluwer Health, Inc. All rights reserved.
Sex differences in GMV and creativity Shi et al. 667
Assessment of general intelligence
The combined Raven’s test is used widely to psycho-
metrically measure individual intelligence and the
Chinese version was revised in 1994 by the Department
of Psychology in East China Normal University. It shows
high reliability and validity [17], and consists of 72 non-
verbal items in ascending order of difficulty. The total
score is computed by summing the items responded to
correctly.
Assessment of creativity
The verbal TTCT was used to assess each participant’s
DT ability. This test consists of seven tasks. Three tasks
ask participants to respond to a vivid scenario by gen-
erating questions, causes, and consequences. Participants
were given 5 min to complete of these tasks. The next
task asked participants to improve a toy elephant by
proposing creative ideas. Ten minutes were provided to
complete this task. In the fifth task, participants were
given 10 min to produce different ideas for the possible
use of cardboard boxes. The sixth task asked participants
to think of several carton-related questions in 5 min. In
the last task, participants were provided with an ima-
ginary scenario and told to imagine several possible
consequences in 5 min.
Given that originality can reflect creativity more strongly
than other aspects of creativity, the current study used
the originality score as the index of the verbal creativity.
Three raters scored the participants. The participant’s
responses were coded to corresponding scores on the
basis of norming scoring guides. First, the three raters
were shown the method of manual scoring and the
creativity definition. The results of the 30 participants
were then given to the three raters, and they were asked
to assess all of the items according to the uniform scoring
criterion. This step was used to determine the inter-rater
correlation coefficient, which was found to be significant
at 0.89.
Imaging data acquisition
All images were collected using a Siemens 3-T Trio scanner
(Siemens Medical Systems, Erlangen, Germany) with a
12-channel phased-array head coil. High-resolution three-
dimensional T1-weighted structural images were obtained
using a Magnetization Prepared Rapid Acquisition Gradient-
echo sequence (Repetition time/echo time = 1900 ms/
2.52 ms; flip angle = 9; Slices = 176; slice thickness = 1.0 mm;
resolution matrix = 256 × 256; voxel size = 1 × 1 × 1 mm3).
Images preprocessing for voxel-based morphometry
A VBM analysis was carried out using SPM8 (Welcome
Trust Center for Neuroimaging, London, UK, http://www.
fil.ion.ucl.ac.uk/spm/software/spm8/ ) with Matlab 7.8
(MathWorks, Natick, Massachusetts, USA). First, each
MRI scan was displayed using MRIcro (designed by
Chris Rorden in the Neuropsychology Lab, Columbia,
668 NeuroReport 2017, Vol 28 No 11
Descriptive statistics of the behavioral measures (N = 356;
Table 1
women = 193, men = 163)
Sex difference
Women
Men (mean ± SD) (mean ± SD) t-Value
Age 20.20 ± 1.35 19.68 ± 1.03 4.118
Combined 65.69 ± 3.86 66.25 ± 3.21 − 1.513
Raven’s test
Originality 43.89 ± 16.13 49.70 ± 17.87 − 3.194
Flexibility 26.12 ± 6.32 28.07 ± 6.15 − 2.900
Fluency 55.70 ± 18.86 59.91 ± 19.27 − 2.075
*P < 0.05.
**P < 0.01.
***P < 0.001.
South Carolina, USA) to screen for artifacts and gross
anatomical abnormalities. For a better registration result,
the reorientation of the images was set to the anterior
commissure manually. Second, the images were seg-
mented into white matter (WM), GM, and cerebrospinal
fluid using a new segmentation in SPM8. Third, the
DARTEL toolbox on SPM8 was used to produce WM
and GM population templates from the entire image
dataset. Fourth, each participant's images were normal-
ized into the Montreal Neurological Institute space and
then modulated to ensure that the relative volumes of
WM and GM were preserved following a spatial nor-
malization. Finally, to increase the signal-to-noise ratio,
these images were smoothed using a 10-mm full-width at
half-maximum Gaussian kernel.
Statistical analysis
A morphological group analysis was carried out using a
voxel-wise analysis of covariance in SPM8 to investigate
whether the relationship between regional gray matter
volume (rGMV) and the originality scores differed
between the sexes. During this analysis, the originality
score, age, combined Raven’s test score, and total GMV
were included as covariates. Except for total GMV, all of
the covariates were modeled to observe their unique
relationship with GMV within each sex using the inter-
actions option in SPM8, whereas total GMV was modeled
as a common association with rGMV across the sexes.
Moreover, t-tests were performed to identify the rela-
tionship between sex and the originality score.
Significant effects were defined as P value of less than
0.05 corrected at a nonstationary cluster level with an
underlying voxel level of P value of less than 0.001 and
value of more than 10 voxels. We then extracted each
participant’s regional mean GMV values from the cluster
of voxels where a significant interaction effect was
shown. These effects were analyzed using SPSS 17.0 for
Windows (SPSS Inc., Chicago, Illinois, USA). To visua-
lize the data, we graphed the interaction pattern.
Copyright r 2017 Wolters Kluwer Health, Inc. All rights reserved.
Results
Behavioral data
Table 1 presents the descriptive statistics and compar-
isons between the men and women with respect to the
P-value different measures. Two significant sex differences were
0.000*** noted in the table: men scored significantly lower than
0.131 women on creativity in terms of originality (t = − 3.194,
P < 0.01), flexibility (t = − 2.900, P < 0.01), and fluency
0.002**
0.004** (t = − 2.075, P < 0.05) and men were older than women
0.039* (t = 4.118, P < 0.001). Given that originality can reflect
creativity more strongly than other aspects, the main
focus of the current study was originality. Correlation
analysis indicated that both the correlation between age
and originality for men and for women were negative but
not significant, which suggested that there was no dif-
ference in the relationship between age and originality
with men and women. Moreover, to focus on whether
verbal creativity (originality) differs between men and
women, we controlled for age as a covariate in the follow-
up MRI data-processing step.
Sex differences in the associations between verbal
creativity (originality) and gray matter volume
To assess the structural difference between men and
women in verbal creativity, we used an analysis of covar-
iance that controlled for age, intelligence, and total GMV.
As Fig. 1 shows, an interaction between sex and originality
was found with respect to the GMV in the left temporo-
occipital junction (TOJ.L; Montreal Neurological Institute
coordinates: − 49.5, − 66, − 6; t = 4.62, P < 0.05; cluster
size = 604 mm3). Specifically, the originality scores were
positively related to the TOJ.L GMV in women, but
negatively related to it in men. Certain regions of interest
existed at an underlying threshold of P value less than
0.001 (uncorrected), including the left inferior parietal
cortex, bilateral superior frontal gyrus, right inferior frontal
gyrus, right inferior temporal gyrus, and left superior par-
ietal cortex (Table 2).
Discussion
To explain why significant sex differences exist in crea-
tivity, the current study investigated the sex differences
in the association between verbal creativity and GMV in
a large sample using VBM. The results indicated that
men scored significantly lower than women on measures
of creativity. Furthermore, an interaction was observed
between sex and originality with respect to the TOJ.
L GMV.
These behavioral results are consistent with some pre-
vious studies (e.g. [9]), but inconsistent with others. For
example, He et al. [18] examined adolescents and found
that males were superior in creative thinking. Grande
et al. [7] investigated adults and found that men with
primary or secondary levels of education scored higher
than their female counterparts on the Figural Originality
Scale, whereas women with a university education scored
 Sex differences in GMV and creativity Shi et al. 669

Fig. 1

The interaction effect between sex and originality scores (verbal creativity) in the regional GMV. The left panel indicates that verbal creativity was
positively associated with the GMV in the TOJ.L in women, but negatively associated among men at the peak voxel (x = − 49.5, y = − 66, z = − 6). The
right panel shows the corresponding partial correlation scatterplots of the interaction effects of sex and verbal creativity in the TOJ.L, previously
adjusted for age, intelligence, and total GMV for illustration purposes only. The y-axis of each scatterplot represents the standardized residuals of the
TTCT (originality) scores. The x-axis represents the standardized residuals of brain region GMV. The standardized residual measures controlled for
age, intelligence, and total GMV. The results are shown as P < 0.05, corrected for multiple comparisons at the cluster level with an underlying voxel
level of P < 0.001, uncorrected. GMV, gray matter volume; TOJ.L, left temporo-occipital junction; TTCT, Torrance Test of Creative Thinking.

Table 2 Sex differences in the associations between verbal creativity (originality) and gray matter volume
Montreal Neurological Institute coordinates

Brain regions Side t-Value x y z Cluster size

Temporo-occipital junction Left 4.62* − 49.5 − 66 −6 604
Inferior parietal cortex Left 3.98 − 52.5 − 34.5 37.5 297
Superior frontal gyrus Right 3.74 18 57 12 46
Superior frontal gyrus Left 3.71 − 20 54 11 121
Inferior frontal gyrus Right 3.70 48 31.5 1.5 87
Inferior temporal gyrus Right 3.59 46.5 − 54 −6 106
Superior parietal cortex Left 3.41 − 25.5 − 55.5 46.5 25

All t-scores reflect a VBM threshold of P < 0.001 (uncorrected) and a minimum cluster size (k) of 20 contiguous voxels.
Mean cluster level corrected at P <0.05.

higher than their male counterparts on the Verbal
Fluency Scale. These findings remind us to consider the
effects of social and cultural factors on the sex differences
present in creativity. One possible explanation for the
inconsistent results found across previous studies is that
social influence differs throughout development. The
environments and resources of primary and middle
school might favor boys because girls are taught to be
polite and restrained, and they might have a con-
sequential inhibited ideation [19]. In college, however,
girls might have access to more resources, and thus, they
begin to perform as well as boys or even better.
In addition to social and cultural factors, the brain imaging
results in the present study found an interaction between
sex and originality with respect to the TOJ.L GMV.

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670 NeuroReport 2017, Vol 28 No 11
Previous studies have found that this region lay between
the most caudal part of the anterior occipital sulcus (ventral
ramus) and the inferior temporal sulcus, near the motion
areas in the human brain [20,21]. According to Mobbs et al.
[22], TOJ was involved in the semantic and linguistic
aspects of humor comprehension, and it may be respon-
sible for detecting incongruence or surprise. Further, Amir
et al. [23,24] found that the activation of TOJ was related
to the linking of remote concepts or ideas to produce
semantic interpretations. Considering that these skills
are important features of creative associative thinking,
one can better understand these neural correlates of
creativity.
The present study also found a difference in the neural
correlates of creativity between women and men; speci-
fically, higher originality in women was linked with more
GMV and in men it was related to less GMV. Some
previous studies have provided evidences for sex differ-
ences in the relationship between creativity and the
brain. For example, Razumnikova et al. [25] conducted an
electroencephalogram study and found that women
showed a high α2 rhythm reactivity during verbal creative
thinking, whereas men showed a high reactivity of the β2
rhythm during figural creative thinking. Abraham et al.
[15] also found different patterns of brain activity that
reflected sex-related differences in strategy. During
conceptual expansion, men showed higher activity in
brain areas related to semantic cognition, decision mak-
ing, and rule learning; however, women showed higher
activity in regions related to social perception and speech
processing. One possible explanation for our findings is
that the verbal creativity tasks in the current study (i.e.
the verbal TTCT tasks involving word retrieval and
semantic processing) showed the function of the TOJ.L.
If this hypothesis is correct, then the behavioral results of
the current study showing that creativity scores were
higher among women than men are easier to understand
because the former sex has better verbal skills than the
latter. Moreover, Ryman et al. [14] found that highly
creative women showed lower connectivity, efficiency,
and clustering in more regions of the brain in processing,
whereas highly creative men showed more direct con-
nections between regions in local processing. This study
did not examine these indexes of connectivity; future
studies should identify the differential functional brain
networks between women and men on the basis of the
findings on structural image.
In summary, our findings suggest that the TOJ.L GMV
plays a unique role in the verbal creativity of men and
women because the latter typically surpass the former in
semantic processing, which is the mean function of the
left temporal region.
Acknowledgements
This research was supported by the National Natural
Science Foundation of China (31571138; 31271087;
Copyright r 2017 Wolters Kluwer Health, Inc. All rights reserved.
31571137), the Social Sciences Research Fund Project of
Beijing (14JYB015), the National Outstanding Young
People Plan, the Program for the Top Young Talents by
Chongqing, and the Beijing Advanced Innovation Center
for Imaging Technology (BAICIT-2016018).
Conflicts of interest
There are no conflicts of interest.
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