Neuroscience Letters 556 (2013) 79–83

Contents lists available at ScienceDirect

Neuroscience Letters
journal homepage: www.elsevier.com/locate/neulet

Gender versus brain size effects on subcortical gray matter volumes in

the human brain
Tianyu Tang a,c , Yun Jiao b,∗ , Xunheng Wang a,c , Zuhong Lu a,c
a
School of Biological Science and Medical Engineering, Southeast University, Nanjing 210096, China
b
Jiangsu Key Laboratory of Molecular Imaging and Functional Imaging, Department of Radiology, Nanjing 210009, China
c
Key Laboratory of Child Development and Learning Science (Ministry of Education), Southeast University, Nanjing 210096, China

h i g h l i g h t s

• Subjects were regrouped by gender and size to evaluate main effects on both factors.
• Brain size effects were distinguished from apparent gender differences.
• Brain size effects were found in right amygdala and bilateral caudate nucleus.
• Gender effects were found in right globus pallidum and bilateral putamen.
• Results found from two different datasets were consistent.

a r t i c l e i n f o a b s t r a c t

Article history: Previous studies had reported that volume differences of gray matter (GM) in subcortical regions of the
Received 23 January 2013 human brain were mainly caused by gender. Meanwhile, other studies had found that the distribution of
Received in revised form 9 September 2013 GM in the human brain varied based on individual brain sizes. Main effects of volume differences of GM
Accepted 26 September 2013
in subcortical regions remain unclear. Therefore, the goals of this study are twofold, namely, to determine
the main effects of volume differences of GM in subcortical regions of the human brain and to investigate
Keywords:
the independent or joint contribution of gender and brain size to subcortical volume differences. In this
Sex differences
study, 40 male and 40 female subjects with comparable brain sizes were selected from a population of
Brain size
Subcortical
198 individuals. The sample was divided into the following four groups: male and female groups with
Gray matter volume comparably large brain sizes and male and female groups with comparably small brain sizes. The main
effects of gender and of brain size and interactions between both factors in subcortical GM volumes were
examined by analyses of covariance (ANCOVAs) using a 2 × 2 design matrix. Volumes of GM in subcortical
regions were extracted and measured by an automatic segmentation method. Furthermore, we used two
datasets to test the reliability of our methods. In both datasets, we found significant brain size effects
in the right amygdala and the bilateral caudate nucleus and significant gender effects in the bilateral
putamen. No interactions between brain size and gender were found. In conclusion, both gender and
brain size independently contributed to volume distribution in different subcortical areas of the human
brain.
© 2013 Elsevier Ireland Ltd. All rights reserved.

1. Introduction reported to be involved in several gender-specific characteristics

Subcortical structures are located between the cerebral cortex
and the medulla oblongata in the human brain. These structures
include the nucleus accumbens, amygdala, caudate nucleus, hip-
pocampus, globus pallidus, putamen and thalamus that had been
∗ Corresponding author at: Jiangsu Key Laboratory of Molecular Imaging and
Functional Imaging, Department of Radiology, Zhongda Hospital, Medical School
of Southeast University, Nanjing 210009, China. Tel.: +86 25 8327 2541;
fax: +86 25 8327 2541.
E-mail address: yunjiao@seu.edu.cn (Y. Jiao).
such as addiction [29], motor control [22], and emotional memory
[5]. In addition, several neuropsychiatric disorders that are clearly
gender-specific are reported to be related to subcortical areas, such
as attention deficit hyperactivity disorder (ADHD) [12], and Parkin-
son’s disease (PD) [4]. Smaller volumes of the amygala [11] and
basal ganglia [23] were found in ADHD groups and smaller volumes
of the putamen was found in PD [13]. Thus, sexual dimorphism in
subcortical regions has gained attention in the neuroscience field.
Structural gender differences in subcortical regions have been
recently studied, including the nucleus accumbens in which pre-
and post-synaptic gender differences were detected [10]. A larger
volume of gray matter (GM) was found in the amygdala among

0304-3940/$ – see front matter © 2013 Elsevier Ireland Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.neulet.2013.09.060
80 T. Tang et al. / Neuroscience Letters 556 (2013) 79–83

males [7] and in the caudate nucleus among females [16,19]. How- Table 1
Age, gray matter volumes and total brain volumes.
ever, no significant gender differences were reported in the caudate
in another region of interest (ROI)-based study [24]. In the hip- Data set I (Beijing Zang)
pocampus, no volume differences between male and female groups
Age GM TBV
were reported, however, after considering age and brain size, the
Male (N = 76) 21.145 ± 1.831 718.582 ± 56.082 1503.467 ± 102.829
results showed that females had a larger hippocampus volume than
Female (N = 122) 21.172 ± 1.835 653.903 ± 51.697 1362.347 ± 97.776
that of males [2]. Studies had observed that males have a signifi- MS (N = 20) 21.200 ± 2.285 656.793 ± 39.209 1376.682 ± 48.735
cantly larger volume in the pallidum and putamen [24] and in the ML (N = 20) 21.300 ± 1.838 710.551 ± 33.350 1488.941 ± 44.448
thalamus among females [19,27]. By contrast, a study stated no gen- FS (N = 20) 21.500 ± 2.090 651.378 ± 34.838 1372.751 ± 49.193
der effects to volume distribution in the thalamus after considering FL (N = 20) 20.800 ± 1.908 715.361 ± 27.542 1489.808 ± 46.306

the effects of brain size [26].

Data set II (Cambridge Buckner)
The brain sizes of males had been reported to be larger than
that of females [18,21]. While the aforementioned studies reported Age GM TBV
on structural gender differences in subcortical regions, a question Male (N = 74) 21.000 ± 2.158 709.032 ± 49.121 1506.803 ± 109.347
emerges regarding the contribution of brain size and of volume Female (N = 123) 21.057 ± 2.413 640.875 ± 40.527 1354.388 ± 94.739
distribution to gender differences [14,18]. Independently investi- MS (N = 20) 20.400 ± 1.569 662.361 ± 30.395 1380.453 ± 53.404
ML (N = 20) 20.850 ± 1.599 709.552 ± 26.451 1506.005 ± 39.774
gating gender from brain size effects entails an alternative process
FS (N = 20) 21.250 ± 2.845 648.080 ± 24.596 1372.722 ± 53.289
in comparing male and female groups with comparable brain sizes FL (N = 20) 20.550 ± 2.762 698.505 ± 29.563 1508.090 ± 45.288
[16,25,30]. Meanwhile, independently investigating brain size from
Data are presented as mean ± SD or number.
gender effects requires strict matching of the gender factor. GM, gray matter; TBV, total brain volume; MS: males with smaller brain size; ML,
In this study, we used an automatic segmentation toolkit [20] Males with larger brain size; FS, Females with smaller brain size; FL, Females with
to extract subcortical structures from the brain. We extracted larger brain size.
seven subcortical structures bilaterally that include the left and Age is shown in years; GM and TBV are shown in milliliters.

right nucleus accumbens, amygdala, caudate nucleus, hippocam-

pus, globus pallidus, putamen, and thalamus. After calculating
the subcortical GM volumes (SGMVs), we conducted analyses of
covariance (ANCOVAs) using a 2 × 2 design matrix to evaluate the
following: (1) gender effects of SGMVs between males and females
with comparable brain sizes, (2) brain size effects between large
and small brains, and (3) interactions between gender and brain
size effects. In addition, we used two large datasets to test the
reliability of this study and to assess the consistency of the results.
2. Materials and methods
2.1. Data information
There were two independent datasets involved in this study.
All of our data were downloaded from the 1000 functional Con-
nectomes Project [3]. In dataset I, from Beijing Zang acquired
with a SIEMENS 3 T Trio scanner, there were totally 198 subjects
(122 males and 76 females) aged from 18 to 26. Parameters for
the scans (T1-weighted sagittal three-dimensional magnetization-
prepared rapid gradient echo sequence: MP-RAGE) were as follows:
128 slices, TR = 2530 ms, TE = 3.39 ms, slice thickness = 1.33 mm, flip
angle = 7◦ , inversion time = 1100 ms, FOV = 256 mm × 256 mm, and
in-plane resolution = 256 mm × 192 mm [15]. In dataset II, from
Cambridge Buckner acquired with a SIEMENS 3 T Trio scanner,
there were totally 198 subjects (123 males and 75 females) aged
from 18 to 30. Parameters for scans (MP-RAGE) were as follows:
TR = 2200 ms, TE = 1.54 ms, flip angle = 7◦ , inversion time = 1100 ms,
FOV = 230 mm × 230 mm, voxel size = 1.2 mm × 1.2 mm × 1.2 mm
[32].
2.2. Preprocessing
Using VBM8 (Version 435, http://dbm.neuro.uni-jena.de/vbm/)
[1] based on SPM8 (http://www.fil.ion.ucl.ac.uk/spm/software/
spm8/), the whole brain was classified into three different types:
GM, white matter (WM) and cerebrospinal fluid (CSF). The volumes
of each tissue were calculated with VBM8 by summing all the rel-
ative tissue probabilities in native space. Total brain volume (TBV)
was defined by adding the volumes of GM, WM and CSF [16].
The left and right nucleus accumbens, amygdala, caudate
nucleus, hippocampus, globus pallidus, putamen and thala-
mus were extracted from the whole brain using an automatic
segmentation toolkit called FIRST (Version 1.2, FMRIB’s Inte-
grated Registration and Segmentation Tool, http://www.fmrib.
ox.ac.uk/fsl/first/index.html) [20] based on FSL (FMRIB Software
Library, http://www.fmrib.ox.ac.uk/fsl/). All the segmentations
were performed on the original structure data. To improve the accu-
racy of the segmentation, an automatic boundary correction was
included [24]. Moreover, for each structure the left and right maps
were generated independently. An example of FIRST segmentation
results for a single subject is shown in Fig. 1. In this study, all seg-
mented structures were further examined manually by overlaying
on the original T1-weighted data. We removed 1 out of 396 (in
dataset II) for the failure of segmentation.
After tissue segmentation with VBM, GM images represented
GM probabilities voxel-wisely. With the extracted structures from
FIRST, SGMVs were calculated by summing all the products of voxel
size with GM probabilities voxel-wisely within each structure in
native space.
2.3. Subject regrouping
Our subject selection strategy was conducted as same as Luders
et al. did in [16]. A total of 40 males and 40 females, paired based
on comparable TBV, were selected from the original dataset. In our
study, the maximum TBV differences between the matched pairs
were 5.855 and 11.982 ml for datasets I and II, respectively. We then
ranked the subjects in each group in ascending order based on TBVs
and identified the first 20 subjects as those with small brains, while
the last 20 subjects as those with large brains. More specifically, the
first 20 male and female subjects identified with small brains were
categorized as MS and FS groups, while the last 20 male and female
subjects identified with large brains were categorized as ML and FL
groups, respectively. Table 1 shows the demographic information of
the subjects from both the original dataset and from the subgroups.
2.4. Statistics analysis
All variables in this study were analyzed using SPSS 19.0. Firstly,
we examined age, global GM volume and TBV differences between
groups with two sample t-tests. To investigate the main effects
of TBV, gender and the interactions between these two, 2 × 2
ANCOVAs were conducted in SGMVs, with TBV and gender as the
 T. Tang et al. / Neuroscience Letters 556 (2013) 79–83
Fig. 1. Automatic segmentation results of subcortical regions in native space overlayed on a T1-weighted image of one single subject. Subcortical regions as listed on figure:
nucleus accumbens (blue), amygdala (turquoise blue), caudate nucleus (emerald greet), hippocampus (yellow), globus pallidus (orange), putamen (red); thalamus (purple).
(For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
independent variables and age as covariate. More specifically, to
examine the main TBV effects in SGMVs, SGMVs were compared
between subjects with large brains (ML and FL) and subjects with
small brains (MS and FS). To examine the main gender effects in
SGMVs, SGMVs were compared between male subjects (ML and
MS) and female subjects (FL and FS). The threshold for all tests was
p-value < 0.05 (Bonferroni corrected).
3. Results
As listed in Table 1, in datasets I and II, male subjects in the
original dataset had a significant larger TBV than that of female sub-
jects, with p-value < 0.001, in addition, the male group had larger
GM volumes than those of the female group, with p-value < 0.001.
No significant age differences were observed between the original
male and female groups.
After regrouping, in both datasets, no significant differences
in age were observed between the subgroups. Larger TBVs were
obtained in the ML than in the MS groups, with p-value < 0.001, as
well as in the FL than in the FS groups, with p-value < 0.001. No dif-
ferences in TBVs were derived between the ML and the FL groups
and between the MS and the FS groups.
Using ANCOVAs, in datasets I, we found significant TBV effects
in the right amygdala, and in the left and right caudate. Signifi-
cant gender effects were found in the right pallidus, and in the left
and right putamen. In dataset II, we found significant TBV effects
in the right amygdala, in the left and right caudate and in the
right hippocampus. In addition, we found gender effects in the left
accumbens and the left and right putamen. In both datasets, no sig-
nificant interactions were identified between brain size and gender.
All the listed test results survived with a threshold as p-value < 0.05
(Bonferroni corrected).
4. Discussion
In this study, we used two datasets to investigate the main
effects of brain size and of gender in SGMVs, respectively. In each
dataset, after calculating TBV, 40 male and 40 female subjects with
comparable brain sizes were selected and divided into four groups,
namely, MS, ML, FS, and FL groups. In both dataset, significant
brain size effects were found in the bilateral caudate and in the
right amygdala, while gender effects were determined in the bilat-
eral putamen. No interactions between gender and brain size were
81
detected, indicating that both gender and brain size effects inde-
pendently contribute to the apparent differences in SGMVs.
In general, male brains are approximately 8–10% larger than
those of females [18]. Thus, in a study aiming to control TBV
between male and female groups, Luders et al. selected 24 males
and 24 females with comparable brain sizes from a total of 145 sub-
jects [16], accounting to 32.65% from the original sample size and a
maximum TBV difference of 5.16 ml. In the present study, we chose
a similar regrouping strategy, accounting to a proportion of 40.04%
and maximum differences of 5.855 and 11.982 ml in datasets I and
II, respectively. As a result, a total of 80 subjects were randomly
selected with matched brain sizes from 198 subjects in the origi-
nal dataset. The proportion varies between different datasets and
depends on the threshold of the maximum difference between the
matched pairs.
In datasets I and II, we found brain size effects in the bilat-
eral caudate. More specifically, subjects with larger brain sizes had
larger GM volumes in the caudate (see Table 2), while male and
female groups with matched brain sizes had no significant GM vol-
ume differences. Luders et al. reported that males had smaller GM
volumes in the bilateral caudate than those of females [16]. Smaller
GM volumes in the caudate of males were also reported in another
earlier study [9]. The current study contradicts these studies, but
our results are consistent with a recent ROI-based study in which no
significant gender effects were detected in the caudate [24]. These
two major reasons can explain the discrepancies. First, different
methods were used. Luders et al. examined modulated GM volumes
that were corrected for individual brain size, whereas we examined
GM volumes that were not corrected for brain size in native space
[17]. Second, a different sample size was used. Filipek et al. used a
small sample size (10 male and 10 female subjects) [9], whereas the
original data pool in the current study and that of Rijpkema et al.
were large at 198 and 1004 subjects, respectively [24].
Brain size effects were detected in the right amygdala of both
datasets in this study. Larger brains were associated with larger
GM volumes in the right amygdala, while no gender effects were
observed in the amygdala. Our results echoed another study, which
indicated that larger GM volume in the amygdala was associ-
ated with larger brains and that the amygdala volume was not
directly proportional to TBV [2]. Moreover, GM volume in amyg-
dala was found larger among males in a VBM study that did not
consider the brain size factor [7]. Our results suggested that the
detected gender differences in the right amygdala were caused by
82 T. Tang et al. / Neuroscience Letters 556 (2013) 79–83

Table 2
Subcortical gray matter volumes and the results of analyses of covariance on the main effects of brain size, gender and interaction between brain size and gender.

Data set I (Beijing Zang)

Subcortical gray matter volumes p-Value

MS (N = 20) ML (N = 20) FS (N = 20) FL (N = 20) TBV Gender TBV × gender

L 0.731 ± 0.152 0.775 ± 0.111 0.703 ± 0.141 0.772 ± 0.141 – – –

Accumbens
R 0.562 ± 0.100 0.624 ± 0.106 0.606 ± 0.098 0.649 ± 0.146 – – –

L 1.318 ± 0.251 1.465 ± 0.429 1.431 ± 0.247 1.457 ± 0.278 – – –

Amygdala
R 1.340 ± 0.323 1.498 ± 0.398 1.437 ± 0.201 1.710 ± 0.237 0.002* – –

L 3.507 ± 0.335 3.888 ± 0.369 3.434 ± 0.292 3.816 ± 0.382 0.000* – –

Caudate
R 3.652 ± 0.390 3.988 ± 0.349 3.502 ± 0.430 3.978 ± 0.429 0.000* – –

L 4.016 ± 0.371 4.038 ± 0.735 3.992 ± 0.358 4.371 ± 0.471 – – –

Hippocampus
R 4.186 ± 0.371 4.273 ± 0.537 4.182 ± 0.509 4.581 ± 0.457 – – –

L 0.098 ± 0.065 0.065 ± 0.041 0.060 ± 0.028 0.056 ± 0.030 – – –

Pallidum
R 0.055 ± 0.042 0.039 ± 0.029 0.027 ± 0.020 0.026 ± 0.018 – 0.002* –

L 3.816 ± 0.549 3.615 ± 0.577 3.199 ± 0.527 3.461 ± 0.655 – 0.002* –

Putamen
R 3.658 ± 0.519 3.582 ± 0.527 3.169 ± 0.468 3.377 ± 0.617 – 0.003* –

L 3.865 ± 0.418 3.786 ± 0.783 3.572 ± 0.578 3.933 ± 0.672 – – –

Thalamus
R 3.774 ± 0.538 3.894 ± 0.735 3.624 ± 0.635 3.982 ± 0.770 – – –

Data set II (Cambridge Buckner)

Subcortical gray matter volumes p-Value

MS (N = 20) ML (N = 20) FS (N = 20) FL (N = 20) TBV Gender TBV × gender

L 0.794 ± 0.117 0.868 ± 0.152 0.689 ± 0.098 0.736 ± 0.109 – 0.000* –

Accumbens
R 0.664 ± 0.128 0.751 ± 0.101 0.659 ± 0.140 0.682 ± 0.157 – – –

L 1.684 ± 0.275 1.710 ± 0.227 1.578 ± 0.203 1.627 ± 0.264 – – –

Amygdala
R 1.555 ± 0.218 1.739 ± 0.268 1.533 ± 0.202 1.678 ± 0.166 0.001* – –

L 3.692 ± 0.355 3.997 ± 0.497 3.447 ± 0.393 3.788 ± 0.568 0.003* – –

Caudate
R 3.944 ± 0.355 4.275 ± 0.493 3.658 ± 0.365 4.081 ± 0.541 0.000* – –

L 4.252 ± 0.508 4.423 ± 0.443 4.130 ± 0.451 4.461 ± 0.405 – – –

Hippocampus
R 4.178 ± 0.526 4.520 ± 0.326 4.096 ± 0.297 4.434 ± 0.350 0.000* – –

L 0.160 ± 0.075 0.119 ± 0.052 0.113 ± 0.058 0.097 ± 0.058 – – –

Pallidum
R 0.104 ± 0.083 0.073 ± 0.033 0.066 ± 0.043 0.047 ± 0.032 – – –

L 4.001 ± 0.563 3.809 ± 0.541 3.349 ± 0.649 3.413 ± 0.618 – 0.000* –

Putamen
R 3.831 ± 0.495 3.751 ± 0.470 3.190 ± 0.533 3.290 ± 0.488 – 0.000* –

L 4.027 ± 0.617 4.450 ± 0.563 3.959 ± 0.563 4.128 ± 0.515 – – –

Thalamus
R 4.056 ± 0.504 4.456 ± 0.490 3.993 ± 0.466 4.180 ± 0.597 – – –

Data are presented as mean ± SD or number.

“–” indicates that the main effect was not significant. The threshold was p-value < 0.05 (Bonferroni corrected).

individual brain size differences between the male and the female
groups.
Gender effects were observed in the bilateral putamen, in which
males exhibited significant larger GM volumes, whereas no brain
size effects were indicated. Our results are consistent with another
study on sexual dimorphism in the basal ganglia [24], which
reported larger GM volumes in the putamen of male groups. More-
over, the putamen is known to be involved in motor circuit [28],
and the motor function generally displays sexual dimorphism [8].
In addition, the putamen was reported to be reduced in PD [13],
to which males are highly susceptible [4]. Overall, we inferred that
gender differences mainly caused SGMVs differences in the puta-
men.
In a word, the main effects of brain size, gender and interaction
between these two were examined in the subcortical regions using
2 × 2 ANCOVAs. Significant brain size effects were observed in the
bilateral caudate and in the right amygdala, while significant gen-
der effects were found in the bilateral putamen. No interactions
between brain size and gender factors were indicated in SGMVs.
Previous studies had determined the association of volume differ-
ences in the caudate and in the amygdala to gender, while brain
size effects were not considered [7,19]. By confirming from two
different datasets, our results showed that, after careful consider-
ation, brain size effects could be distinguished from the apparent
gender differences. In the supplementary document, we listed
correlation analysis results of the bilateral caudate and putamen
volumes. The results were partly accordant to our present results.
These results confirmed that our current results were reasonable
and ANCOVA was suitable for the present study.
We conducted the analysis in two different datasets to test the
reliability of our study. Though our results from both datasets were
mostly consistent, indicating their reliability, a number of differ-
ences were noted. We, for example, observed gender effects in the
right pallidum in dataset I, but not in dataset II. Moreover, in dataset
II, TBV effects in the right hippocampus and gender effects in the left
accumbens were found, but not in dataset I. The different machines
and varied populations of two different datasets might be one of
our limitations of this work. Magnetic resonance imaging signals
that acquired from different machines in this study may have var-
ied, resulting in different results. Additionally, two different ethnic
groups were present in our datasets. Ethnic populations usually
have distinct genetic makeup, diet, and environmental factors that
may influence their brain development [6]. These two reasons can
explain the contrasting results of the two datasets.
 T. Tang et al. / Neuroscience Letters 556 (2013) 79–83
Furthermore, in this study, we investigated gender and brain
size effects to SGMVs. Consisting of neuronal bodies, axons, den-
drites, synapses, glia cells and others, GM is a major component of
the central nervous system [16]. With the assumption that more
GM volume reflects a larger number of neurons and better per-
formance of cognitive functions, several studies had attempted to
explain the effect of gender differences to GM in various regions
[16,31]. In our study, we found significant larger GM volume in the
putamen between brain sizes matched male and female groups.
With the involvement of the putamen in motor functions, this
observation on the GM volume explains the generally better per-
formance and faster development of motor functions among male
subjects than females [28]. However, the mechanism of GM volume
increase must be investigated carefully. We will continue to search
neurological evidence that will explain the relationship between
GM volume and cognitive functions in the future.
5. Conclusion
To our knowledge, this study is the first to distinguish brain size
effects from gender effects in subcortical areas using an ROI volu-
metric method. Based on the results of the two datasets, significant
brain size effects are found in the right amygdala and in the bilateral
caudate, while gender effects are observed in the bilateral putamen.
We conclude that both gender and brain size effects contribute to
apparent gender differences in SGMVs.
Conflicts of interest
There are no conflicts of interest.
Acknowledgements
The work was supported by National Program on Key Basic
Research Project (No. 2013CB733800, 2013CB733803) and The
National Natural Science Foundation of China General Projects (No.
81271739). The authors thank the 1000 Functional Connectomes
Project for kindly sharing the dataset.
Appendix A. Supplementary data
Supplementary data associated with this article can be
found, in the online version, at http://dx.doi.org/10.1016/
j.neulet.2013.09.060.
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