Integrative systems 1
Altered resting-state functional connectivity of default-mode
network and sensorimotor network in heavy metal
music lovers
Yan Suna,b, Congcong Zhanga,b, Shuxia Duana,b, Xiaoxia Duc and
Vince D. Calhound,e,f
The aim of this study was to investigate the spontaneous
neural activity and functional connectivity (FC) in heavy
metal music lovers (HMML) compared with classical music
lovers (CML) during resting state. Forty HMML and 31 CML
underwent resting-state functional MRI scans. Fractional
amplitude of low-frequency fluctuations (fALFF) and seed-
based resting-state FC were computed to explore regional
activity and functional integration. A voxel-based two-
sample t-test was used to test the differences between the
two groups. Compared with CML, HMML showed functional
alterations: higher fALFF in the right precentral gyrus, the
bilateral paracentral lobule, and the left middle occipital
gyrus, lower fALFF in the left medial superior frontal gyrus,
an altered FC in the default-mode network, lower
connectivity between the right precentral gyrus and the left
cerebellum-6 and the right cerebellum-3, and an altered FC
between the left paracentral lobule and the sensorimotor
network, lower in the right paracentral lobule and the right
inferior temporal gyrus FC. The results may partly explain
Introduction
Individual music preferences are a long-term stable
emotional state shaped by the personality and regulate
the brain’s response [1]. Heavy metal music is rock music
with a particular emphasis on strong sound, beat and
personal style and complex melody, which expresses a
variety of intense emotions (e.g. anger, provocation) and
heavy metal music styles show stress-related negative
effects, including sleep disorders, weariness, and anxiety
[2,3]. A study in 2010 showed that one in three teenagers
often listen to heavy metal music [4]. Understanding the
neural mechanism of heavy metal music lovers (HMML)
can help us develop a healthy development of a per-
sonality plan for HMML.
In recent years, researchers have carried out considerable
research on the effects of heavy metal music. Early
research showed that HMML had a higher proportion of
drug abuse, smoking, and reckless behavior and long-
term listening to heavy metal music will lead to disorders
of behavioral and emotional cognition in HMML [3–5].
In the meantime, a large number of studies have also
proved that different types of musical stimulations can
activate different brain regions. When listening to sad
music, there was an increase in the blood oxygenation-
0959-4965 Copyright © 2017 Wolters Kluwer Health, Inc. All rights reserved.
Copyright r 2017 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
the disorders of behavioral and emotional cognition in
HMML compared with CML and are consistent with our
predictions. These findings may help provide a basic
understanding of the potential neural mechanism
of HMML. NeuroReport 00:000–000 Copyright © 2017
Wolters Kluwer Health, Inc. All rights reserved.
NeuroReport 2017, 00:000–000
Keywords: default-mode network, functional connectivity,
heavy metal music lovers, resting-state functional MRI,
sensorimotor network
a
School of Psychology, Liaoning Normal University, Dalian, bLiaoning Collaborative
Innovation Center of Children and Adolescents Healthy Personality Assessment
and Cultivation, Liaoning, cDepartment of Physics, Shanghai Key Laboratory of
Magnetic Resonance, East China Normal University, Shanghai, China, dMind
Research Network, eDepartment of Psychiatry and fElectrical Engineering,
University of New Mexico, Albuquerque, New Mexico, USA
Correspondence to Yan Sun, PhD, Liaoning Normal University, Dalian, Liaoning
Province 116029, China
Tel: + 86 139 4090 0485; e-mail: sun9199@163.com
Received 23 June 2017 accepted 1 August 2017
level dependent signal in the hippocampus (HIC) and
the amygdala. While listening to happy music, there were
significant increases in the ventral and dorsal striatum,
anterior cingulate, and parahippocampal gyrus [6]. Mozart
music is believed to enhance the listeners’ cognitive
performance and increase the listeners’ corresponding
brain activation [7]. Rhythmic music has been shown to
activate the brain areas mostly involved in movement [8].
The activity of particular brain areas is thus likely dif-
ferent in long-term HMML. Despite this, few studies
have explored the neural mechanism of HMML.
Whether or not there are functional changes in particular
brain regions involved in HMML remain unclear.
Blood oxygenation-level dependent functional MRI sig-
nals have been used widely to investigate brain oscilla-
tory modulations [9]. The amplitude of low-frequency
oscillations measured as the fractional amplitude of low-
frequency fluctuations (fALFF), represent the strength
of intrinsic spontaneous neural activity and gross pulsatile
effects can be avoided in fALFF [10]. Resting-state
functional connectivity (RSFC) represents brain func-
tional connections (cross-correlations) during rest [11].
Both fALFF and RSFC have been used widely in
amyotrophic lateral sclerosis [9], generalized anxiety
DOI: 10.1097/WNR.0000000000000883
 2 NeuroReport 2017, Vol 00 No 00
disorder [11], and schizophrenia [12]. These studies show
the utility of fALFF and RSFC as promising methods to
explore brain functional alterations.
Usually, classical music includes jazz and folk music and
it’s lovers always convey a gentle image to others. In
contrast heavy metal music includes rock and alternative
music and it’s lovers are typically thought to express a
hard image to others [3]. Researchers have carried out
behavioral and emotional cognition studies to compare
these two groups [3,13]. However, there has not yet been
a study to evaluate brain function differences between
classical music lovers (CML) and HMML. In this study,
we used CML as a control group to investigate the dif-
ferences in the neural mechanisms between HMML
and CML.
In summary, we aimed to use fALFF and RSFC to
explore the alterations in spontaneous neural activity and
functional connectivity (FC) in HMML; we hypothe-
sized that compared with CML, (a) changes in sponta-
neous neural activity (fALFF) in HMML would be
found and (b) significant differences in RSFC between
regions with fALFF alterations and cognitive, behavioral,
and emotional-related brain regions in HMML would
be found.
Patients and methods
Participants
There is no consistent way to identify music style pre-
ferences now and previous studies suggest that the best
way to evaluate individual music preference is self-report
[1,4,5]. The criteria for screening participants were as fol-
lows: (a) choose heavy metal music or classical music from
14 kinds of music genres as their favorite music and self-
reported preference score of heavy metal music or classical
music is higher than three points [preference was rated on a
five-point Likert-type scale with endpoints at 1 (not at all)
and 5 (a great deal)]; [1] (b) correctly list three or more
heavy metal musicians or classical musicians; [1] (c)
volunteers deem that they are HMML or classical music
lovers; [4] and (d) volunteers take the initiative to listen to
heavy metal music or classical music for at least 1 year on
an average of at least 5 h every week [5]. On the basis of
this standard, 71 participants were selected including 40
HMML (22 men, 18 women, 23.03 ± 4.92 years) and 31
CML (10 men, 21 women, 24.19 ± 3.97 years). Age
(P = 0.229) and sex (P = 0.058) differences were not sig-
nificantly different. Participants reported no physical or
mental illness and voluntarily signed an informed consent.
The volunteers were all recruited from among college
students in school and the experiment was audited by the
Ethics Committee of Liaoning Normal university.
MRI data acquisition
Images were collected on a 3.0 T German Siemens Vision
Scanner (Siemens Healthineers, Shanghai, China). The par-
ticipants were instructed to relax, keep their eyes closed, stay
Copyright r 2017 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
awake, and avoid active thinking activities. 210 functional
images of each participant were acquired using an echo-planar
imaging sequence (slices = 33, repetition time/echo
time = 2000 ms/30 ms, flip angle = 90°, field of view = 220
mm × 220 mm, slice thickness = 3 mm, matrix = 64 × 64,
voxel size = 3.4 mm × 3.4 mm × 3 mm), lasting 7 min T1
structural images were acquired for spatial normalization and
localization (repetition time/echo time = 2530 ms/2.34 ms, flip
angle = 7°, slice thickness = 1 mm, field of view = 256
mm × 256 mm, matrix = 256 × 256, voxel size = 1.0 mm
× 1.0 mm × 1.0 mm). All participants were scanned success-
fully and none of them reported being uncomfortable during
or after the procedure.
Data preprocessing
Preprocessing was performed using SPM8 (http://www.fil.
ion.ucl.ac.uk/spm/software/spm8) and REST (http://www.
restfmri.net). The DICOM files were converted into
NifTI images, and the first 10 volumes were removed.
Preprocessing included slice timing correction, head-
motion correction, spatial normalization to the Montreal
Neurological Institute space using T1 structural images,
resampling to 3 mm × 3 mm × 3 mm, spatial smoothing
with a Gaussian kernel (full width at half maximum = 4
mm), linear detrending, and a band-pass filter
(0.01–0.08 Hz) using REST software. The data of all
participants fulfilled the criteria of maximum translation
less than 2 mm and rotation less than 2°; no significant
differences between the groups were found for any
movement directions (P > 0.58) in the maximum move-
ment parameters.
Fractional amplitude of low-frequency fluctuations
analysis
In this study, we used fALFF for further analysis as
ALFF is more susceptible to physical noise [10]. fALFF
was calculated using the REST software. After pre-
processing, a fast Fourier transform was used to convert
the functional MRI data from the time domain into the
frequency domain. The fALFF represents the relative
contribution of low-frequency oscillations within a spe-
cific frequency band (0.01–0.08 Hz) to the full frequency
range (0–0.25 Hz) [10]. Then, the fALFF of each voxel
was divided by the global mean values for standardiza-
tion. Finally, the whole-brain voxel-wise fALFF of each
participant in the HMML and CML groups were
obtained.
Two-sample t-tests were used to compare the differences
in fALFF between groups with age, sex, and grey matter
as covariates using the REST software. Significance in
the resulting statistical maps was set at 0.05 (corrected for
multiple comparisons); multiple-comparison corrections
were performed using Monte Carlo simulation (single
voxel P = 0.05, 1000 simulations, cluster connection
radius r = 5 mm, full width at half maximum = 8 mm, the
union of the two-group one-sample t-test significant brain
 Altered FC in HMML Sun et al. 3

Fig. 1

Parametric maps overlapped on the three-dimensional T1 template images in software (slice viewer, REST, version 1.8; http://www.restfmri.net) show
fALFF differences between HMML and CML. The left medial superior frontal gyrus shows lower fALFF values in HMML compared with CML and are
depicted with cold colors (blue, light blue, green); four regions (left paracentral lobule, right paracentral lobule, right precentral gyrus, and left middle
occipital gyrus ) show higher fALFF values in HMML compared with CML and are depicted with warm colors (red, orange, yellow) (P < 0.05, with αsim
correction). On the right, color bars indicate t values from a global voxel-based two-sample t-test analysis. CML, classical music lovers; fALFF,
fractional amplitude of low-frequency fluctuations; HMML, heavy metal music lovers; MOG, middle occipital gyrus; PCL, paracentral lobule; PreCG,
precentral gyrus; SFGmed, medial superior frontal gyrus.

regions as a mask). The resulting statistical map of Table 1 Significant changes in fractional amplitude of low-
frequency fluctuations of heavy metal music lovers
fALFF is shown in Fig. 1. The results were visualized
using the REST slice viewer (http://www.restfmri.net). Montreal Neurological
Institute coordinates

Functional connectivity analysis Number of

Brain regions Side x y z voxels Peak t value
FC analysis was carried out using significantly altered
fALFF, which were defined as regions of interest. Higher fALFF in HMML
Extracting the average time series of regions of interest to PreCG Right 60 −6 45 85 4.6139
PCL Right 3 − 36 60 130 3.4456
analyze FC based on the whole brain, head motion PCL Left 0 − 21 57 83 3.0214
parameters, global mean signal, white matter signals, and MOG Left − 39 − 87 15 70 5.4308
cerebrospinal fluid signals as covariates were extracted Lower fALFF in Left −3 66 0 73 − 4.5432
HMML
[11]. Finally, correlation maps were transformed from (SFGmed)
r into z-value FC maps, followed by two-sample t-tests
fALFF, fractional amplitude of low-frequency fluctuations; HMML, heavy metal
between two groups with age, sex, and gray matter as music lovers; MOG, middle occipital gyrus; PCL, paracentral lobule; PreCG,
covariates. An αsim-corrected significance level of P value precentral gyrus; SFGmed, medial superior frontal gyrus.
of less than 0.05 was obtained for clusters with an indi-
vidual voxel height threshold of a P value of less
HMML showed significantly higher FC with the bilat-
than 0.05.
eral superior parietal gyrus (SPG) and itself. With the
seed located in the left PCL, HMML showed sig-
Result nificantly lower FC with the left PreCG and higher FC
Regional neural activity with the left postcentral gyrus. With the seed located in
Compared with CML, HMML showed higher fALFF in the left SFGmed, HMML showed significantly lower FC
the right precentral gyrus (PreCG), the bilateral para- with the left MOG, right angular gyrus (ANG), left HIC,
central lobule (PCL), and the left middle occipital gyrus and bilateral middle temporal gyrus (MTG). With the
(MOG); lower fALFF was observed in the left medial seed located in the right PreCG, HMML showed sig-
superior frontal gyrus (SFGmed) (P < 0.05, αsim-corrected). nificantly lower FC with the right cerebellum-3 and left
The results are shown in Fig. 1 and Table 1. cerebellum-6. With the seed located in the right PCL,
HMML showed significantly lower FC with the right
Voxel-wise analysis of resting-state neural functional inferior temporal gyrus (ITG). The results are shown in
connectivity Fig. 2 and Table 2.
We selected the left MOG, bilateral PCL, left SFGmed,
and right PreCG as seeds because of the significantly
altered fALFF in HMML compared with CML. A voxel-
based two-sample t-test was performed to examine the Discussion
differences in RSFC between the two groups (P < 0.05, In our study, we found that the spontaneous activity of
αsim-corrected). With the seed located in the left MOG, right PreCG, bilateral PCL, and left MOG in HMML

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 4 NeuroReport 2017, Vol 00 No 00

Fig. 2

Sagittal plane shows an altered functional connectivity (FC) between HMML and CML. The red nodes represent seeds with significantly altered
fALFF for calculating RSFC. The blue nodes and green lines represent a lower FC in HMML compared with CML, whereas black nodes and yellow
lines represent higher FC. The results were visualized using the BrainNet viewer package (http://www.nitrc.org/projects/bnv). ANG, angular gyrus;
CER-3, cerebellum-3; CER-6, cerebellum-6; CML, classical music lovers; fALFF, fractional amplitude of low-frequency fluctuations; HMML, heavy
metal music lovers; HIC, hippocampus; ITG, inferior temporal gyrus; MOG, middle occipital gyrus; PCL, paracentral lobule; PoCG, postcentral gyrus;
PreCG, precentral gyrus; RSFC, resting-state functional connectivity; SPG, superior parietal gyrus; SFGmed, medial superior frontal gyrus.

Table 2 Regions with significantly altered functional connectivity in addition, Farzaneh et al.’s [8] research showed that
heavy metal music lovers
bilateral PreCG were activated when listening to rhyth-
Montreal mic music compared with smoothing rhythmic music,
Neurological Institute
coordinates
although the rhythm of heavy metal music is generally
stronger than classical music [2]. Thus, long-term lis-
Seed regions Connected tening to heavy metal music may increase the activity of
of interest region Number
(side) (side) x y z of voxels Peak t value PreCG, which may be another reason why the fALFF of
PreCG in HMML is higher than CML. PCL is a part of
HMML > CML
MOG (left) MOG (left) − 33 − 84 18 127 3.7863 the primary motor area whose activation is associated
SPG (right) 30 − 63 57 692 5.4597 with the movements of the leg and the foot [15], and
SPG (left) − 21 − 63 45 138 3.4064
PCL (left) PoCG (left) − 36 − 30 72 119 3.4241
MOG plays an important role in action judgment [16].
HMML < CML Compared with CML, HMML tend to show varying
SFGmed MOG (left) − 39 − 69 33 170 − 3.7743 degrees of risk-taking behaviors such as drug use and
(left)
ANG (right) 45 − 63 39 96 − 3.1311 suicidality and the phenomenon of hyperactivity occurs
HIC (left) − 30 − 15 − 12 91 − 3.8649 [4,5]. We speculated that higher fALFF in PCL and
MTG (left) − 57 − 27 − 15 87 − 3.5517
MTG (right) 57 − 27 − 12 200 − 3.7568
MOG may lead to impulsive behaviors and hyperactivity
PreCG CER-3 9 − 39 − 21 127 − 3.7338 in HMML compared with CML.
(right) (right)
CER-6 (left) −9 − 60 − 24 99 − 3.8407 Additional alteration was also found in the left SFGmed.
PCL (right) ITG (right) 45 − 51 − 24 90 − 3.7806
PCL (left) PreCG (left) − 54 3 21 130 −4.8744
The Mozart effect shows that classical music can improve
the cognitive performance of the listeners and increase
ANG, angular gyrus; CER-3, cerebellum-3; CER-6, cerebellum-6; HIC, hippo- the activation of the corresponding brain areas [7],
campus; HMML < CML, the FC of HMML is significantly lower than CML;
HMML > CML, the FC of HMML is significantly higher than CML; ITG, inferior whereas SFGmed is in charge of individual cognitive
temporal gyrus; MTG, middle temporal gyrus; PoCG, postcentral gyrus; PreCG, control [17]. This may partly explain the lower fALFF of
precentral gyrus; SPG, superior parietal gyrus.
SFGmed in HMML compared with CML. In addition,
HMML are heavily influenced by violent lyrics and
was significantly stronger than that of CML. PreCG is intense rhythms, which have been related to behavior
mainly responsible for the movement of the tongue [14]. including the lack of cognitive control in behavioral dis-
Compared with CML, HMML are more willing to sing orders [5] compared with CML. Our finding of lower
and the movement of the tongue will change [3], which fALFF in SFGmed may contribute toward the lower
may affect the PreCG, which may be one reason why the ability of cognitive control in HMML compared
fALFF of PreCG in HMML is higher than CML. In with CML.

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The functional features of the brain can be described as
functional segregation and functional integration [11].
Altered RSFC were also found in widespread brain
regions apart from changes in low-frequency oscillation in
the present study. The altered RSFC and fALFF indi-
cate that the local characteristics of the several brain areas
in HMML may change, further enriching the neurolo-
gical models for HMML.
In our study, reduced FC of the left SFGmed was found in
the left MOG, right ANG, left HIC, and bilateral MTG,
and increased FC of left MOG was found in the bilateral
SPG and the other part of left MOG. MOG, ANG, and
HIC are part of the DMN [18]. The anterior part of the
DMN includes SFG, MTG, and SPG [19]. Altered FC of
DMN was one of our findings. As described, SFGmed has
been associated with individual cognitive control [17] and
MOG has been associated with action judgment [16].
Several functional neuroimaging studies had suggested
the strong involvement of bilateral ANG in the theory-of-
mind, which is an index of social cognition [20], HIC
contributes toward anxiety [11] and MTG is responsible
for the cognition of the sentence [21]. All of these regions
are associated with the function of cognition and emo-
tion. We speculated that the lower FC in DMN is asso-
ciated with the failure of integration between cognition
and emotion, and may result in negative impact related to
stress such as sleep disorders, sadness, and exhaustion in
HMML compared with CML [2,13].
The functional compensation effect assumes that increased
FC in particular brain regions may serve as a compensatory
mechanism [22]. Our finding of increased connectivity
between left MOG and bilateral SPG as well as left MOG
itself in DMN may be a compensation for the decreases in
the DMN. In this case, the DMN may be involved in
transforming a deficient neural loop into a relatively intact
neural loop.
The postcentral gyrus and PreCG are the core brain areas
of the sensorimotor network and sensorimotor network
are associated with action execution as well as somatic
sensation [23]. PCL represents the movements of the leg
and foot [15]. Both PCL and the sensorimotor network
are associated with similar functions. The particular FC
between PCL and the sensorimotor network in our
findings indicates that the sensory and motor functions in
HMML may change compared with CML, which may
contribute toward higher sensation seeking and more
risky behaviors in HMML than CML [4,5]. ITG is
involved in cognitive processing [24]. Research has
shown that the functional connection of the brain can
reflect the structural connection of the brain [25],
decreased FC between PCL and ITG suggests that the
neurobiological loop of the two brain regions may be
changed; in this condition, individuals cannot carry out
cognitive processing on their own behaviors, which may
explain why HMML are more inclined to take
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Altered FC in HMML Sun et al. 5
provocative actions to resolve hostility and antagonism
compared with CML [5,7].
Several issues should be considered further. First, in this
study, we had relatively small sample sizes, which limits
our statistical power. Second, our findings provide only a
basic neural exploration for HMML. Multimodel analysis
may increase the reliability of this study. Third, to enrich
the diversity of research, future work could include other
types of music lovers. Fourth, It cannot be shown directly
that the brain changes are connected to behavioral changes.
Fifth, it is difficult to specifically track cerebellar granule
cells with the current technology now; thus, the function of
the cerebellum is still being explored [26]. Thus, we did
not discuss the functional changes in the cerebellum.
Conclusion
This is the first study to explore the neural mechanism of
HMML. We found that HMML have altered spontaneous
regional neural activity involving the function of move-
ment and cognition during rest compared with CML.
Seed-based RSFC differences between HMML and CML
were also found in the related networks such as the DMN
and the sensorimotor network. These may be related to the
disorders of behavioral and emotional cognition in HMML
compared with CML and may potentially represent a
neural mechanism underlying HMML.
Acknowledgements
This research is supported by the MOE (Ministry of
Education in China) Project of Humanities and Social
Sciences (17YJA190011), the Humanities and Social Science
Special Project of the educational department in Liaoning
Province (ZJ2015034), and The ‘13th Five-year Plan’ Project
of education science in Liaoning Province (JG16CB343).
Conflicts of interest
There are no conflicts of interest.
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