Hearing Research 373 (2019) 32e47

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Hearing Research
journal homepage: www.elsevier.com/locate/heares

Research Paper

The power of language: Functional brain network topology of deaf and

hearing in relation to sign language experience
Michel R.T. Sinke a, *, Jan W. Buitenhuis a, Frank van der Maas c, d, Job Nwiboko d,
Rick M. Dijkhuizen a, Eric van Diessen b, 1, Willem M. Otte a, b, 1
a
Biomedical MR Imaging and Spectroscopy Group, Center for Image Sciences, University Medical Center Utrecht and Utrecht University, Utrecht, the
Netherlands
b
Department of Pediatric Neurology, Brain Center Rudolf Magnus, University Medical Center Utrecht, Utrecht, the Netherlands
c ~o Baseadana Comunidade (RBC) Effata, Bissora
Reabilitaça ~, Oio, Guinea-Bissau
d
CBR Effata, Omorodu Iseke Ebonyi LGA, Ebonyi State, Nigeria

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

Article history: Prolonged auditory sensory deprivation leads to brain reorganization. This is indicated by functional
Received 31 May 2018 enhancement in remaining sensory systems and known as cross-modal plasticity. In this study we
Received in revised form investigated differences in functional brain network topology between deaf and hearing individuals. We
8 December 2018
also studied altered functional network responses between deaf and hearing individuals with a recording
Accepted 12 December 2018
Available online 15 December 2018
paradigm containing an eyes-closed and eyes-open condition.
Electroencephalography activity was recorded in a group of sign language-trained deaf (N ¼ 71) and
hearing people (N ¼ 122) living in rural Africa. Functional brain networks were constructed from the
Keywords:
Cross-modal plasticity
functional connectivity between fourteen electrodes distributed over the scalp. Functional connectivity
Deafness was quantified with the phase lag index based on bandpass filtered epochs of brain signal. We studied
ASL the functional connectivity between the auditory, somatosensory and visual cortex and performed
EEG whole-brain minimum spanning tree analysis to capture network backbone characteristics.
Functional networks Functional connectivity between different regions involved in sensory information processing tended
Minimum spanning tree to be stronger in deaf people during the eyes-closed condition in both the alpha and beta frequency
band. Furthermore, we found differences in functional backbone topology between deaf and hearing
individuals. The backbone topology altered during transition from the eyes-closed to eyes-open condi-
tion irrespective of deafness, but was more pronounced in deaf individuals. The transition of backbone
strength was different between individuals with congenital, pre-lingual or post-lingual deafness. Func-
tional backbone characteristics correlated with the experience of sign language. Overall, our study
revealed more insights in functional network reorganization caused by auditory deprivation and cross-
modal plasticity. It further supports the idea of a brain plasticity potential in deaf and hearing people. The
association between network organization and acquired sign language experience reflects the ability of
ongoing brain adaptation in people with hearing disabilities.
© 2018 Elsevier B.V. All rights reserved.

1. Introduction

Impairment or loss of hearing interferes with many activities in

Abbreviations: ASL, American Sign Language; CBR, Community-Based Rehabil-
itation; EEG, Electroencephalography; MRI, Magnetic Resonance Imaging; MST,
Minimum Spanning Tree
* Corresponding author. Biomedical MR Imaging and Spectroscopy Group, Center
for Image Sciences, University Medical Center Utrecht, Yalelaan 2, 3584 CM,
Utrecht, the Netherlands.
E-mail address: m.r.t.sinke@umcutrecht.nl (M.R.T. Sinke).
1
Shared last author.
daily life, specifically limiting communication with others. This
could easily lead to social isolation. The prevalence of this serious
disability is greatest in middle- and low-income countries (Durkin,
2002; Stevens et al., 2013; WHO, 2014). While in the United States
about two out of every 1000 children are born with disabling
hearing loss (Vohr, 2003), this number is considerably higher in
Sub-Saharan Africa where about two percent of the children is born

https://doi.org/10.1016/j.heares.2018.12.006
0378-5955/© 2018 Elsevier B.V. All rights reserved.
 M.R.T. Sinke et al. / Hearing Research 373 (2019) 32e47
with disabling hearing loss (WHO, 2012). Many of these children
have profound hearing loss resulting in absolute deafness. Infec-
tious diseases are a major cause of deafness in these regions
(Mulwafu et al., 2016).
Prolonged periods of sensory deprivation often leads to exten-
sive reorganization in the brain. This reorganization is caused by
compensatory and cross-modal plasticity (Bavelier and Neville,
2002; Merabet and Pascual-Leone, 2010; Ptito et al., 2001). Brain
reorganization after auditory deprivation has been mapped by
different functional neuroimaging modalities, such as positron
emission tomography, functional near-infrared spectroscopy,
functional magnetic resonance imaging (fMRI) and electroen-
cephalography (EEG) (Buckley and Tobey, 2011; Dewey and Hartley,
2015; Doucet et al., 2006; Finney et al., 2001; Yoshida et al., 2011).
Consequently, deaf are better than hearing people at detecting vi-
sual stimuli (e.g. Almeida et al., 2015; Bavelier et al., 2006, 2000;
Bosworth and Dobkins, 2002; Brozinsky and Bavelier, 2004; Dye
et al., 2007; Finney and Dobkins, 2001; Hauser et al., 2007;
Neville and Lawson, 1987a, 1987b) and show increased tactile
sensitivity as well (Auer et al., 2010; Lev€anen and Hamdorf, 2001;
Meredith and Lomber, 2011). Accordingly, the auditory cortex of
deaf is found to be responsive to non-auditory stimuli (e.g. Almeida
et al., 2015; Auer et al., 2010; Buckley and Tobey, 2011; Doucet et al.,
2006; Finney et al., 2001; Karns et al., 2012; Meredith and Lomber,
2011; Neville and Lawson, 1987b; Scott et al., 2014). For example
fMRI and positron emission tomography studies showed that the
cortical auditory and association areas of deaf people are respon-
sive to visual motion stimuli. These regions include the planum
temporale (Petitto, 2000; Sadato et al., 2005; Shiell et al., 2016) and
primary auditory cortices, like posterior superior temporal gyrus
(Almeida et al., 2015; Ding et al., 2015; Karns et al., 2012; Li et al.,
2015) and Heschl's gyrus (Karns et al., 2012; Meyer et al., 2007;
Scott et al., 2014; Smith et al., 2011). Cortical reorganization
(Campbell and Sharma, 2014, 2013) and responsive auditory cortex
to visual stimuli in deaf have also been described with functional
brain data recorded with EEG (e.g. Buckley and Tobey, 2011; Doucet
et al., 2006; Neville and Lawson, 1987b, 1987a). While this reor-
ganization occurs inevitably as a result of profound deafness, cross-
modal plasticity also strongly relates to the acquisition and use of
sign language (Meyer et al., 2007; Pe nicaud et al., 2013). Further-
more, the extent of cross-modal plasticity is dependent on the age
of onset and the duration of deafness (Brotherton et al., 2016; Li
et al., 2013). Although stimuli- and task-based approaches have
provided valuable insights in cross-modal plasticity, they do not
capture the mutual dependency of different functional brain re-
gions as well as the integrative nature of the human brain (Hackett,
2012; Stam and van Straaten, 2012).
The human brain forms a complex integrative network, which
consists of spatially distributed, but functionally connected regions
that continuously interact with each other (Bassett et al., 2018;
Bassett and Sporns, 2017; Bullmore et al., 2009; Bullmore and
Sporns, 2009; van den Heuvel and Hulshoff Pol, 2010). As such,
functional brain connectivity and reorganization can be better
understood when these processes are not studied in isolation. Brain
network analysis explicitly takes the interdependencies between
functionally connected regions into account as it shifts emphasis
from specific locational changes to global topological alternations.
The functional network topology, and potential reorganization
therein, can be effectively mapped with several network metrics
(Bassett et al., 2018; Bassett and Sporns, 2017; Bullmore and Sporns,
2012). Classical graph analysis describes the human brain as a
collection of nodes (i.e. functional brain regions such as the audi-
tory or visual cortex) and edges (i.e. the functional connections
between regions), and provides quantitative information on the
33
topological properties of these networks (Bullmore and Sporns,
2009; Heuvel et al., 2012; Rubinov and Sporns, 2010). The healthy
human brain has been characterized as a complex network that
effectively combines global and efficient integration with segrega-
tion of functionally specialized brain regions (Bullmore and Sporns,
2012). This unique topology with high integration and segregation
is defined as a small-world network organization (Bullmore and
Sporns, 2009; Watts and Strogatz, 1998). Deviation from a small-
world organization has been related to many neurological and
psychiatric disorders (Bassett and Bullmore, 2009; Stam, 2014).
Surprisingly few studies have used network analysis to examine
reorganization of brain networks in deaf individuals. Pre-lingual
deaf adults showed increased network clustering and nodal effi-
ciency compared to controls, whereas brain networks from post-
lingual deaf adults did not differ from controls (Kim et al., 2014).
This indicates that auditory experience might affect the
morphology of brain networks in deaf adults. In another study
increased functional connectivity was found between regions
within the limbic system, a system involved in sensory information
processing (Li et al., 2016). Functional network hubs shifted in the
deaf subjects. The small-worldness did not differ between pre-
lingual deaf as compared to hearing controls (Li et al., 2016). Yet
another study found increased functional connectivity in brain
networks in deaf during rest, which was also shown to be related to
sign language experience (Malaia et al., 2014).
Resting-state functional connectivity measurements can be
performed in an eyes-open or eyes-closed condition. Opening and
closing the eyes are very basic attention-directing behaviors. Eyes-
open is related to ‘exteroceptive’ awareness, characterized by more
specialized overt attention and oculomotor activity, whereas eyes-
closed is related to ‘interoceptive’ awareness, characterized by
more integrative multisensory activity and imagination (Xu et al.,
2014). Eyes-open and eyes-closed conditions relate to different
brain states (Marx et al., 2004, 2003; Zhang et al., 2015) and to-
pological organizations of functional networks (Go mez-Ramírez
et al., 2017; Tan et al., 2013; Xu et al., 2014). This is even so in
darkness (Hüfner et al., 2009, 2008). In EEG-studies functional
networks showed increased global efficiency and decreased clus-
tering during the eyes-open state, specifically in the alpha band,
which might be due to alpha desynchronization, i.e. a reduction in
the number of functional connections in the eyes-open state
(Go mez-Ramírez et al., 2017; Miraglia et al., 2016; Tan et al., 2013).
Despite the usefulness of classical network analysis in capturing
brain network reorganization, it has some intrinsic limitations. The
classical network analysis is particularly limited in comparing inter-
subject networks with different network densities (van Wijk et al.,
2010). The network density is defined as the number of connections
relative to the potential number of connections. Commonly used
network metrics, such as the clustering coefficient e used to
measure network segregation e and average path length e used to
measure network integration e are highly affected by the number
of connections within a network (Stam et al., 2014; van Wijk et al.,
2010). Therefore, comparing healthy and affected (or reorganized)
brain networks, in a situation of cross-modal plasticity or alpha
desynchronization, might yield biased results (Tewarie et al., 2015;
van Wijk et al., 2010; Zalesky et al., 2010). Solutions have been
provided. A promising alternative network characterization
approach not limited by the network density is the assessment of
the network backbone. Network backbones are robustly and effi-
ciently operationalized by the minimum spanning tree (MST) (Stam
et al., 2014; Tewarie et al., 2015). An increasing number of studies
have shown the usefulness of MSTs in capturing subtle network
changes in brain development and ageing (Boersma et al., 2013;
Otte et al., 2015; Smit et al., 2016; Vourkas et al., 2014). MSTs have
34 M.R.T. Sinke et al. / Hearing Research 373 (2019) 32e47

also been useful in characterizing multiple sclerosis, Alzheimer's
disease and epilepsy (Engels et al., 2015; Tewarie et al., 2014; van
Diessen et al., 2016, 2014; Sinke et al., 2018).
The present study therefore investigated the effects of prolonged
periods of deafness on the functional brain network backbone to-
pology. To that aim we acquired resting-state EEGs in deaf and hearing
individuals. Data were recorded within a unique homogeneous pop-
ulation living in a representative rural region in sub-Saharan Africa. In
this region deafness is a common disability and cochlear implants are
not available. We hypothesized stronger functional connectivity (i.e.
more integration) between auditory cortex and other sensory (i.e.
visual and somatosensory) cortices in deaf people, due to cross-modal
plasticity. Hence, we also expected differences in functional network
backbone topology between controls and deaf. Given the expected
cross-modal plasticity as well as auditory sensitivity to visual stimuli,
we further expected larger shifts in functional network topology be-
tween eyes-open (i.e. ‘exteroceptive’ awareness) and eyes-closed (i.e.
‘interoceptive’ awareness) in deaf. We also explored whether (shifts
in) functional backbone topologies were different between congen-
ital, pre-lingual and post-lingual deaf. Lastly, we anticipated a rela-
tionship between functional backbone characteristics and years of
American Sign Language (ASL) experience.
2. Methods
2.1. Study setting and ethics
The study pipeline as described below is schematically visual-
ized in Fig. 1. Our study was conducted at two inclusive primary
schools and one inclusive secondary school, located in two separate
rural villages in Ebonyi State, southeast Nigeria. The schools are
part of a Community-Based Rehabilitation (CBR) program, which
implies that all students has to live in surrounding villages and
communities, aiming for a full integration within the community.
Inclusive education means that both students with and without
disabilities are allowed to participate in regular classes, and are
supported to learn, contribute and participate in all aspects of the
educational program. This inclusive educational approach is a po-
tential strategy to reduce the individual as well as shared burden of
disability (Eleweke and Rodda, 2002; Pfo €rtner, 2014). The number
of students with and without disabilities enrolled in the schools is
approximately equal. Since the integration of deaf people forms one
of the main focuses of this CBR program, the majority of students
with disability are deaf. Standard ASL forms an integral part of the
educational program for more than twenty years. This sign lan-
guage has to be learned by all teachers and students, both the
hearing and the deaf. Besides, deaf students also receive speech
therapy. All lessons are taught in English and if a teacher does not
yet sufficiently master sign language there will be an interpreter
who translates spoken language into sign language for deaf stu-
dents and vice versa. The CBR program leads to an increasing
amount of people within the community that speak sign language.
This implies a more regular use, development and integration of
sign language by deaf students in their daily lives.
Our study was approved by the organizational boards (RBC/CBR
Effata), the local health ministry (Izzi, Local Government Area) and
the federal government (Ebonyi State House of Assembly, Abakaliki
[7-11-2016]) in Nigeria. The study protocol was clearly explained to
all students in class before they were asked to participate in the EEG
recordings. Written informed consent was obtained from adult
participants and caretakers of students below eighteen years. In
addition, we also obtained assent from the students below eighteen

Fig. 1. Schematic overview of the study pipeline. Resting-state electroencephalography (EEG) was acquired for 5 min with wireless headsets in deaf and controls. The sensor
locations corresponding to the fourteen channels are shown in orange; the reference sensors are shown in blue. The first minute of data acquisition, required for acclimatization,
was discarded, yielding two blocks of recordings e 2 min with eyes-closed and 2 min with eyes-open. The order of the eyes condition (‘open’ and ‘closed’) was alternated. Sub-
sequently, functional networks were constructed from ten-second epochs from distinct frequency bands (i.e. delta, theta, alpha, beta and gamma), and functional network backbone
metrics were determined for all bands. These network backbone metrics were related to years of sign language experience. Main effects between groups (i.e. deaf and control) and
conditions (i.e. eyes-open and eyes-closed) as well as interaction effects between group and condition were assessed using model selection within a Bayesian framework.
 M.R.T. Sinke et al. / Hearing Research 373 (2019) 32e47
years.
2.2. Participants
Table 1 shows the demographic information of all participants.
We included 193 participants between ten and 43 years old (mean
age of 18.5 (standard deviation 6.0); gender: 103 male, 90 female),
both students and teachers. Sign language experience of partici-
pants varied between zero and seventeen years at the time of
recording. We selected both hearing (n ¼ 122) and deaf (n ¼ 71)
participants. The pre-lingual deaf participants were all capable of
lip reading.
2.3. Data acquisition
We used a sixteen sensor/fourteen channel EEG monitor
configured to sample at 128 Hz with a 16-bit resolution (EMOTIV
Inc, San Francisco, USA), which has been validated and successfully
applied in several studies (Aspinall et al., 2013; Badcock et al., 2015,
2013; McMahan et al., 2015; Prause et al., 2016; Yu and Sim, 2016).
This wireless headset can be connected to a computer via Bluetooth
and is an invaluable tool to collect EEG signals from participants in
rural or resource-limited areas, where access to a standard EEG
system is often impossible or burdensome. Two sensors were
preserved for reference and grounding: the ‘common mode sense’
(CMS; located at P3) sensor was used as the active reference for
absolute referencing. The ‘driven right leg’ (DRL; located at P4)
sensor was used for feedback noise cancelation. The electrodes
were located at anterofrontal (AF3, AF4, F3, F4, F7, F8), frontocentral
(FC5, FC6), occipital (O1, O2), parietal (P7, P8) and temporal sites
(T7, T8), according to the International 10e20 system. Signal quality
scores are recorded for each electrode with a range from one to five
(no units), with five as best quality score.
Participants were seated in a comfortable chair in a sound-
attenuated room where the Emotiv headset was placed. Partici-
pants were instructed to keep their eyes closed for the first 3 min and
open in the next 2 min, or vice versa. The order of the condition
sequence was assigned alternatingly, so that half of the participants
started in the eyes-open condition whereas the other half of the
participants started in the eyes-closed condition. The researcher
kept a log on deviations from the protocol, or unusual events in the
environment, that may affect the experiment. Example recordings
are shown in Fig. 2. As an EEG contains a multitude of overlapping
signal waves with distinct amplitudes and frequencies we separated
the signal into the five most common frequency ranges. The EEG
signals were band-pass filtered into the delta (0.5e4 Hz), theta
(4e8 Hz), alpha (8e16 Hz), beta (16e32 Hz) and gamma (32e64 Hz)
frequency bands. Examples are shown in Suppl. Figure 1 and 2.
2.4. Data cleaning and window selection
Time segments were removed from the recordings if i) the
research log indicated a deviation from the protocol, ii) the EEG
Table 1
Participant demographics.
Deaf
congenital pre-lingual
N total 42 22
Sex 13 males/29 females 16 males/6 females
Age (years) 18 ± 5 (range 10e30) 19.6 ± 4.4 (range 10e26)
First eyes condition 25 open/17 closed 11 open/11 closed
Sign language experience (years) 8.9 ± 3.5 (range 2e16) 8.9 ± 3.4 (range 1e16)
35
signal quality score was below four for any of the channels, and iii)
if the absolute deviation of the gyroscope signals relative to the
gyroscope signal median exceeded five times the standard devia-
tion. This threshold was based on visual data inspection (See
example in Suppl. Figure 3). Subsequently, the cleaned and filtered
time-series were cut into ten-second epochs. Functional connec-
tivity measurements as well as multiple network backbone metrics
has been shown to stabilize within recordings if the epoch length is
6 s or longer (Fraschini et al., 2016). In addition, multiple epochs per
subject further increase the stability of network backbone metrics
(van Diessen et al., 2015). Therefore we used multiple epochs
combined with this conservative ten-second length.
2.5. Functional connectivity
For each epoch a functional network was constructed, which can
either be visualized as a connectivity matrix or a network graph
(Fig. 3). Recorded time-series within each epoch were used to
determine functional connectivity (i.e. forming the ‘edges’ in a
network) between different electrodes capturing neuronal signals
from underlying brain areas (i.e. forming the ‘nodes’ in a network).
Functional connectivity was computed and quantified with the
phase lag index. This is a measure of the asymmetry of the distri-
bution of instantaneous phase differences between two time series
and scales between zero and one (Pillai and Sperling, 2006). It is
relative resistant to the influence of common sources, including
volume conduction and active reference electrodes. An index of
zero indicates no phase coupling (i.e. no functional connectivity)
between time series, or coupling with a phase difference centered
on zero ± p radians. A non-zero index indicates the presence of
phase coupling (i.e. functional connectivity), where higher values
indicate stronger functional connections. A more mathematical
description of computing the phase lag index can be found else-
where (Stam et al., 2007).
2.6. Functional connectivity strength between auditory, visual and
somatosensory cortices
Since we expected remodeling of the auditory cortex in deaf
people, reflected as enhanced functional connectivity between the
auditory and sensory cortices, we characterized in both groups the
average phase lag index between sets of electrodes. These sets were
the temporal electrodes T7/T8, covering the auditory cortex, the
parietal electrodes P7/P8, covering the somatosensory cortex, and
the occipital electrodes O1/O2, covering the visual cortex, in eyes-
open and eyes-closed conditions.
2.7. Minimum spanning tree analysis
For each functional network a minimum spanning tree was
calculated from the connectivity graph G by applying Kruskal's al-
gorithm (Kruskal, 1956) (Fig. 3B). This tree captures the network's
backbone and is defined as a subset of the network nodes (forming
Hearing controls
post-lingual sign language experience no sign language experience
7 65 57
7 males 31 males/34 females 36 males/21 females
16.6 ± 4.1 (range 10e22) 17.3 ± 5.6 (range 12e39) 20 ± 7.6 (range 12e43)
2 open/5 closed 30 open/35 closed 28 open/29 closed
8.1 ± 3.7 (range 3e15) 2.3 ± 2.6 (range 1e17) e
36 M.R.T. Sinke et al. / Hearing Research 373 (2019) 32e47

Fig. 2. Raw EEG time-series of one participant. The visualized time-series were acquired from a deaf male (22 years old). Vertical grey lines indicate the initial acclimatization
period, the first 2 min (i.e. eyes-closed in this subject) and the second 2 min (i.e. eyes-open). The y-scaling is arbitrary. Labels of the fourteen channels are shown on top of the time-
series. Abbreviations of these channel labels are explained in the main text.

the original weighted graph G) that connects all the nodes and does
not contain cycles or loops (Jackson and Read, 2010). Mathemati-
cally, a minimum spanning tree T minimizes the sum of the costs of
its edges, over the set of all possible spanning trees on G (Hidalgo
et al., 2007). Since we are interested in the strongest functional
connections (i.e. the network backbone), we first inverted the edge
weights of the functional network before determining the MSTs.
Subsequently, several MST metrics were calculated at the nodal or
network level. Although some metrics are determined at the nodal
level (e.g. degree or betweenness centrality), they can still be used
to summarize e or indicate e specific properties for the backbone
as a whole. For example with the ‘maximum degree’ or the ‘average
 M.R.T. Sinke et al. / Hearing Research 373 (2019) 32e47 37

Fig. 3. Schematic overview of functional network and minimum spanning tree (MST) construction. (A) EEG epochs were measured from 14 electrodes, represented as network
nodes. The electrodes were placed across the left (L, yellow) and right (R, orange) hemisphere (top), two electrodes served as references (blue). The recorded time-series (bottom)
were used to determine functional connectivity between brain regions. (B) The determined functional connections can either be depicted as a weighted functional network graph
(top) or an adjacency matrix (bottom) where columns and rows represent nodes and colored squares indicate functional connectivity between nodes. The color indicate functional
connectivity strength (i.e. darker ¼ stronger). (C) The weighted functional network can be used to determine the minimal spanning tree (MST), which only includes the strongest
connections, forming a functional network backbone. This determined MST can also be depicted as a network graph (top) or an adjacency matrix (bottom). Subsequently, MST
metrics, such as leaf fraction and diameter, can be determined. Abbreviations of channel labels are explained in the main text.

strength’, where higher values may indicate higher overall con- 1

nectivity. The following MST metrics were calculated at nodal or
network level:
i) Maximum node degree (nodal): every tree was summarized
by taking the maximum node degree: Smax, the node with
the maximum number of connections.
ii) Leaf number (Nleaf) (network): the number of nodes of the tree
with exactly one connection to any other node (with
maximum degree ¼ 1). A higher leaf number is related to
increased global efficiency and integration (Stam et al., 2014;
Tewarie et al., 2015).
iii) Diameter (d) (network): the largest distance between any two
nodes in a tree, which has a lower bound of two and an upper
bound of m ¼ N e 1. The largest possible diameter will
decrease with increasing leaf number (Boersma et al., 2013;
Stam et al., 2014; Tewarie et al., 2015).
iv) Eccentricity (network): the shortest path length between a
tree node I and any other node from the tree. Eccentricity
decreases when nodes become more central in the tree.
v) Radius (nodal): the smallest node eccentricity in the tree. The
lower the eccentricity, the more central a node in a tree.
vi) Strength (nodal): the tree node strength is a summation of all
nodal connection weights (Hagmann et al., 2010; Rubinov
and Sporns, 2010).
vii) Maximum betweenness centrality (BCmax): a network hub
metric which relies on the identification of the number of
shortest paths that pass through a node (Rubinov and Sporns,
2010). The more the passages, the higher the betweenness-
centrality (i.e. hubness), which is defined by
Pn gjk ðiÞ
bci ¼ ðn1Þðn2Þ jsk;ksi;jsi gjk where gjk is the shortest path
between two nodes and gjk(i) is the number of node paths
that actually pass through i. We summarized the tree by
taking the maximum betweenness centrality.
viii) Closeness centrality (nodal): the inverse of the sum of all
distances to other nodes (Sabidussi, 1966).
2.8. Statistical analyses
All statistical analyses were performed within a Bayesian
framework. Differences between groups, eye conditions and in-
teractions between groups and eye conditions were evaluated with
Bayes factors. Bayes factors were extracted from Bayesian model
comparisons. This was done for all frequency bands separately. We
determined the model likelihood of a null model without an
interaction effect of group and condition as well as the likelihood of
an alternative model with an interaction effect of group and con-
dition for functional connectivity strength. This was done for all
MST metrics and for their potential relationship with sign language
experience. Bayes factors give the ratio of model likelihoods, indi-
cating which model is supported by the data. For example, if e
given the data e a null model (M0) without an effect of condition
(i.e. eyes-open versus eyes-closed) on functional connectivity
strength has a very low probability, whereas an alternative model
(M1) with an effect of condition on functional connectivity strength
has a high probability, this would yield a high Bayes factor (e.g. 50).
This may be interpreted as very strong evidence for M1 as M1 is fifty
times more likely than M0 in explaining the data. Table 2 gives an
overview of Bayes factors and their interpretation (Raftery, 1995).
38 M.R.T. Sinke et al. / Hearing Research 373 (2019) 32e47

Table 2
Bayes factors and their interpretations, based on (Raftery, 1995). M0: the baseline model without interaction term, M1: the alternative model with interaction term. In the
subsequent tables the Bayes factors for M1 are reported only.

Bayes factor Interpretation

> 100 Extreme evidence for M1

30 e 100 Very strong evidence for M1
10 e 30 Strong evidence for M1
3 e 10 Moderate evidence for M1
1 e 3 Anecdotal evidence for M1
1 No evidence
1/3 e 1 Anecdotal evidence for M0
1/10 e 1/3 Moderate evidence for M0
1/30 e 1/10 Strong evidence for M0
1/100 e 1/30 Very strong evidence for M0
< 1/100 Extreme evidence for M0

Since sex (Boersma et al., 2011) and age (Smit et al., 2012) influence
functional network topologies, we tested whether models with
strong evidence were affected by sex- and age.
All network analyses, statistical modeling and visualizations
were performed in R (http://www.r-project.org/) using the pack-
ages igraph, BayesFactor, reshape2, dplyr and ggplot2. Epoch data
and scripts are freely available at the Open Science Framework in
anonymized form (Otte et al., 2018b) and the GitHub repository
(Otte et al., 2018a).
3. Results
3.1. Functional connectivity strength between auditory, visual and
somatosensory cortices
Fig. 4 and Suppl. Figure 6 show the functional connectivity
strength between the occipital cortex and the parietal cortex for the
different frequency bands. Occipital-parietal functional connectiv-
ity strength was lower in the eyes-open condition compared to the
eyes-closed condition in the theta, alpha and beta frequency bands.
After transition from eyes-closed to eyes-open, differences in
functional connectivity strength were most pronounced in the
alpha frequency band with a significant reduction of 54.9% (95%
confidence interval (CI): -68.2% to 41.6%) in controls and an even
larger reduction of 88.0% (95% CI: -112% to 63.6% in deaf (Fig. 4B).
A decrease in functional connectivity strength from eyes-closed to
eyes-open was also present in the beta frequency band, with a
reduction of 27.7% (95% CI: -37.3 to 18.0) in controls and 36.1%
(95% CI: -49.2 to 23.0) in deaf. These reductions in functional
connectivity strength in the alpha and beta band were supported
by Bayes factors of respectively >100 (i.e. labeled as ‘extreme evi-
dence’) and 2.6 (‘moderate evidence’) (Table 3).
Similar trends were seen for functional connectivity strength be-
tween the occipital cortex and temporal cortex (Suppl. Figure 4 and
Suppl. Figure 7) as well as between the parietal cortex and tempo-
ral cortex (Suppl. Figure 5 and Suppl. Figure 8). However, for those
connections no significant differences were found between controls
and deaf in functional connectivity reduction from eyes-open to eyes-
closed, as indicated by Bayes factors of <1 (Suppl. Table 1 and
Suppl. Table 2). The parietal-temporal delta-band connectivity
strength was significantly more reduced from eyes-closed to eyes-
open in deaf, while no reduction was found in controls

Fig. 4. Functional connectivity strength between the occipital cortex and the parietal cortex. (A) The average functional connectivity, quantified with the phase lag index,
between O1/O2 and P7/P8 (y-axis) is shown for eyes-open and eyes-closed conditions (x-axis) and all frequency bands (top) in controls and deaf people. (B) The delta functional
connectivity between eyes-open en eyes-closed is plotted as percentage change relative to the eyes-open functional connectivity values for each frequency band, based on the data
shown in the left panel: D in % ¼ 100  (closed e open)/open.
 M.R.T. Sinke et al. / Hearing Research 373 (2019) 32e47 39

Table 3 Furthermore, for the alpha band there was moderate to strong
Bayes factors of the interaction effect between condition (i.e. evidence for a larger increase in both betweenness and closeness
eyes-closed and eyes-open) and group (i.e. deaf and controls) in
relation to occipital-parietal functional connectivity strength
centrality in deaf. Anecdotal evidence was found for larger shifts in
(per frequency band). leaf number and diameter e in the alpha band e as well as in
closeness centrality e in the beta band e in deaf (Table 4). All ev-
Frequency Bayes factor
idence was still present if age and sex were added to the models.
Delta (0.5e4 Hz) 0.04 We found that the decrease in average connectivity strength
Theta (4e8 Hz) 0.07
(Suppl. Figure 9) and increase in closeness centrality
Alpha (8e16 Hz) >100 V
Beta (16e32 Hz) 2.39 I (Suppl. Figure 10) from eyes-closed to eyes-open was different
Gamma (32e64 Hz) 0.04 across the congenital, pre-lingual and post-lingual deafness types.
I
Anecdotal evidence, V
Extreme evidence for interaction.
This is supported by the Bayes factors in Suppl. Table 3.

3.4. Relation between backbone characteristics and American Sign

(Suppl. Figure 5), as indicated by the high Bayes factor (Suppl. Table 2).
All evidence was still present if age and sex were added to the models.
3.2. Functional backbone differences between eyes-open and eyes-
closed conditions
Transition from eyes-closed to eyes-open initiated visible
changes in functional network topology, as indicated by changes in
backbone metrics. The most notable effects were found in the alpha
and beta bands (Table 4), which are shown in Fig. 5. Overall the
backbone leaf number, the average and maximum strength as well
as the kappa were lower in the eyes-open condition as compared to
the eyes-closed condition. In contrast, the diameter, eccentricity,
radius as well as the median and maximum closeness centrality
were higher in the eyes-open condition compared to the eyes-
closed condition. Interestingly, in contrast to deaf, controls did
not show a transition effect on some network metrics in the alpha
band (i.e. leaf number, eccentricity, radius and diameter).
3.3. Larger functional backbone modifications in deaf
Language
We investigated the relationship between sign language expe-
rience and functional backbone characteristics. Initially, with no
distinction made between deaf and controls. Sign language expe-
rience was related to altered backbone characteristics in the delta,
theta and alpha band. The most pronounced effects were found in
the theta band (Table 5), which are visualized in Figs. 6 and 7. More
specifically, for the theta band an increase in ASL experience was
related to a higher average backbone connectivity strength and a
lower closeness centrality for the eyes-closed condition (Fig. 6).
Furthermore, strong evidence was found for a positive relationship
between sign language experience and higher backbone connec-
tivity strength for the delta band (Table 5). Fig. 7 shows the rela-
tionship between sign language experience and functional
backbone characteristics for deaf subjects only. Again most pro-
nounced effects were found for the theta band (Table 6) with a
positive relation between sign language experience and higher
average backbone connectivity strength. All associations were still
present if age and sex were added to the models.

Some functional backbone characteristics were different be- 4. Discussion

tween deaf and hearing controls (Fig. 5). In both the alpha and beta
band, functional backbone strength was stronger in the eyes-closed
condition and weaker in the eyes-open condition in deaf as
compared to hearing controls. In the alpha band the leaf number
was lower in deaf, whereas the diameter and radius were larger in
the eyes-open condition.
Several functional backbone characteristics showed larger shifts
in deaf than controls when comparing eyes-closed to eyes-open
(Fig. 5). For both the alpha and beta band, evidence was found for
a larger decrease in the average and maximum backbone connec-
tivity strength in deaf (as indicated by the Bayes factors in Table 4).
The present study used resting-state EEG to map functional
network backbone differences between deaf and hearing people.
We showed that transition from eyes-closed to eyes-open was
associated with changes in functional connectivity strength be-
tween occipital and parietal lobes as well as changes in functional
backbone topology. In both deaf and hearing, these changes
occurred especially in the alpha and beta frequency bands. More-
over, the difference in functional connectivity strength as well as in
functional backbone characteristics between eyes-closed to eyes-
open tended to be larger in deaf as compared to hearing controls.

Table 4
Bayes factors of the interaction effect between condition (i.e. eyes-closed and eyes-open) and group (i.e. deaf and controls) in relation to the network backbone metrics (shown
per frequency band).

MST-metric Delta band (0.5-4 Hz) Theta band (4e8 Hz) Alpha band (8e16 Hz) Beta band (16e32 Hz) Gamma band (32e64 Hz)

Strength (max) 0.09 0.05 >100 V 1.37 I 0.06

Strength (mean) 0.03 0.19 >100 V 57.82 IV
0.07
Degree (max) 0.04 0.06 0.27 0.06 0.09
BC (max) 0.02 0.06 0.08 0.06 0.06
BC (median) 0.06 0.06 4.63 II 0.06 0.14
CC (max) 0.04 0.27 26.64 III 1.59 I 0.09
CC (median) 0.04 0.26 93.37 IV 2.61 I 0.10
Leaf 0.07 0.06 2.31 I 0.08 0.09
Diameter 0.08 0.06 2.42 I 0.08 0.10
Eccentricity 0.07 0.06 0.39 0.07 0.08
Radius 0.08 0.05 0.16 0.06 0.06
Tree-hierarchy 0.06 0.05 0.73 0.14 0.11
Kappa 0.10 0.10 0.62 0.06 0.12
I II III IV V
BC ¼ betweenness centrality, CC ¼ closeness centrality, Anecdotal evidence, Moderate evidence, Strong evidence, Very strong evidence Extreme evidence for
interaction effect between group and condition.
40 M.R.T. Sinke et al. / Hearing Research 373 (2019) 32e47

Fig. 5. Network backbone comparisons between eyes-open and eyes-closed conditions for both deaf and controls. Functional network backbone characteristics in the alpha
band (8e16Hz) and beta band (16e32 Hz) (top), are shown for deaf (yellow) and controls (blue) for both the eyes-open and eyes-closed condition (x-axis) and indicated by the
following minimum spanning tree metrics (y-axis), (from top-left to bottom-right): diameter, maximum closeness centrality, median closeness centrality, leaf number, maximum
strength, mean strength, eccentricity, radius and kappa. Error bars represent the 95% confidence intervals.

4.1. Functional cortical remapping
We examined functional connectivity strength between sensory
regions involved in auditory, visual and somatosensory information
processing. With some evidence we can state that functional
connectivity appears stronger in deaf, specifically in the alpha and
beta bands. This might indicate increased integration between the
different sensory cortical regions in deaf. Our results are in agree-
ment with previous fMRI studies that also found increased audio-
visual connectivity in deaf (Bola et al., 2017; Li et al., 2016, 2013;
 M.R.T. Sinke et al. / Hearing Research 373 (2019) 32e47 41

Table 5
Bayes factors of the relationship between the network backbone metrics and sign language experience in all participants.

MST-metric Delta band (0.5-4 Hz) Theta band (4e8 Hz) Alpha band (8e16 Hz) Beta band (16e32 Hz) Gamma band (32e64 Hz)

Strength (max) 20.92 III 0.73 0.07 0.04 0.05

Strength (mean) >100 V >100 V 66.84 IV
0.09 0.09
Degree (max) 0.22 0.06 0.37 0.08 0.04
BC (max) 3.94 II 0.05 0.06 0.06 0.05
BC (median) 0.07 0.05 0.09 0.04 0.05
CC (max) 0.91 2.37 I 62.60 IV
0.05 0.18
CC (median) 11.80 III 52.06 IV 46.38 IV
0.04 0.25
Leaf 0.04 0.04 0.21, 0.05 0.05
Diameter 0.04 0.04 0.21 0.04 0.05
Eccentricity 0.84 0.06 0.13 0.05 0.05
Radius 2.40 I 0.05 0.09 0.05 0.05
Tree-hierarchy 0.04 0.04 0.11 0.04 0.04
Kappa 0.17 0.05 0.86 0.08 0.04

BC ¼ betweenness centrality, CC ¼ closeness centrality, I Anecdotal evidence, II Moderate evidence, III Strong evidence, IV Very strong evidence, V Extreme evidence for relation
of MST metric with sign language experience.

Fig. 6. The relation between American Sign Language (ASL) and functional backbone characteristics. The sign language experience in years (x-axis) is related to functional
backbone characteristics (y-axis) in the theta band (4e8 Hz) for both the eyes-open (yellow) and eyes-closed (blue) condition, as indicated by the following minimum spanning tree
metrics (from top-left to bottom-right): mean strength, maximum degree, median betweenness centrality (BC), median closeness centrality (CC), leaf number, diameter, radius and
kappa. Shaded areas: 95% confidence intervals.

Shiell et al., 2014). With the shifts from an eyes-closed to an eyes-
open condition we found a reduction in functional connectivity
strength. This is expected given the shift from more ‘interoceptive’
awareness, characterized by integrative multisensory activity, to-
wards more ‘exteroceptive’ awareness focused on attention and
oculomotor activity (Marx et al., 2004, 2003; Xu et al., 2014). Spe-
cifically for the alpha band, this change may be related to ‘alpha
desynchronization’ during the eyes-open state (Barry et al., 2009;
Go mez-Ramírez et al., 2017; Xu et al., 2014). Moreover, we found
this reduction in functional connectivity strength from eyes-closed
to eyes-open to be larger in deaf than hearing controls. This may be
explained by long-term auditory deprivation and related cross-
modal plasticity mechanisms (Bavelier and Neville, 2002;
Merabet and Pascual-Leone, 2010). It may be explained more
specifically by the enhanced sensitivity of the auditory cortex to
non-auditory stimuli (e.g. Almeida et al., 2015; Auer et al., 2010;
Brozinsky and Bavelier, 2004; Dye et al., 2007; Finney and Dobkins,
2001; Leva€nen and Hamdorf, 2001; Neville and Lawson, 1987a,
1987b) and increased audiovisual connectivity in deaf (Bola et al.,
2017; Li et al., 2016, 2013; Shiell et al., 2014) together with the
reduced integrative multi-sensory activity in the eyes-open state
 mez-Ramírez et al., 2017; Xu et al., 2014).
(Go
4.2. Functional backbone differences between eyes-open and eyes-
closed conditions
We found functional backbone differences between the eyes-
open and eyes-closed conditions in both deaf and hearing
42 M.R.T. Sinke et al. / Hearing Research 373 (2019) 32e47

Fig. 7. The relation between American Sign Language (ASL) and functional backbone characteristics in deaf subject only. The sign language experience in years (x-axis) related
to functional backbone characteristics (y-axis) in the theta band (4e8 Hz) for both the eyes-open (yellow) and eyes-closed (blue) condition, as indicated by the following minimum
spanning tree metrics (from top-left to bottom-right): mean strength, maximum degree, median betweenness centrality (BC), median closeness centrality (CC), leaf number,
diameter, radius and kappa. Shaded areas: 95% confidence intervals.

Table 6
Bayes factors of the relationship between the network backbone metric and ASL-experience in deaf people only.

MST-metric Delta band (0.5-4 Hz) Theta band (4e8 Hz) Alpha band (8e16 Hz) Beta band (16e32 Hz) Gamma band (32e64 Hz)
I
Strength (max) 1.56 3.37 II 0.05 0.12 0.10
Strength (mean) 0.18 43.35 IV 0.71 0.11 0.09
II
Degree (max) 8.14 0.22 0.51 0.10 0.16
I
BC (max) 1.97 0.06 0.07 0.06 0.07
BC (median) 0.61 0.45 0.09 0.06 0.07
I
CC (max) 0.04 0.22 2.08 0.06 0.07
I
CC (median) 0.07 0.99 1.75 0.07 0.07
Leaf 0.36 0.46 0.15 0.10 0.08
Diameter 0.38 0.46 0.16 0.10 0.08
Eccentricity 0.69 0.10 0.10 0.06 0.05
I
Radius 2.44 0.10 0.08 0.05 0.07
Tree-hierarchy 0.04 0.38 0.11 0.09 0.06
II
Kappa 5.00 0.44 0.50 0.21 0.09

BC ¼ betweenness centrality, CC ¼ closeness centrality, I Anecdotal evidence, II

Moderate evidence, IV
Very strong evidence for relation of MST metric with sign language
experience.

subjects, mainly in the alpha and beta bands. During the eyes-open
condition the functional network backbone showed an increased
diameter and eccentricity combined with a decreased leaf number
and connectivity strength, although hearing controls did not show
differences in diameter and leaf number in the alpha band. These
network metrics indicate that the functional backbone topology in
the eyes-open condition was more chainlike (i.e. less integrated and
with reduced global efficiency), whereas during the eyes-closed
condition the topology was more star-like (i.e. more functional
integration and increased global efficiency) (Stam et al., 2014).
These results also nicely fit with the reduced connectivity and
integration in the ‘exteroceptive’ state, as well as the alpha
desynchronization, during the eyes-open condition (Barry et al.,
2007; Chen et al., 2008; Go mez-Ramírez et al., 2017; Marx et al.,
2004; Xu et al., 2014). Other studies reported increased global ef-
ficiency and decreased clustering of functional networks in the
alpha band (Miraglia et al., 2016; Tan et al., 2013) and beta-band
(Gaal et al., 2010; Knyazev et al., 2015) in the eyes-open condition
as compared to the eyes-closed condition, which seem to partly
contradict our findings. This could potentially be explained by the
distinct age groups. One study showed similar effects as our study
in participants between 18 and 35 years, but the opposite effects in
participants between 51 and 80 years (Knyazev et al., 2015). This
pattern is in line with (Miraglia et al., 2016). However, two other
studies also showed contrasting results in younger participants
(Gaal et al., 2010; Tan et al., 2013). These discrepancies might be due
 M.R.T. Sinke et al. / Hearing Research 373 (2019) 32e47
to methodological differences as two studies (i.e. Miraglia et al.,
2016; Tan et al., 2013) used a large number of EEG electrodes or
regions of interest (i.e. respectively 128 and 84) compared to our
study. Increased network sizes, with potential higher densities,
may arguably affect alteration of topological network characteris-
tics if analyzed with classical network metrics (van Wijk et al.,
2010). Network size also affects backbone metrics (Tewarie et al.,
2014), which may explain the discrepancy between our study and
Gaal et al. (2010).
4.3. Larger functional backbone modifications in deaf
We found some backbone differences between deaf and hearing
subjects. Functional backbones in deaf showed higher strength in
the eyes-closed, while lower strength during the eyes-open con-
dition, in both the alpha and beta band. Also in the eyes-open
condition, the leaf number was lower, while the radius and diam-
eter were larger, which means that the functional network topol-
ogy in this state is different between deaf and hearing. More
specifically, the functional backbone of deaf shows less integration
(i.e. reduced global efficiency) and increased clustering. Previous
network studies in deaf also showed increased clustering and local
efficiency, although the small-worldness was preserved (Kim et al.,
2014; Li et al., 2016).
Furthermore, we found larger functional backbone shifts in
these functional backbone characteristics, from the eyes-open to
the eyes-closed condition in deaf people. The patterns in functional
backbone strength correspond with changes we found in functional
connectivity strength between the different sensory cortical re-
gions. They additionally indicate large-scale functional connectivity
changes, i.e. beyond the sensory cortices, since the functional
backbone topology is more altered in deaf when going from eyes-
closed to eyes-open. Accordingly, these findings may also be
explained by transition from ‘exteroceptive’ awareness to ‘intero-
ceptive’ awareness (Marx et al., 2004, 2003; Xu et al., 2014)
together with alterations in inter-regional connectivity e partly
due to alpha desynchronization (Barry et al., 2009; Go  mez-Ramírez
et al., 2017; Xu et al., 2014) e combined with auditory deprivation
and cross-modal plasticity (Bavelier and Neville, 2002; Merabet
and Pascual-Leone, 2010).
We also found that the functional backbone connectivity
strength differed between the different forms of deafness. Func-
tional backbone connectivity might depend on whether people are
born deaf or acquired deafness later in life. Both congenital and pre-
lingual deafness showed similar patterns as hearing controls,
whereas post-lingual deaf showed the largest deviation, which is in
agreement with previous findings. It has been shown that cross-
modal plasticity is dependent on the age of onset and duration of
deafness (Brotherton et al., 2016; Li et al., 2016, 2013; Sadato et al.,
2004). However, given the limited number of post-lingual deaf in
our study as well as the complex relationship of cross-modal
plasticity with other factors, such as age of onset, duration of
deafness and sign-language experience, it is impossible to be
conclusive.
4.4. Relation between backbone characteristics and sign language
experience
Sign language comprehension have shown to be related to
activation of brain regions which are normally considered to be
involved in unimodal (e.g. speech or sound) auditory processing,
such as frontal and temporal regions (Li et al., 2016; Liu et al., 2017;
Malaia et al., 2014; Meyer et al., 2007; Neville et al., 1998;
Nishimura et al., 1999; Petitto, 2000; Sadato et al., 2005). Language
43
comprehension requires higher cognitive functions. Increased use
and experience in sign language may therefore arguably enhance
functional integration between different brain regions as well as
cross-modal plasticity (Nishimura et al., 1999; Petitto, 2000; Sadato
et al., 2005). Accordingly, we found a relation between years of sign
language experience and functional backbone characteristics. This
was found most prominently in the theta band, but also in the delta
and alpha bands. In both deaf and hearing, increasing experience in
sign language was related to a higher average backbone strength,
suggesting increased global efficiency and integration. The
decreased closeness centrality suggests more segregation and local
clustering. Our reported relations with sign language experience
are in line with previous examinations of functional network dif-
ferences between hearing signers and non-signers. That study
found sign-language comprehension to be related to increased
local efficiency, small-worldness and modularity (i.e. segregation)
(Liu et al., 2017). To our knowledge no network studies were per-
formed on sign-language comprehension in deaf. However, other
connectivity studies in deaf showed enhanced functional connec-
tivity between brain regions which are specifically recruited for
higher cognitive functions, such as comprehension of sign language
(Li et al., 2016; Malaia et al., 2014). Further research is needed to
elucidate the mechanisms of reorganization in functional brain
networks in relation to sign language acquisition and experience.
4.5. Differences between frequency bands
Our study shows that the effects of deafness, eyes-condition or
sign-language experience are limited to specific frequency bands,
which suggests that auditory deprivation does not alter functional
networks as much in all frequency bands. Different brain networks
and behavioral functionalities are related to distinct frequency
bands (Başar et al., 2000; Buschman and Miller, 2007; Klimesch,
1999; Wro bel, 2000; Wrobel et al., 2007). Cognitive tasks that
involve working memory, such as sign language, are mostly related
to alpha and theta activity (Klimesch, 1999; Stam and van Straaten,
2012). This may explain the relationship we found between sign
language experience and functional backbone topology in those
frequency bands. Furthermore, both the alpha and beta band are
related to attention, including visual attention (Stam and van
Straaten, 2012; Wro  bel, 2000; Wrobel et al., 2007). These bands
alter by transition from eyes-closed (i.e. ‘interoceptive’ awareness)
to eyes-open (i.e. ‘exteroceptive’ awareness) (Barry et al., 2009,
2007; Go  mez-Ramírez et al., 2017). Overall, it seems therefore that
reorganization in topology of functional brain networks in deaf is
strongly associated with cognitive functioning as well as with
attentional state. Further research is nonetheless needed to inves-
tigate this into more detail.
4.6. Advantages of study design and tools
Our study used the unbiased MST approach (Tewarie et al., 2015)
for network analyses. The methodology illustrates that acquired
backbone metrics are highly suitable in exploring the topology and
connectivity of brain networks and cross modal neuroplasticity
(Engels et al., 2015; Tewarie et al., 2014; van Diessen et al., 2016).
Our study yielded a unique dataset of subjects with intermediate to
long periods of auditory deprivation combined with different levels
of sign language experience. Such a dataset would be difficult to
acquire in Western countries with well-established health-care
systems and many people with hearing disabilities equipped with a
cochlear implant. Cochlear implants have shown to be related to
functional cortical reorganization (Strelnikov et al., 2010) and
almost normal developing auditory language processing (Hammes
44 M.R.T. Sinke et al. / Hearing Research 373 (2019) 32e47
et al., 2002). In our study population, none of the participants had a
cochlear implant. Lastly, our study shows the usefulness of a
portable EEG device. These mobile devices are invaluable tools for
use in rural or resource-limited settings. It enabled us to acquire
recordings from participants in a country where auditory depri-
vation e and neurological disorders in general e are more preva-
lent than in Western countries, but where neuroimaging research is
often impossible or burdensome due to geographic conditions,
poor health-care infrastructure and high levels of poverty.
4.7. Study limitations and future directions
Our study has limitations. The neural brain activity was
measured at a limited amount of scalp locations. EEG also lacks
information from deeper brain structures. The EEG signals are
linear combinations of the neural generators they project to the
scalp location of the electrodes. The precision of functional network
mapping is consequently reduced. Other neuroimaging techniques,
such as fMRI, might therefore be more capable to capture different
activation patterns of the whole brain at both cortical and sub-
cortical level. The use of wireless headsets for EEG recording may
have increased the noise in the EEG signal, and affected the back-
bone computations. However, recent studies have shown similar
performance of wireless headsets compared to standard EEG
hardware (Badcock et al., 2013; David Hairston et al., 2014; Schiatti
et al., 2016).
History taking in our study might be affected by a recall bias.
Patient records (i.e. dates of births) in Nigeria are not stored like
they are in modern Western countries. Many people living in rural
Nigeria do not exactly know their birthday. This bias may have
increased the noise-level in the regression analysis.
Apart from backbone analysis future studies may try alternative
promising network analysis techniques such as dynamic functional
connectivity modeling (Avena-Koenigsberger et al., 2017;
Breakspear, 2017), Bayesian exponential random graph models
(Caimo and Friel, 2011; Sinke et al., 2016), mixed-effect models
(Simpson and Laurienti, 2015) and Gibbs distribution models (La
Rosa et al., 2016). These techniques also enable unbiased compar-
ison of networks differing in size and density but may capture more
subtle differences between groups. Combining techniques might
further elucidate the role of specific brain areas in functional
network alterations in normal and sensory lacking conditions. This
may ultimately improve our understanding of neuroplasticity
occurring after auditory and other types of sensory deprivation.
5. Conclusion
In conclusion, we were able to detect functional backbone dif-
ferences between eyes-closed and eyes-open conditions as well as
larger shifts in functional backbone characteristics in deaf as
compared to controls. Effects that are presumably a consequence of
auditory deprivation and cross-modal plasticity. Subtle differences
were seen between different forms of deafness. Our study
demonstrated functional network backbone characteristics to be
related with increasing experience of sign language. Our study
provide original insights into the organization and reorganization
of functional brain networks derived from EEG data, both in deaf
and healthy people. Our results further underpin the notion of
brain-wide neuroplasticity mechanisms and global network reor-
ganization in the cortex of deaf, which emphasize the importance
to study the brain e as well as cross-modal plasticity e from a
network perspective. The link between the functional network
backbone characteristics and acquired sign language experience
reflects ongoing brain adaptation in both hearing and deaf people.
Contributors
MRTS, JWB, EvD and WMO were involved in the study design.
MRTS, JWB, FvdM, JN and WMO were involved in the data acqui-
sition. MRTS, JWB, and WMO performed the data analysis. MRTS,
JWB, FvdM, JN, RMD, EvD and WMO interpreted the data and wrote
the manuscript.
Funding
This work was supported by the Netherlands Organisation for
Scientific Research (NWO-VENI 016.168.038), and the Dutch Brain
Foundation [F2014(1)-06].
Disclosure/conflict of interest
None of the authors has any conflict of interest to disclose in
relation to this work.
Appendix A. Supplementary data
Supplementary data to this article can be found online at
https://doi.org/10.1016/j.heares.2018.12.006.
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