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Differences in functional brain network connectivity during stories presented in audio, illustrated, and animated format in preschool-age children

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The American Academy of Pediatrics (AAP) recommends that parents begin reading to their children soon after birth, and limits on screen-based media. Benefits of traditional book-sharing are well documented in children, while cited deleterious effects of animated content on narrative processing are controversial. The influence of story format on underlying functional brain networks has not previously been studied. Thirty-three healthy children were recruited for this study via advertisement at an academic medical center, which involved functional magnetic resonance imaging (fMRI) at a single visit. Twenty-seven of them completed fMRI (82%; 15 boys, 12 girls; mean 58 ± 8 months old). The fMRI protocol involved the presentation of 3 similar, unrhymed stories by the same author lasting 5 min each in audio, illustrated, and animated format during separate runs, followed by a test of factual recall. Within- and between-network functional connectivity (FC) was compared across formats involving five functional networks, which were defined via literature review and refined via a data-driven parcellation method: visual perception, visual imagery, language, Default Mode (DMN), and cerebellar association. For illustration relative to audio, FC was decreased within the language network and increased between visual, DMN, and cerebellar networks, suggesting decreased strain on the language network afforded by pictures and visual imagery. Between-network connectivity was decreased for all networks for animation relative to the other formats, particularly illustration, suggesting a bias towards visual perception at the expense of network integration. These findings suggest substantial differences in functional brain network connectivity for animated and more traditional story formats in preschool-age children, reinforcing the appeal of illustrated storybooks at this age to provide efficient scaffolding for language, and suggesting novel neurobiological correlates of how functional networks may contribute to this process.
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Brain Imaging and Behavior
ISSN 1931-7557
Brain Imaging and Behavior
DOI 10.1007/s11682-018-9985-y
Differences in functional brain network
connectivity during stories presented in
audio, illustrated, and animated format in
preschool-age children
John S.Hutton, Jonathan Dudley, Tzipi
Horowitz-Kraus, Tom DeWitt & Scott
K.Holland
1 23
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ORIGINAL RESEARCH
Differences in functional brain network connectivity during stories
presented in audio, illustrated, and animated format
in preschool-age children
John S. Hutton
1,2,3
&Jonathan Dudley
1,3,4
&Tzipi Horowitz-Kraus
1,2,3,5
&Tom DeWitt
1,2,3
&Scott K. Holland
6,7
#Springer Science+Business Media, LLC, part of Springer Nature 2018
Abstract
The American Academy of Pediatrics (AAP) recommends that parents begin reading to their children soon after
birth, and limits on screen-based media. Benefits of traditional book-sharing are well documented in children, while
cited deleterious effects of animated content on narrative processing are controversial. The influence of story format
on underlying functional brain networks has not previously been studied. Thirty-three healthy children were recruited
for this study via advertisement at an academic medical center, which involved functional magnetic resonance
imaging (fMRI) at a single visit. Twenty-seven of them completed fMRI (82%; 15 boys, 12 girls; mean 58 ±
8 months old). The fMRI protocol involved the presentation of 3 similar, unrhymed stories by the same author
lasting 5 min each in audio, illustrated, and animated format during separate runs, followed by a test of factual
recall. Within- and between-network functional connectivity (FC) was compared across formats involving five func-
tional networks, which were defined via literature review and refined via a data-driven parcellation method: visual
perception, visual imagery, language, Default Mode (DMN), and cerebellar association. For illustration relative to
audio, FC was decreased within the language network and increased between visual, DMN, and cerebellar networks,
suggesting decreased strain on the language network afforded by pictures and visual imagery. Between-network
connectivity was decreased for all networks for animation relative to the other formats, particularly illustration,
suggesting a bias towards visual perception at the expense of network integration. These findings suggest substantial
differences in functional brain network connectivity for animated and more traditional story formats in preschool-age
children, reinforcing the appeal of illustrated storybooks
at this age to provide efficient scaffolding for language,
and suggesting novel neurobiological correlates of how
functional networks may contribute to this process.
Keywords fMRI .Functional connectivity .Narrative
processing .Story listening .Children .Visual imagery .
Screen time .Shared reading
Abbreviations
AAP American Academy of Pediatrics
BOLD Blood oxygen leveldependent
CB Cerebellar network
DMN Default Mode Network
FDR False discovery rate
FC Functional connectivity
fMRI Functional magnetic resonance imaging
LLanguagenetwork
MNI Montreal Neurologic Institute
Electronic supplementary material The online version of this article
(https://doi.org/10.1007/s11682-018-9985-y) contains supplementary
material, which is available to authorized users.
*John S. Hutton
John1.Hutton@cchmc.org
1
Department of Pediatrics, University of Cincinnati College of
Medicine, Cincinnati, OH, USA
2
Division of General and Community Pediatrics, Medical Center,
3333 Burnet Avenue, MLC 15008, Cincinnati, OH 45229, USA
3
Reading and Literacy Discovery Center, Cincinnati Childrens
Hospital Medical Center, 3333 Burnet Avenue, MLC 15008,
Cincinnati, OH 45229, USA
4
Pediatric Neuroimaging Research Consortium, Cincinnati Childrens
Hospital Medical Center, Cincinnati, OH, USA
5
Educational Neuroimaging Center, Technion, Israel
6
Department of Physics, University of Cincinnati, Cincinnati, OH,
USA
7
Medpace, Inc., Cincinnati, OH, USA
Brain Imaging and Behavior
https://doi.org/10.1007/s11682-018-9985-y
Author's personal copy
SES Socioeconomic status
VI Visual imagery network
VP Visual perception network
Introduction
The American Academy of Pediatrics (AAP) recommends
that parents begin reading to their children as soon as possible
after birth, citing enduring cognitive, social-emotional, and
neurobiological benefits (AAP Council on Early Childhood
et al. 2014). By contrast, the AAP recommends limits on
screen-based media, citing developmental and health risks
with early and excessive use (AAP Council on
Communications and Media 2016).Ledbytelevision,
screen-based media is ubiquitous in childrens lives, perceived
benefits for learning and creativity major motivators for use
(Garrison and Christakis 2005; Zimmerman et al. 2007;
Rideout 2017). Portable platforms such tablet-based apps
add unprecedented dimensions to story sharing, including an-
imation, responsive touch screens, and the option for a device
to serve as the reader (Parish-Morris et al. 2013). However,
while controversial, animated content has been associated
with deleterious effects on narrative comprehension in chil-
dren, compared to traditional storybooks (Chiong et al. 2012;
Parish-Morris et al. 2013; Bus et al. 2015).
As reading is a relatively new invention, children are not
born with a hard-wired brain network supporting this ability
(Dehaene et al. 2015; Horowitz-Kraus and Hutton 2015).
Instead, language, visual, and other networks are Brecycled^
and integrated in response to reading exposure and practice
(Dehaene et al. 2015, Horowitz-Kraus and Hutton 2015).
While primary visual and auditory networks mature relatively
early, those for higher-order skills exhibit protracted develop-
ment (Gogtay et al. 2004; Power et al. 2010), including seman-
tic language (Price 2012) and the default-mode network
(DMN), implicated in internally-oriented processes such as ep-
isodic memory and visual imagery (Fair et al. 2008; Daselaar
et al. 2010; Sestieri et al. 2011). The cerebellum plays an im-
portant role in the mastery of cognitive skills (Stoodley 2012;
Buckner 2013), and is engaged during narrative processing in
preschool-age children (Hutton et al. 2017a,b).
Visual imagery is a higher-order skill that enables listeners
and readers to Bsee a story^in their minds eye and bring it to
life, even in the absence of visual stimulus (Bridge et al.
2012), supporting comprehension on cognitive and emotional
levels (Gambrell and Jawitz 1993;Justetal.2004; Ganis and
Schendan 2011; Pearson et al. 2015). The use of imagery is
associated with enhanced reading ability and learning (Levin
1972; Gambrell and Jawitz 1993; McDonough et al. 2011),
memory consolidation and recall (Oliver et al. 2016), and
long-term mental health (Pearson et al. 2015). Successful ap-
plication of imagery involves the integration of primary and
higher-order visual, lexical-semantic, executive, and limbic
brain areas (Mechelli et al. 2004;Daselaaretal.2010;Ganis
and Schendan 2011). The influence of story format on the
integration of brain networks supporting imagery and narra-
tive processing has not previously been studied.
Functional connectivity (FC) analysis via Blood Oxygen
Level Dependent functional Magnetic Resonance Imaging
(BOLD fMRI) is a powerful means to explore the engagement
and integration of brain networks during a variety of cognitive
states or task conditions (Bastos and Schoffelen 2015), and com-
parison between them (Di et al. 2013;Brayetal.2015). While
many questions remain unanswered regarding optimal FC con-
figurations within- and between-networks in such analyses, gen-
eral principles include topological efficiency, modularity (spe-
cialization of different regions for specific functions), and robust
integration supporting adaptive, higher-level function (Sporns
2011; Bullmore and Sporns 2012). The aim of this study was
to explore FC within and between functional brain networks
supporting imagery, language, and learning during stories pre-
sented in audio, illustrated, and animated format in preschool-age
children. This age range is particularly important as it represents a
dynamic span of brain development and plasticity (Knudsen
2004; Power et al. 2010) highly influenced by cognitive stimu-
lation in the home (Hutton et al. 2015;2017a,b), notably shared
reading and screen-based media use (Rideout 2017). Our hypoth-
esis was that increasing visual stimulus would be associated with
progressively higher FC for visual perception, lower FC involv-
ing imagery and language, and less cerebellar engagement for
more visually stimulating formats, attributable to less need to
access and integrate internally derived images.
Methods
Participants
This study involved 33 healthy, preschool-age children re-
cruited recruited via advertisement at our institution.
Exclusion criteria included prematurity before 38 weeks, de-
velopmental delay, head trauma, bilingual/non-English speak-
ing household, kindergarten attendance, and standard contra-
indications to MRI. Written informed consent was obtained
from a custodial parent for each child, families were compen-
sated for time and travel, and our study was approved by the
Cincinnati Childrens Hospital Institutional Review Board.
Magnetic resonance imaging and preprocessing
MRI was performed via a 3 T Philips Ingenia scanner with a
32-channel head coil equipped with an Avotec audiovisual
system. For fMRI, BOLD-weighted scans covering the entire
brain with voxel size 2.5 × 2.5 × 3.5 mm were acquired via
multiband acquisition, with multiband factor of 4, SENSE =
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1.5, flip angle 57 degrees, and TR/TE = 597/30 ms. Details of
play-based acclimatization techniques used with children pri-
or to MRI are described by Vannest, et al. (Vannest et al.
2014). All children were awake and non-sedated during
MRI, alertness monitored with a ViewPoint® visual eye-
tracking system (Arrington Research, Inc., Scottsdale, AZ).
Our protocol involved a T1-weighted anatomical scan lasting
approximately 6 min, and four BOLD fMRI sequences lasting
approximately 5 min each (resting state and 3 active tasks).
MRI data pre-processing was performed in the CONN tool-
box using standard spatial and temporal pipelines (Whitfield-
Gabrieli and Nieto-Castanon 2012). As connectivity analyses
are highly susceptible to bias from head movement, CONNs
Artifact Detection Tool (ART) was used to calculate
framewise composite movement, and frameswith >1 mm mo-
tion or global mean intensity z-score > ± 6 were demarcated as
outliers and excluded from first-level analyses. In addition to
this scrubbing, temporal preprocessing and denoising includ-
ed bandpass filtering (0.0080.09 Hz) and regression of the
following: zero- and first-order derivatives of framewise trans-
lational and rotational motion parameters, principal compo-
nents of BOLD signals originating from white matter and
cerebrospinal fluid compartment (top 5 of each), and the he-
modynamic response convolved effect of task time series.
fMRI story protocol
Our fMRI protocol involved a series of continuous task states
increasing in density of visual stimuli. Three different chil-
drens storybooks lasting approximately 5 min each (294
± 6 s) were presented without interruption in three formats
(audio, audio + illustration, animation), separated by 23-
min pauses. We developed this protocol to address concerns
regarding excessive motion and confusion/anxiety with tradi-
tional fMRI block designs in children, and to present an eco-
logicaltask state comparable to story presentation in the real
world (Hasson et al. 2010). A different story was used for each
format to address the potential confound of repeated exposure
to narrative content (i.e. the same story 3 times) rendering later
trials less difficult or interesting. The order of story presenta-
tion was the same for each child (audio audio + illustration
animation), to address potentially confounding visual prim-
ing effects and concerns that exposure to animated content can
negatively influence cognitive function during subsequent
tasks at this age (Lillard and Peterson 2011).
The three stories used were published picture books written
by the same author and intended to be read aloud, non-
rhymed, and similar in lexical, syntactic, and semantic con-
tent, with Lexile® level from 460 to 490 (MetaMetrics,
Durham NC). Content for the audio and illustrated stories
was downloaded with permission from the authors website
(RobertMunsch.com), read aloud by the author without music
or other enhancement. During the audio task, children
watched a blank screen with cross fixation. During the
illustrated task, high-resolution images from the book were
paired with audio narrative and presented via a video screen.
The animatedstory was from a series adapted for television (A
Bunch of Munsch, YouTube) that closely adheres to the sto-
rybook version, presented via a video screen.
Immediately following MRI, children were asked three
questions per story regarding basic factual content, whether
they could hear the story well (1 = yes, 2 = no), and how in-
teresting it was (1 = very, 2 = kind of, 3 = not very). Of note,
these questions were added to our protocol midwayalong, and
administered to 14 of 27 children. Responses were compared
between formats via 2-tailed t-tests.
Functional brain network definition and parcellation
Five functional brain networks involved with narrative pro-
cessing were defined via literature review, emphasizing meta-
analyses and connectivity-based research involving children,
summarized in Table 1.Thesewere:1)visualperception(VP;
(Calhoun et al. 2001)), 2) higher-order visual/imagery (VI;
(Mechelli et al. 2004, Daselaar et al. 2010)), 3) Default
Mode (DMN; (Fair et al. 2008, Uddin et al. 2009)), 4) lan-
guage (L; (Binder et al. 2009,Price2012)), and 5) cerebellar
association (CB; (Stoodley 2012,Buckner2013)). The DMN
was included given its core role in visual imagery, notably via
access to episodic memory (Daselaar et al. 2010; Sestieri et al.
2011). The cerebellar network was included given its
established role in narrative processing and other cognitive
functions (Buckner 2013;Huttonetal.2017a,b). The lan-
guage network emphasized semantic processing, given behav-
ioral evidence of lexical-semantic benefits associated with
shared reading (High and Klass 2014), cited negative effects
of animated content on narrative comprehension (Chiong et al.
2012; Parish-Morris et al. 2013; AAP Council on
Communications and Media 2016), and no known association
of either with acoustic or phonological abilities.
The spatial extent of the functional networks was generated
in terms of neurological Brodmann Areas (BA) and, when
appropriate, anatomically delineated structures (e.G.
hippocampus and cerebellar regions (Diedrichsen et al.
2009)). Although these delineations are useful for framing
hypotheses and contextualizing results, in particular with re-
spect to a methodologically varied body of neuroimaging lit-
erature, they are ill-suited as region of interest (ROI) defini-
tions in connectivity analyses for two related reasons: 1) The
shape and volumes of these delineations are heterogenous and
often encompass very large areas of the cerebrum, and 2)
Actual patterns of functional connectivity often do not closely
follow anatomical or cytoarchitectural boundaries and typical-
ly have a much finer resolution. Thus, using such definitions
as ROIs can bias results and substantially reduce the sensitiv-
ity of connectivity analyses. Accordingly, we applied an
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Table 1 A priori defined functional brain networks
Brain Network (reference) Brodmann Areas (bilateral) Functional Areas (bilateral) Number of areas defined by parcellation
Default Mode (DMN) (Fair, 2008; Uddin 2010) 7 Precuneus 117
8, 9, 10 Dorsomedial Prefrontal (DMPFC)
23, 29, 30, 31 39 Posterior cingulate gyrus
34, 35, 36 Angular gyrus
Parahippocampus
Visual Imagery (Mechelli, 2004; Daselaar 2010) 7 Precuneus 83
9 Dorsolateral Prefrontal (DLPFC)
19 Visual association cortex
37 Fusiform gyrus
Hippocampus Hippocampus
Visual Perception (Calhoun, 2001) 17, 18 Primary visual cortex 47
37 Fusiform gyrus
Semantic Language (Price 2012, Binder 2009) 21 Middle temporal gyrus 79
22 Superior temporal gyrus (Wernickes)
38 Temporal pole
39 Angular gyrus
44, 45 Inferior frontal gyrus (Brocas)
47 Orbitofrontal gyrus
Cerebellar Association (Stoodley 2012, Buckner 2013) N/A Crus I, II, Lobule VI, VIIb 46
Functional brain networks defined a priori as neurological Brodmann Areas or anatomical names via the Harvard-Oxford Functional Brain or Automated Anatomical Labeling Atlas. Primary references for
each network are included in parentheses. The number in the right column is the number of areas (nodes) for the respective network derived via parcellation
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established, data-driven parcellation approach (Craddock
et al. 2012) to generate functionally homogenous ROIs of
similar sizes within the spatial extent of our five networks.
First, the preprocessed functional data from the resting state
were masked to each of our networks of interest. Then,
voxelwise temporal correlation matrices were computed for
each subject. These matrices were then averaged across sub-
jects and a normalized cut spectral clustering algorithm was
applied to generate N preliminary ROIs per network where N
was chosen such that resultant ROIs were roughly 2.14 mL in
volume (or, spheroids of ~8 mm radius). Lastly, the networks
were refined to eliminate functionally incongruous ROIs that
resulted from the inclusion of very large Brodmann Areas in
the initial network definitions. Connectivity matrices were
generated for each network using the resting state data, and
ROIs with median connectivity strength (Fisher transformed
r) of less than 0.1 across all subjects were discarded. Using this
approach, 372 ROIs were defined, comprising our five refined
networks (Table 1).
Functional connectivity analysis
The CONN toolbox was used for all FC analyses (Whitfield-
Gabrieli and Nieto-Castanon 2012), to extract ROI time series
data from spatially preprocessed functional data, apply tempo-
ral denoising (aCompCor, bandpass filtering), and compute
first-level connectivity measures for each of the story formats.
We then used custom MATLAB-based programming to ex-
plore second-level FC within and between our refined net-
works. Because we hypothesized format-dependent differences
in connectivity at the network level, we computed aggregate
functional connectivity (FC) measures, which were calculated
as the mean of the sum of pair-wise, Fisher-transformed, bivar-
iate correlation coefficients for all ROIs within or between net-
works. FC scores were then compared between story formats
(e.g. audio vs. illustration) via 2-tailed, paired t-tests. False dis-
covery rate correction (FDR) was applied, accounting for the
number of network comparisons in each contrast (15).
Significant results at the network level were further ex-
plored via post hoc analyses. For each of these, ROI-level
connections within/between relevant networks were tested be-
tween story formats using 2-tailed, paired t-tests. False discov-
ery rate correction was applied, accounting for the number of
possible connections in each analysis (on the order of 10
3
).
Results
Demographics
Twenty-seven of the thirty-three children arriving for their study
visit (82%) completed functional MRI (15 boys, 12 girls; mean
58 ± 8 months, range 4471; all Caucasian). Fifty-six percent of
mothers were college graduates, 26% graduate level, 15% high
school, and 4% below high school. Fifteen percent reported
household income under $50,000/year, 33%
$50,000$100,000/year, and 52% over $100,000/year.
Story post-tests
Fourteen children completed story post-tests. All reported be-
ing able to hear each story equally well, and there was no
significant difference in interest (all Bkind of^interesting, on
average). Mean correct responses were 81% for audio (±
33%), 70% for illustration (± 22%), and 50% for animation
(± 33%), a significant difference for audio>animation
(p< 0.05), marginal for illustration>animation (p< 0.1), and
not significant for audio>illustration.
Subject motion during story formats and resting state
For quality assurance, several summary motion statistics were
computed for each subject and each task condition: number of
demarcated outliers, mean framewise composite motion, and
root-mean square of framewise change in global mean inten-
sity. The number of outliers was significantly greater for rest
than for each story format (p< 0.05), yet not significantly
different between story formats. Similarly, composite motion
was consistently yet non-significantly greater during rest com-
pared to each story format (p= 0.11, 0.15, and 0.08, respec-
tively), yet not significantly different between story tasks.
Intensity was not significantly different between rest and each
format, or between story formats.
Functional connectivity for individual story formats
and resting state
Within-network FC was significantly, though variably, posi-
tive for all networks in each story format and during resting
state, suggesting network coherence. Between-network FC
was significantly, even more variably, positive in all story
formats for all network pairs, with the exception of VP-L,
which was marginally positive for illustration only. Within-
and between-network FC did not significantly correlate with
gender, maternal education, or income level in any formats or
resting state.
Functional connectivity differences between story
formats
Comparisons of within- and between-network FC changes
across story formats are summarized in Fig. 1and Table 2.
In addition to examples below, three-view renderings of sig-
nificant within- and between-network FC differences between
story formats elucidated via post hoc tests are provided online
(eFigure 19).
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Illustration relative to audio
For illustration relative to audio, within-L FC was decreased
16%, largely driven by fewer inter-hemispheric connections,
showninFig.2. Regions of interest (ROI) highly involved in
these changes were anterior/superior temporal (BA 22, 38) and
inferior frontal (BA 44, 45) areas, classical language areas in the
Wernicke-Geshwind model (Holland et al. 2007;Price2012).
Between-network FC was increased for VP-CB (66%), VP-
DMN (55%), and VP-VI (32%), largely driven by increased
inter-hemispheric connections, and for VP-CB, increased con-
nections with the left cerebral hemisphere, especially fusiform
areas (BA 37). An example (VP-DMN) is shown in Fig. 3.
Animation relative to illustration
For animation relative to illustration, within-VP FC was de-
creased 19%, largely driven by decreased inter-hemispheric
connections and connections between primary visual and fu-
siform (BA 37) areas. Between-network FC was decreased
Fig. 1 Comparison of within- and between-network functional
connectivity changes between story formats. Connectivity wheels
show the percent change in functional connectivity (FC) within and
between networks, for audio, illustrated, and animated format. For each
wheel, the Btread^represents within-network FC and the Bspokes^
represent between-network FC, applying false discovery rate correction
(p< 0.05). Solid lines reflect statistically significant differences, with red
reflecting increased FC and blue reflecting decreased FC. There were
significant changes in illustration relative to audio (within-L decrease;
VP-CB, VP-DMN, and VP-VI increases), animation relative to audio
(VP-L decrease), and animation relative to illustration (decreases
within-VP and between all networks)
Table 2 Summary of significant functional connectivity changes for each story format contrast
Contrast Network(s) Avg
ΔConnectivity
%
Change
Tot al RO I-
ROI
Altered
(p<0.05)
% Positive/
Negative
% L/R/Cross-Hemispheric
Illustration-Audio Language 0.04.0 16% 3081 43 0/100 37/16/47
Perception-DMN 0.039 55% 5499 143 90/10 18/38/44
Perception-Imagery 0.041 32% 3901 292 87/13 29/26/51
Perception-Cerebellum 0.037 66% 2162 4 75/25 100/0/0
Animation-Illustration Perception 0.048 19% 1081 27 4/96 11/48/41
Perception-Cerebellum 0.025 26% 2162 0 ––
Perception-DMN 0.040 37% 5499 41 5/95 7/34/59
Perception-Language 0.055 82% 3713 291 0/100 31/20/49
Perception-Imagery 0.022 13% 3901 11 18/82 36/18/45
Cerebellum-DMN 0.027 24% 5382 0 ––
Cerebellum-Language 0.029 32% 3634 0 ––
Cerebellum-Imagery 0.038 32% 3818 0 ––
DMN-Language 0.027 19% 9243 38 11/89 11/34/55
DMN-Imagery 0.029 17% 9711 16 44/56 6/25/69
Language-Imagery 0.050 49% 6557 352 0/100 24/24/52
Animation-Audio Perception-Language 0.044 78% 3713 289 3/97 30/20/50
Significant changes in functional connectivity (FC) within and between networks for each story format contrast surviving false discovery rate correction
(p< 0.05), detailed by post hoc tests. Columns show involved networks, average change in FC, the percentage of possible connections significantly
altered, percentage ofpositive and negative changes, and percentage involving left, right, and cross-hemispheric connections. We attribute the absence of
significantly altered ROI-level connections involving the cerebellar network for animation>illustration as attributable to similar changes in FCacrossthe
entirety of the cerebellar network rather than localized effects
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for all network pairs (13% to 82%, mean 33%, summary
Table 2), largely involving inter-hemispheric connections.
FC decreases involving visual and language ROI were dif-
fuse, particularly precuneus (BA 7), fusiform (BA 37),
superior/middle temporal (BA 21, 22), and angular gyri
(BA 39). An example is shown in Fig. 4(VI-L). Despite
overall decreases (24%32%), post-hoc tests did not identify
ROI-level changes in FC involving the cerebellar network,
attributable to relative functional homogeneity and similar
changes across the entirety of the CB network for this
contrast.
Animation relative to audio
For animation relative to audio, FC was decreased 78% be-
tween VP-L, largely driven by decreased inter-hemispheric
connections, highly involving fusiform (BA 37), superior/
middle temporal (BA 21, 22), and inferior frontal (BA 44,
45) areas. FC was marginally decreased within-CB, within-
DMN, within-L, and within-VP, and between L-VI (p<0.15,
FDR corrected).
Discussion
Cognitive, social-emotional, and neurobiological benefits of
shared storybook reading are well-documented in children
(National Early Literacy Panel 2008, Hutton et al. 2015,
U.S. Department of Education 2015,Huttonetal.2017a,b),
and the American Academy of Pediatrics (AAP) recommends
parents begin reading to their children as soon as possibleafter
birth (AAP Council on Early Childhood et al. 2014). Despite
AAP recommendations and evidence and advocacy behind
them, shared reading of traditional storybooks remains rela-
tively low (Scholastic 2015; Rideout 2017; Read Aloud
15 Minutes National Campaign 2018). Fueled by perceived
benefits for creativity and learning, screen-based media use is
ubiquitous and rising in children, beginning in infancy
(Garrison and Christakis 2005; Zimmerman et al. 2007;
Rideout 2017). Joining TV, increasingly popular screen-
based platforms such as tablets have added unprecedented
dimensions to story sharing, including animation and the op-
tion of a device to serve as the Breader^(Parish-Morris et al.
2013; Rideout 2017). Portable devices have eliminated bar-
riers to access, providing unprecedented opportunities for
Fig. 2 Changes in functional connectivity within the language
network in illustrated format relative to audio. FC was decreased
16%, with 47% of the decrease involving inter-hemispheric connections,
37% involving the left hemisphere, and 16% involving the right
hemisphere. Blue lines designate significantly decreased pairwise
connections. Nodes represent regions of interest, with red reflecting
positive contribution to FC change, blue reflecting negative
contribution to FC change, and white reflecting no change, depth of
color reflecting magnitude of effect. Post hoc analyses were performed
using 2-tailed t-tests, with analysis-level FDR correction, p<0.05
Fig. 3 Changes in functional connectivity between visual perception
and Default Mode networks in illustrated format relative to audio.
FC was increased 55%, with 44% of the increase involving inter-
hemispheric connections, 18% involving the left hemisphere, and 38%
involving the right hemisphere. Red lines designate significantly
increased pairwise connections (90%) and blue lines designate
significantly decreased pairwise connections (10%). Nodes represent
regions of interest, with red reflecting positive contribution to FC
change, blue reflecting negative contribution to FC change, and white
reflecting no change, depth of color reflecting magnitude of effect. Post
hoc analyses were performed using 2-tailed t-tests, with analysis-level
FDR correction, p<0.05
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solitary and excessive use (Ma and Birken 2017). While con-
troversial, there is evidence of negative effects of animated
content on parent-child engagement, comprehension, and cog-
nitive function relative to traditional storybooks (Chiong et al.
2012; Parish-Morris et al. 2013; Bus et al. 2015; Lillard et al.
2015).
Proposed mechanisms of deleterious effects of inopportune
screen-based media use include inadequate practice of self-
regulation and creative skills (Christakis et al. 2009; AAP
Council on Communications and Media 2016). The aim of
this study was to explore the influence of story format on the
integration of functional brain networks involved with skill
refinement (cerebellar), language, and imagery, the latter a
critical skill that helps bring stories Bto life^in support of
narrative comprehension and learning (Gambrell and
Koskinen 2002; Ganis and Schendan 2011; McDonough
et al. 2011). This question is particularly relevant for
preschool-age children, whose brains are growing rapidly
(Knudsen 2004; Power et al. 2010) and responsive to cogni-
tive stimulation at home (Hutton et al. 2015;2017a,b), of
which shared reading and screen-based media are major con-
tributors (Rideout 2017). Our hypothesis was that increasing
visual loading, especially animated content, would bias func-
tional networks towards visual perception, with progressively
less integration of the other networks, particularly visual im-
agery and language.
Decreased within-network FC during the illustrated story
relative to audio in the language (L) network is consistent with
our hypothesis and the adage that Ba picture is worth 1000
words.^Diffuse, bilateral activation in frontal and temporal
language areas during audio story listening is well-described
in children, interpreted as reflecting difficulty or strain
(Holland et al. 2007;Berletal.2010). Thus, diffusely lower
inter-hemispheric FC in these areas found for this contrast
(Fig. 2), suggests reduced workload in the L network. It is
reasonable to infer that the catalyst for this finding was in-
creased FC between VP, VI, and DMN (an Bimagery
module^), a potential mechanism by which illustrations and
internally-generated images could be integrated to illuminate
the narrative. Primary visual processing areas are known to
participate in imagery, notably via access to fusiform lexical-
semantic regions (Schmithorst et al. 2007; Whittingstall et al.
2014), which were major drivers of the increase in FC for this
contrast (Fig. 3). This cognitive/developmental process has
been described in behavioral-educational literature as scaf-
folding,where support necessary for a given child, age, and
task is incrementally provided to assist with mastery (Wood
et al. 1976; Crain-Thoreson and Dale 1999;McDonough et al.
2011). Our findings provide a novel neurobiological correlate
for the appeal of illustrated storybooks for young children.
Consistent with evidence that they provide scaffolding for
language (Crain-Thoreson and Dale 1999), we observed max-
imal FC between networks involved with perception (VP;
illustrations) and imagery (VP, VI, DMN) with decreased
strain on the language network (within-L, cross-hemispheric)
during the illustrated story relative to other formats.
Within-network FC in the language network was only mar-
ginally decreased during animation relative to audio, suggest-
ing less effective scaffolding provided by animated content.
Possibly fueling this blunted effect was a sharp drop in FC
between VP-L involving fusiform and superior/middle tem-
poral areas and intraparietal sulcus (IPS), well-described col-
laborators in visual-language association (Price 2012;Ardila
et al. 2015), and marginal decreases between VI-L and DMN-
L. Within-network FC in the VP network was attenuated by
less inter-hemispheric connectivity and lower FC between pri-
mary visual and fusiform areas. FC for visual perception has
been shown to be more focal in primary visual areas than
during image retrieval (i.e. imagery), consistent with this find-
ing (Seidkhani et al. 2017). Altogether, these findings suggest
a bias towards focal visual perception for animation relative to
the other formats, which may occupy constrained neural re-
sources at this age such that integration with language, imag-
ery, and other higher-order networks is less favorable.
The possibility that animated story presentation may hyper-
stimulate visual perception networks at the expense of their
Fig. 4 Changes in functional connectivity between visual imagery
and language networks in animated format relative to illustration.
FC was decreased 49%, with 52% of the decrease involving inter-
hemispheric connections, 24% involving the left hemisphere, and 24%
involving the right hemisphere. Blue lines designate significantly
decreased pair-wise connections (100%). Nodes represent regions of
interest, with blue reflecting negative contribution to FC change, and
white reflecting no change, depth of color reflecting magnitude of
effect. Post hoc analyses were performed using 2-tailed t-tests, with
analysis-level FDR correction, p<0.05
Brain Imaging and Behavior
Author's personal copy
integration with higher-order cognitive networks is consistent
with our finding of globally decreased FC between all net-
works for animated format relative to illustration (13% to
82%; Table 2). Interestingly, such a decrease did not occur
for illustration relative to audio and was less pronounced for
animation relative to audio, suggesting a complex, non-linear
effect. For animation relative to illustration, sharply lower FC
between VI-L involving the IPS (Fig. 4) and DMN-L involv-
ing precuneus (Huijbers et al. 2011), are consistent with de-
creased recruitment of imagery for this contrast (Just et al.
2004; Price 2012). Similarly, the precipitous drop involving
VP-L (82%) concentrated in fusiform and superior/middle
temporal/IPS is consistent with decreased imagery, given the
overlapping functional role of VP for image retrieval (Ardila
et al. 2015). In addition to imagery effects, decreases in FC
between VP-DMN suggest diminished self-referential pro-
cessing during animation relative to the other formats
(Molnar-Szakacs and Uddin 2013;Xiaoetal.2015).
Antagonism between the DMN and task-positive, especially
visual, networks is well-documented (Uddin et al. 2009;
Raichle 2015). However, Raichle proposed a model of
DMN/task-positive integration where a Bsense of self^is ap-
plied to the task (Raichle 2015). It is possible that illustration
provides a moderate level of visual stimulation to not interfere
with this self-referential aspect of story sharing (e.g. Fig. 3),
manifest in children as introspection, or sense of wonder. By
contrast, diminished DMN engagement during animated con-
tent seems consistent with absent screen gazing often noted in
children watching cartoons. The DMN is a core network as-
sociated with numerous aspects of higher-order cognitive
function and long-term mental health, including imagery
(Daselaar et al. 2010), memory consolidation (Mohan et al.
2016), and creativity (De Pisapia et al. 2016). Thus, these
findings related to potential effects of story format on DMN
recruitment and integration, seem important for further study.
While classically associated with motor skills, the cerebel-
lum is increasingly recognized as playing a supporting role in
language and other cognitive functions (Stoodley 2012;
Buckner 2013), including a proposed Bturbocharger^effect
during story listening (Hutton et al. 2017a,b). Increased FC
between CB-VP for illustration relative to audio and broadly
attenuated cerebellar FC during animation align with this role,
suggesting cerebellar engagement proportional to the level of
cognitive work required. Lower comprehension scores for an-
imation relative to other formats suggest a more passive, per-
haps less Bturbocharged^experience, though our assessment
was rudimentary. As decreased cerebellar engagement has
been associated with deficits in skill refinement and learning
(Guell et al. 2015), it is possible that lower FC involving CB
during animation reflects sub-optimal neural configuration for
the application and refinement of imagery and related skills,
though our cross-sectional design cannot discern such effects.
By contrast, it is intriguing to speculate that higher cerebellar
FC during illustrated format may reflect more favorable neural
configuration for the practice of such skills at this age.
Altogether, our findings suggest that neurobiological
mechanisms underlying animated story processing are sub-
stantially different from audio and especially illustrated for-
mats in preschool-age children. The moderate level of visual
stimulus contributed by illustrations may provide age-
appropriate scaffolding to generate imagery and assist the lan-
guage network, an integrative skill reinforced by cerebellar
association areas. This is consistent with the age-old appeal
of illustrated storybooks books for young children, their well-
documented potential to fuel imagery and comprehension
(Levin 1972;GambrellandJawitz1993; Gambrell and
Koskinen 2002), and Bruner/Vygosky theories of learning
(Wertsch 1980;Christakisetal.2007). While a precise defi-
nition has not yet been determined, the FC pattern observed
during illustrated format may be optimal in terms of general
principles of healthy brain networks, notably robust connec-
tivity between functional modules supporting higher-order
skills (Bullmore and Sporns 2012). By contrast, FC patterns
during audio alone suggest greater strain in the language net-
work and less well-integrated scaffolding, potentially attribut-
able to less efficient access to images referenced in the narra-
tive at this age. At the other extreme, by providing a stream of
fast-moving visual content, animated story format may more
broadly suppress the integration of language and higher-order
brain networks such as imagery and Default Mode, which
may be suboptimal for the developing brain.
Our study has limitations. Our results are in terms of mean
FC during each format, while dynamic FC analyses may re-
veal other differences. The stories used were by the same
author with a particular style, and our findings may not apply
to other styles. We view this as a worthwhile tradeoff,
allowing us to control for important narrative variables across
formats. The three stories used were different, presented in the
same order for each child. However, this design eliminated the
confound of repeat exposure to the same story likely to make
subsequent trials less interesting, or easier. Gradually increas-
ing visual stimulus also minimized visual priming effects,
while addressing concerns about the potential of animated
content to negatively affect performance on subsequent tasks
at this age (Lillard and Peterson 2011 and Lillard et al. 2015).
Given technological constraints, shared reading during MRI is
not currently feasible. However, audio and animation were
presented in a reasonably ecological way (headphones and
screen), and we suspect that greater differences between illus-
trated and other formats would manifest on a parentslap.Our
sample size was relatively small (27), though respectable es-
pecially given the young age of our sample population, and
exceeding sample sizes in recently published, connectivity-
based analyses involving functional networks and continuous
task paradigms (Bray et al. 2015;Horowitz-Krausetal.2018;
Web e r e t al. 2018). Our assessment of story recall was
Brain Imaging and Behavior
Author's personal copy
rudimentary and administered to only 14 of 27 children,
though its finding of equivalent interest and significantly low-
er scores for the animated story provides useful insights into
our MRI results. Our sample involved Caucasian, largely
higher-SES children, though general mechanisms of neural
processing seem unlikely to be influenced by race, and SES-
related covariates did not significantly influence our results.
Our analyses were limited to five functional networks, though
thesewererigorouslydetermined affording a hypothesis-
driven approach that increased our statistical power. Our net-
works were largely defined in terms of Brodmann Areas, with
some included in more than one network, yet refined via an
established parcellation approach (Craddock et al. 2012).
Our study also has important strengths. Our fMRI para-
digm involved continuous story presentation akin to the real
world, resulting in a high success rate in very young children.
Our analyses involved an innovative, connectivity-based ap-
proach affording comparisons of functional networks in ag-
gregate and at the ROI level, which aligns with the current
shift away from modular views of brain function towards
network-level analyses (Sporns 2013). Our hypothesis was
in the context of documented benefits of shared reading
(National Early Literacy Panel 2008,Huttonetal.2015)and
concerns about animated content in young children (Chiong
et al. 2012; Parish-Morris et al. 2013; Lillard et al. 2015).
While highly preliminary, our findings provide novel, neuro-
biological insights into these cited benefits and risks, and cor-
responding AAP recommendations (AAP Council on Early
Childhood et al. 2014; AAP Council on Communications
and Media 2016). Longitudinal studies involving comprehen-
sive behavioral measures are needed to explore whether short-
term effects observed in our study result in long-term differ-
ences in these networks and the skills they support, notably
reading abilities. These are critical questions in the context of
achildsearlyBcognitive ecosystem,^where unprecedented
technological shifts influence how content is provided in the
digital age.
Conclusions
This study revealed substantial differences in the functional
connectivity of visual, language, Default Mode, and cerebellar
brain networks during stories presented in audio, illustrated,
and animated format in preschool-age children. Illustrated for-
mat was associated with reduced strain on the language net-
work and maximal integration of visual perception, imagery,
Default Mode, and cerebellar networks, suggesting a novel
neurobiological correlate of the well-documented appeal of
childrens picture books to provide scaffolding for language
and learning. By contrast, audio alone may provide subopti-
mal scaffolding at this age to catalyze such integration, and
continuous animated content may render it less favorable,
with a bias towards focal visual perception. As higher-order
skills require practice, particularly in the home environment,
our findings raise important questions regarding the influence
of story format on the development and integration of func-
tional brain networks, and provide insights for further
research.
Acknowledgments The authors would like to thank Christy Banks for
coordinating recruitment and administration of our fMRI protocol, and
Dr. Jennifer Vannest for providing critique of early drafts of this manu-
script. We thank Robert Munsch for his writing and storytelling, and
permission to use audio and video versions used in this research. We
finally thank the Thrasher Research Fund for their support of early-
career investigators and this work.
Contributorsstatement John S. Hutton designed all aspects of the
study including brain network selection and definition, collaborated in
analyses, drafted the initial manuscript and subsequent revisions, and
approved the final manuscript as submitted.
Jonathan Dudley conducted brain network parcellation and all fMRI
and other statistical analyses used in this study, created all tables and
figures, assisted with manuscript preparation and revision, and approved
the final manuscript as submitted.
Tzipi Horowitz-Kraus provided guidance on study design and anal-
ysis, assisted with MRI acquisition, reviewed and revised the manuscript,
and approved the final manuscript as submitted.
Tom DeWitt provided guidance on study design, analysis, and pre-
sentation, reviewed and revised the manuscript, and approved the final
manuscript as submitted.
Scott K. Holland provided guidance on study design and presenta-
tion, developed the concept for the a priori network connectivity approach
used in the analysis, helped develop and oversaw the MRI acquisition
protocol, and reviewed and approved the final manuscript as submitted.
Funding source This study was funded by a grant from the Thrasher
Research Fund with additional support provided via a Ruth L Kirschstein
National Research Service Award (Hutton).
Compliance with ethical standards
Conflict of interest Drs. Hutton, Dudley, Horowitz-Kraus, DeWitt, and
Holland declare that they have no conflict of interest.
Informed consent All procedures followed were in accordance withthe
ethical standards of the responsible committee on human experimentation
(institutional and national) and with the Helsinki Declaration of 1975, and
the applicable revisions at the time of the investigation. Informed consent
was obtained from all patients for being included in the study.
Financial disclosure The authors have no financial relationships rele-
vant to this article to disclose.
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Brain Imaging and Behavior
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... Most importantly, the usage time and contents should not impact children's time for sleep, physical activity, and other activities related to health (American Academy of Pediatrics, 2016). Recent studies indicated that the usage of tablets may risk a negative impact on children's early neurological and physiological development (Anderson et al., 2017;Horowitz-Kraus & Hutton, 2018;Hutton et al., 2020;Paulus et al., 2019;Zivan et al., 2019). For instance, more screen time was associated with decreased functional connectivity between regions related to language (Hutton et al., 2020), visual perception (Horowitz-Kraus & Hutton, 2018), and visual-attention abilities (Zivan et al., 2019). ...
... Recent studies indicated that the usage of tablets may risk a negative impact on children's early neurological and physiological development (Anderson et al., 2017;Horowitz-Kraus & Hutton, 2018;Hutton et al., 2020;Paulus et al., 2019;Zivan et al., 2019). For instance, more screen time was associated with decreased functional connectivity between regions related to language (Hutton et al., 2020), visual perception (Horowitz-Kraus & Hutton, 2018), and visual-attention abilities (Zivan et al., 2019). The language, visual perception, and visual-attention abilities are crucial for the cognitive development (Anderson et al., 2017). ...
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This study aims to investigate the relationships between touchscreen tablet usage time and attention performance in preschool children. Seventy-five young children with typical development were recruited. The accuracy rate and reaction time of their attention performance improved with age. Significant differences in accuracy rates, reaction time, and executive attention performance between young children who use touchscreen tablets more or less often were observed. Children who spent more time using touchscreen tablets had better accuracy rates and faster reaction time in the Attentional Network Task test. However, children who spent more time on tablets performed slower in terms of executive attention. These findings add to the understanding of the experience of using touchscreen tablets and its relationship with the attention performance of young children.
... For example, EEG responses to brief cartoon movies have been successfully collected in 7-month-olds using multivariate temporal response functions, thus validating the use of this naturalistic paradigm in a pediatric sample (Jessen, Fiedler, Münte, & Obleser, 2019). fMRI has also been used to study language-related brain function in pre-school children (4-to-6-year-olds) using story-listening tasks (Hutton et al., 2017(Hutton et al., , 2020Romeo et al., 2018). Neural patterns evoked during naturalistic viewing correlate with developmental behavioral measures such as children's language exposure at home (King et al., 2021;Romeo et al., 2018), mother-child reading behavior (Hutton et al., 2017), episodic memory skills (Cantlon & Li, 2013), social cognitive scores (Richardson, Lisandrelli, Riobueno-Naylor, & Saxe, 2018) and attention abilities (Moraczewski, Chen, & Redcay, 2018). ...
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Understanding language neurobiology in early childhood is essential for characterizing the developmental structural and functional changes that lead to the mature adult language network. In the last two decades, the field of language neurodevelopment has received increasing attention, particularly given the rapid advances in the implementation of neuroimaging techniques and analytic approaches that allow detailed investigations into the developing brain across a variety of cognitive domains. These methodological and analytical advances hold the promise of developing early markers of language outcomes that allow diagnosis and clinical interventions at the earliest stages of development. Here, we argue that findings in language neurobiology need to be integrated within an approach that captures the dynamic nature and inherent variability that characterizes the developing brain and the interplay between behavior and (structural and functional) neural patterns. Accordingly, we describe a framework for understanding language neurobiology in early development, which minimally requires an explicit characterization of the following core domains: i) computations underlying language learning mechanisms, ii) developmental patterns of change across neural and behavioral measures, iii) environmental variables that reinforce language learning (e.g., the social context), and iv) brain maturational constraints for optimal neural plasticity, which determine the infant's sensitivity to learning from the environment. We discuss each of these domains in the context of recent behavioral and neuroimaging findings and consider the need for quantitatively modeling two main sources of variation: individual differences or trait-like patterns of variation and within-subject differences or state-like patterns of variation. The goal is to enable models that allow prediction of language outcomes from neural measures that take into account these two types of variation. Finally, we examine how future methodological approaches would benefit from the inclusion of more ecologically valid paradigms that complement and allow generalization of traditional controlled laboratory methods.
... Moreover, younger and younger children have their own electronic devices, which they have at their fingertips in their bedrooms, completely beyond parental control [26]. Scientists agree that handheld devices delay speech development and other forms of communication in young children [27,28]. The young users, often busy with replying to received messages, do not realise the lateness of the hour, and the agitation resulting both from the chats and light from the screens causes disturbances in the daily sleep rhythm of children and adolescents [29]. ...
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The number of children using portable electronic devices and the Internet has been on the increase in recent years. This study aimed to analyse how the overuse of various types of electronic devices and the Internet interfere with the sleep patterns and lifestyle of children and adolescents. This study group included 376 participants (189 girls, 187 boys) aged 6–15. The body composition estimates were obtained by means of a foot-to-foot bioelectrical impedance analysis whereas the body height was measured with the use of a stadiometer. The questionnaire survey consisted of questions concerning the children’s lifestyle, new media use, eating and sleeping habits, their physical activity as well as their socio-demographic data. The correlation of the two variables was calculated with the Spearman rank correlation coefficient. Correspondingly, the odds ratio (OR) and 95% confidence intervals (CIs) were measured. This study indicated that the use of the media resulted in a significant drop in the study group’s physical activity but also had a negative association with their sleeping and eating habits. In conclusion, health professionals ought to provide parents with more guidance on appropriate new media use.
... It has been shown, in addition, that increased activity in small children's executive and auditory-visual networks during narratives' comprehension predicts their later reading ability ( Horowitz-Kraus et al., 2013 ). In parallel with this, illustrated stories seem to support language development in preschool-age children by reducing reliance on the brain's language networks ( Hutton et al., 2018 ). Finally, naturalistic studies have demonstrated that a second language acquired early in life is processed similarly to the first language, even if acquired passively ( Bloch et al., 2009 ). ...
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Using movies and narratives as naturalistic stimuli in human neuroimaging studies has yielded significant advances in understanding of cognitive and emotional functions. The relevant literature was reviewed, with emphasis on how the use of naturalistic stimuli has helped advance scientific understanding of human memory, attention, language, emotions, and social cognition in ways that would have been difficult otherwise. These advances include discovering a cortical hierarchy of temporal receptive windows, which supports processing of dynamic information that accumulates over several time scales, such as immediate reactions vs. slowly emerging patterns in social interactions. Naturalistic stimuli have also helped elucidate how the hippocampus supports segmentation and memorization of events in day-to-day life and have afforded insights into attentional brain mechanisms underlying our ability to adopt specific perspectives during natural viewing. Further, neuroimaging studies with naturalistic stimuli have revealed the role of the default-mode network in narrative-processing and in social cognition. Finally, by robustly eliciting genuine emotions, these stimuli have helped elucidate the brain basis of both basic and social emotions apparently manifested as highly overlapping yet distinguishable patterns of brain activity.
... In terms of functional activations, functional Magnetic Resonance Imaging (fMRI) has been used to show that newborns and young infants bilaterally activate fronto-temporal areas with a right predominance in the auditory cortices when presented with infant-directed speech (Dehaene et al., 2002(Dehaene et al., , 2006Perani et al., 2011). Older children between 5 and 6 years of age exhibit left fronto-temporal functional activations during passive story listening paradigms (Hutton et al., 2018;Romeo et al., 2018, see also Weiss-Croft & Baldeweg 2015, for a systematic review on the maturation of language networks based on fMRI studies). Taken together, these studies show that the gradual development of language abilities from early perception to word production and lexical and morphosyntactic learning is supported by the progressive development and maturation of the language brain network (Catani & Bambini, 2014). ...
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Brain imaging methods such as functional Magnetic Resonance Imaging (fMRI) and Diffusion Tensor Imaging (DTI) have already been used to decipher the functional and structural brain changes occurring during normal language development. However, little is known about the differentiation of the language network after an early lesion. While in adults, stroke over the left hemisphere generally induces post-stroke aphasia, it is not always the case when a stroke occurs in the perinatal period, thus revealing a remarkable plastic power of the language network during early development. In particular, the role of perilesional tissues, as opposed to undamaged brain areas in the functional recovery of language functions after an early insult, remains unclear. In this review article, we provide an overview of the extant literature using functional and structural neuroimaging data revealing the signatures of brain plasticity underlying near-normal language development.
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Objective To explore relationship between EEG theta activity and clinical data that imply the degree of genetic determination of epilepsy. Methods Clinical data of interest were epilepsy diagnosis and positive / negative family history of epilepsy. Study groups were: idiopathic generalized epilepsy (IGE), focal epilepsy (FE); FE of unknown etiology (FEUNK), FE of postnatal-acquired etiology (FEPA); all patients with positive / negative family history of epilepsy (FAPALL, FANALL, respectively), disregarding of the syndrome; FAP patients with 1st degree affected relative (FAP1) and those with 2nd degree epileptic relative only (FAP2). Quantitative EEG analysis assessed amount of theta (3.5-7.0 Hz) activity in 180 seconds of artifact-free waking EEG background activity for each patient and group. Group comparison was carried out by nonparametric statistics. Results Differences of theta activity were: FAPALL > FANALL (p=0.01); FAP1 > FAP2 (p=0.2752). IGE > FE (p=0.02); FEUNK > FEPA (p=0.07). Conclusions This was the first attempt to explore and quantitatively ascertain relationship between an EEG variable and clinical data that imply greater or lesser degree of genetic determination in epilepsy. Significance Theta activity is endophenotype that bridges the gap between epilepsy susceptibility genes and clinical phenotypes. Amount of theta activity is indicative of degree of genetic determination of the epilepsies.
Chapter
The chapter examines how oral story listening affects visualization skills (also referred to as mental representations). It is known that children who visualize when reading comprehend better than those who don’t. Preliterate children who listen to oral stories co-construct the narrative using visualization, just as fluent readers co-create stories they read. Structure and elements of traditional narratives, and how oral storytelling is delivered, suggest why young listeners visualize. Listeners use memories and knowledge resulting in narrative that is personal and deeply understood, as suggested in reader response theory. The chapter continues discussions comparing oral storytelling and shared picture book reading.
Chapter
Using classroom observation, interviews, and current research, both qualitative and quantitative, this chapter examines the focus children display when listening to oral stories. The authors propose that oral story listening contributes to the ability of students to focus (including those with attention issues), and explore scientific explanations for this. These include use of folk tales following the classic narrative arc, and physical responses when listening to narratives. Recent neurological studies on the development of the “narrative” or “reading” brain are also discussed. Together these demonstrate how, like shared reading, oral story listening helps in unique ways to develop emergent literacy skills including vocabulary and narrative understanding.
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Importance Literacy has been described as an important social determinant of health. Its components emerge in infancy and are dependent on genetic, medical, and environmental factors. The American Academy of Pediatrics advocates a substantial role for pediatricians in literacy promotion, developmental surveillance, and school readiness to promote cognitive, relational, and brain development. Many children, especially those from minority and underserved households, enter kindergarten unprepared to learn to read and subsequently have difficulty in school. Observations Emergent literacy is a developmental process beginning in infancy. Component skills are supported by brain regions that must be adequately stimulated and integrated to form a functional reading network. Trajectories are associated with genetic, medical, and environmental factors, notably the home literacy environment, which is defined as resources, motivation, and stimulation that encourage the literacy development process. Eco-biodevelopmental models are advocated by the American Academy of Pediatrics, and these models offer insights into the neurobiological processes associated with environmental factors and the ways in which these processes may be addressed to improve outcomes. Emergent literacy is well suited for such a model, particularly because the mechanisms underlying component skills are elucidated. In addition to cognitive-behavioral benefits, the association of home literacy environment with the developing brain before kindergarten has recently been described via neuroimaging. Rather than a passive approach, which may subject the child to stress and engender negative attitudes, early literacy screening and interventions that are administered by pediatric practitioners can help identify potential reading difficulties, address risk factors during a period when neural plasticity is high, and improve outcomes. Conclusions and Relevance Neuroimaging and behavioral evidence inform an eco-biodevelopmental model of emergent literacy that is associated with genetic, medical, and home literacy environmental factors before kindergarten, a time of rapid brain development. This framework is consistent with recommendations from the American Academy of Pediatrics and provides insights to help identify risk factors and signs of potential reading difficulties, tailor guidance, and provide direction for future research.
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Network neuroscience is a thriving and rapidly expanding field. Empirical data on brain networks, from molecular to behavioral scales, are ever increasing in size and complexity. These developments lead to a strong demand for appropriate tools and methods that model and analyze brain network data, such as those provided by graph theory. This brief review surveys some of the most commonly used and neurobiologically insightful graph measures and techniques. Among these, the detection of network communities or modules, and the identification of central network elements that facilitate communication and signal transfer, are particularly salient. A number of emerging trends are the growing use of generative models, dynamic (time-varying) and multilayer networks, as well as the application of algebraic topology. Overall, graph theory methods are centrally important to understanding the architecture, development, and evolution of brain networks.
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This study investigates the dynamics of attention during continuous, naturalistic interactions in a video game. Specifically, the effect of repeated distraction on a continuous primary task is related to a functional model of network connectivity. We introduce the Nonlinear Attentional Saturation Hypothesis (NASH), which predicts that effective connectivity within attentional networks increases nonlinearly with decreasing distraction over time, and exhibits dampening at critical parameter values. Functional Magnetic Resonance Imaging (fMRI) data collected using a naturalistic behavioral paradigm coupled with an interactive video game is used to test the hypothesis. As predicted, connectivity in pre-defined regions corresponding to attentional networks increases as distraction decreases. Moreover, the functional relationship between connectivity and distraction is convex, that is, network connectivity somewhat increases as distraction decreases during the continuous primary task, however, connectivity increases considerably as distraction falls below critical levels. This result characterizes the nonlinear pattern of connectivity within attentional networks, particularly with respect to their dynamics during behavior. These results are also summarized in the form of a network structure analysis, which underscores the role of various nodes in regulating the global network state. In conclusion, we situate the implications of this research in the context of cognitive complexity and an emerging theory of flow during media exposure.
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Throughout recorded history, and across cultures, humans have made visual art. In recent years, the neural bases of creativity, including artistic creativity, have become a topic of interest. In this study we investigated the neural bases of the visual creative process with both professional artists and a group of control participants. We tested the idea that creativity (planning an artwork) would influence the functional connectivity between regions involved in the default mode network (DMN), implicated in divergent thinking and generating novel ideas, and the executive control network (EN), implicated in evaluating and selecting ideas. We measured functional connectivity with functional Magnetic Resonance Imaging (fMRI) during three different conditions: rest, visual imagery of the alphabet and planning an artwork to be executed immediately after the scanning session. Consistent with our hypothesis, we found stronger connectivity between areas of the DMN and EN during the creative task, and this difference was enhanced in professional artists. These findings suggest that creativity involves an expert balance of two brain networks typically viewed as being in opposition.
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Several researchers have reported that instructing participants to imagine items using the Deese-Roediger-McDermott (DRM) paradigm lowers false memory rates (Foley, Wozniak, & Gillum, 2006). However, other researchers have found that imagery does not always lower false memory rates (Robin, 2010), and investigators have examined the effects of imagery manipulation on semantic but not phonological lists. In the present study, we presented 102 participants with semantic and phonological DRM lists, followed by a free recall test and final recognition test. Some participants received instructions to imagine list items during the study phase to facilitate memory, and others were simply told to remember list items. Imagery instructions enhanced correct memories and further suggested a trend for decreased false memories. A test type by list type interaction also emerged, with phonological lists eliciting higher false memories at recall, and semantic lists eliciting higher false memories at recognition. Directions for future research are discussed.
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The role of the parent or educator in a child’s learning is a key feature in child development. Evidence supports the impact of early language exposure for future language and cognitive abilities and of home reading environment on neural circuits supporting language and reading. As shared parent–child reading is largely contingent on the reading ability of the parent, the aim of the current study was to explore association of parental reading ability on functional connectivity of brain networks involved with reading acquisition in their children. Twenty-two 4-year-old girls and their mothers participated in the current study. Maternal reading fluency was applied as predictors of functional connectivity analyses of a stories-listening functional MRI task. Results indicate a positive association between maternal fluency scores and greater functional connectivity between regions in the future reading network and brain regions supporting language and cognitive control in the children. Maternal reading fluency is important in facilitating development of a child’s reading network. Implications regarding shared reading are discussed, and an extended ecological model for child language and literacy development is proposed.
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Objective: To explore the relationship between maternal shared reading quality (verbal interactivity and engagement) and brain function during story listening in at-risk, preschool-age children, in the context of behavioral evidence and American Academy of Pediatrics, recommendations. Study design: In this cross-sectional study, 22 healthy, 4-year-old girls from low socioeconomic status households completed functional magnetic resonance imaging using an established story listening task, followed by videotaped observation of uncoached mother-daughter reading of the same, age-appropriate picture book. Shared reading quality was independently scored applying dialogic reading and other evidence-based criteria reflecting interactivity and engagement, and applied as a predictor of neural activation during the functional magnetic resonance imaging task, controlling for income and maternal education. Results: Shared reading quality scores were generally low and negatively correlated with maternal distraction by smartphones (P < .05). Scores were positively correlated with activation in left-sided brain areas supporting expressive and complex language, social-emotional integration, and working memory (P <.05, false discovery rate corrected). Conclusions: Maternal shared reading quality is positively correlated with brain activation supporting complex language, executive function, and social-emotional processing in at-risk, preschool-age children. These findings represent novel neural biomarkers of how this modifiable aspect of home reading environment may influence foundational emergent literacy skills, reinforce behavioral evidence and American Academy of Pediatrics, recommendations, and underscore the potential of dialogic reading interventions to promote healthy brain development, especially in at-risk households.
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In free visual exploration, eye-movement is immediately followed by dynamic reconfiguration of brain functional connectivity. We studied the task-dependency of this process in a combined visual search-change detection experiment. Participants viewed two (nearly) same displays in succession. First time they had to find and remember multiple targets among distractors, so the ongoing task involved memory encoding. Second time they had to determine if a target had changed in orientation, so the ongoing task involved memory retrieval. From multichannel EEG recorded during 200 ms intervals time-locked to fixation onsets, we estimated the functional connectivity using a weighted phase lag index at the frequencies of theta, alpha, and beta bands, and derived global and local measures of the functional connectivity graphs. We found differences between both memory task conditions for several network measures, such as mean path length, radius, diameter, closeness and eccentricity, mainly in the alpha band. Both the local and the global measures indicated that encoding involved a more segregated mode of operation than retrieval. These differences arose immediately after fixation onset and persisted for the entire duration of the lambda complex, an evoked potential commonly associated with early visual perception. We concluded that encoding and retrieval differentially shape network configurations involved in early visual perception, affecting the way the visual input is processed at each fixation. These findings demonstrate that task requirements dynamically control the functional connectivity networks involved in early visual perception.
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Infants, toddlers, and preschoolers are now growing up in environments saturated with a variety of traditional and new technologies, which they are adopting at increasing rates. Although there has been much hope for the educational potential of interactive media for young children, accompanied by fears about their overuse during this crucial period of rapid brain development, research in this area still remains limited. This policy statement reviews the existing literature on television, videos, and mobile/interactive technologies; their potential for educational benefit; and related health concerns for young children (0 to 5 years of age). The statement also highlights areas in which pediatric providers can offer specific guidance to families in managing their young children's media use, not only in terms of content or time limits, but also emphasizing the importance of parent-child shared media use and allowing the child time to take part in other developmentally healthy activities.
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Expanding behavioral and neurobiological evidence affirms benefits of shared (especially parent-child) reading on cognitive development during early childhood. However, the majority of this evidence involves factors under caregiver control, the influence of those intrinsic to the child, such as interest or engagement in reading, largely indirect or unclear. The cerebellum is increasingly recognized as playing a “smoothing” role in higher-level cognitive processing and learning, via feedback loops with language, limbic and association cortices. We utilized functional MRI to explore the relationship between child engagement during a mother-child reading observation and neural activation and connectivity during a story listening task, in a sample of 4-year old girls. Children exhibiting greater interest and engagement in the narrative showed increased activation in right-sided cerebellar association areas during the task, and greater functional connectivity between this activation cluster and language and executive function areas. Our findings suggest a potential cerebellar “boost” mechanism responsive to child engagement level that may contribute to emergent literacy development during early childhood, and synergy between caregiver and child factors during story sharing.
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The relationship of cortical structure and specific neuronal circuitry to global brain function, particularly its perturbations related to the development and progression of neuropathology, is an area of great interest in neurobehavioral science. Disruption of these neural networks can be associated with a wide range of neurological and neuropsychiatric disorders. Herein we review activity of the Default Mode Network (DMN) in neurological and neuropsychiatric disorders, including Alzheimer’s disease, Parkinson’s disease, Epilepsy (Temporal Lobe Epilepsy - TLE), attention deficit hyperactivity disorder (ADHD), and mood disorders. We discuss the implications of DMN disruptions and their relationship to the neurocognitive model of each disease entity, the utility of DMN assessment in clinical evaluation, and the changes of the DMN following treatment.