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abstract BACKGROUND AND OBJECTIVES: Parent-child reading is widely advocated to promote cognitive
development, including in recommendations from the American Academy of Pediatrics to begin
this practice at birth. Although parent-child reading has been shown in behavioral studies to
improve oral language and print concepts, quantifiable effects on the brain have not been
previously studied. Our study used blood oxygen level–dependent functional magnetic
resonance imaging to examine the relationship between home reading environment and brain
activity during a story listening task in a sample of preschool-age children. We hypothesized that
while listening to stories, children with greater home reading exposure would exhibit higher
activation of left-sided brain regions involved with semantic processing (extraction of meaning).
METHODS: Nineteen 3- to 5-year-old children were selected from a longitudinal study of normal
brain development. All completed blood oxygen level–dependent functional magnetic
resonance imaging using an age-appropriate story listening task, where narrative alternated
with tones. We performed a series of whole-brain regression analyses applying composite,
subscale, and individual reading-related items from the validated StimQ-P measure of home
cognitive environment as explanatory variables for neural activation.
RESULTS: Higher reading exposure (StimQ-P Reading subscale score) was positively correlated (P ,
.05, corrected) with neural activation in the left-sided parietal-temporal-occipital association
cortex, a “hub” region supporting semantic language processing, controlling for household income.
CONCLUSIONS:In preschool children listening to stories, greater home reading exposure is
positively associated with activation of brain areas supporting mental imagery and narrative
comprehension, controlling for household income. These neural biomarkers may help inform
eco-bio-developmental models of emergent literacy.
a
WHAT’S KNOWN ON THIS SUBJECT: The American Division of General and Community Pediatrics, bPediatric Neuroimaging Research Consortium, cCommunication
Sciences Research Center, and dDivision of Radiology, Cincinnati Children’s Hospital Medical Center, Cincinnati,
Academy of Pediatrics recommends parent-child Ohio; and eDepartment of Pediatrics, New York University School of Medicine and Bellevue Hospital Center, New
reading from infancy through at least York, New York
kindergarten, the span of maximal brain growth. Dr Hutton conceptualized and designed the study, performed all data analysis, and drafted the
Home literacy environment, including reading initial manuscript and subsequent revisions; Dr Horowitz-Kraus provided guidance on study design
behaviors and access to books, has been shown and analysis, assisted with coordination of data collection, and reviewed and revised the
manuscript; Dr Mendelsohn served as national outside facilitator and mentor for this project,
to promote oral language and print concepts. provided advice on the use of the StimQ measure, and reviewed and revised the manuscript;
Dr DeWitt provided guidance on the study design and reviewed and revised the manuscript;
WHAT THIS STUDY ADDS: Home reading
Dr Holland designed and secured funding for the parent neuroimaging study and acquired imaging
environment is positively associated with activation and behavioral data in all participants; he was also responsible for image and behavioral data
of brain areas supporting narrative comprehension quality control, database archiving and first-level analysis of fMRI data and participated in the study
and mental imagery in preschool children. This design for addition of reading measures and supervised collection of the StimQ questionnaire; and
all authors approved the final manuscript as submitted.
offers novel insight into the neurobiological
foundations of emergent literacy and potential
effect of shared reading during early childhood.
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September 2015 467
initiation of reading to their child, statistical threshold of P , .05, TABLE 1 Demographic Characteristics of
which is not included in the StimQ-P. applying a false discovery rate (FDR) C-MIND Sample Subjects
correction for multiple voxel Characteristic n %
fMRI Acquisition Specifications and comparisons across the brain. Using Sample 19 100
Preliminary Analyses these, we obtained a whole-brain, Age (y)
Details of techniques used to group mean activation map for our 19 3+ 10 52
4+ 6 32
acclimatize children to the MRI subjects, representing mean neural
5+ 3 16
acquisition process are described by activation listening to stories, minus Gender
Vannest et al.32 Details of BOLD MRI activation listening to tones (ie, Male 8 42
acquisition specifications used in the activation attributable to the story Female 11 58
C-MIND study are described in task, excluding general acoustic Annual household income (US$)
,5000 0 0
Schmithorst et al.35,48 Details of data processing).
5000–10 000 1 5
preprocessing for the C-MIND study 10–15 000 1 5
are described in Sroka et al.49 All Regression With StimQ-P and Other 15 000–25 000 2 11
children were awake and nonsedated Predictors 25 000–35 000 1 5
during MRI scans. Voxel size used for 35 000–50 000 2 11
For each subject, the z score map 50 000–75 000 4 21
acquisition and analysis was 3 3 3 3 representing the contrast of (stories 75 000–100 000 4 21
4 mm. We used the FEAT (fMRI Expert . tones) was used as the dependent 100 000–150 000 2 11
Analysis Tool) modality of FSL (fMRI- variable in a series of “higher-level” .150 000 2 11
Brain Software Library, Oxford, United regression analyses, applying StimQ-P Household income level
Kingdom) for all group mean and Below 200% poverty (low) 7 37
scores (Reading, PIDA, PVR, Above 200% poverty 12 63
higher-level regression analyses.50 Composite) or responses to individual Children in the household
questions as the explanatory variable. 1 3 16
fMRI Story Listening Task and Group 2–3 12 63
Mean Analysis Income category (low/not low) was
applied as a binary covariate when 4–5 3 16
The story listening task consists of 10 6 1 5
significant neural activation was
alternating blocks of active and found, with household income
control conditions (5 each) of 64 ,200% of the 2015 Federal Poverty StimQ-P and Other Behavioral
seconds’ duration. During the “active” Guidelines,51 adjusted for household Predictors
condition, a series of 5 recorded size, defined as low income (see
stories of 9 to 10 sentences each read A summary of StimQ-P subscale and
Table 1).52 Subject age and gender
in a female voice was presented via composite scores, and reported age of
were considered as covariates but
headphones. The stories were initiation of shared reading are
excluded because no significant
designed by a speech pathologist with described in Table 2 and Fig 1.
correlation was found between neural
consistent vocabulary and syntax activation and either variable.
appropriate for young children Group Mean Activation for the
Regression maps of neural activation
(download: https://www.irc.cchmc. Narrative Comprehension Task
(stories . tones), along with
org/software/pedaudio.php). The summary statistics for size, intensity, Group mean activation for the
control condition consisted of and location of activation clusters, narrative condition compared with
nonspeech tones in a range of were reported for all significant baseline tones (all voxels P , .05,
frequencies simulating human speech results, using a threshold for FDR correction) involved bilateral,
to control for baseline acoustic statistical significance of P , .05 left-lateralized cortical and
processing. Subjects closed their eyes applying FDR correction. The subcortical regions involved with
or saw a blank screen during scanning. FSLView50 package was used to acoustic, phonological, and semantic
During task presentation, the MRI identify brain areas corresponding to language processing (see Fig 2), as
scanner continuously acquired BOLD- active clusters in normalized, three- described by Karunanayaka et al.54
weighted scans, covering the entire dimensional, Montreal Neurologic
brain with 24 slices at 4-second Institute (MNI) coordinate space,53 Regression of Neural Activation With
intervals. Image time series data were using the Harvard-Oxford Cortical StimQ-P Scores and Other Predictors
entered into a general linear model Structural Atlas (2-mm scale). Applying linear regression, StimQ-P
for “first-level,” voxelwise analysis, Reading subscale scores were
using the story and tone intervals as positively correlated with higher
the regressor of interest. Contrast RESULTS activation in a confluent region of left-
maps (stories . tones activation) Demographic characteristics for our sided, posterior cortex involving the
were converted to z score maps with sample are described in Table 1. occipital fusiform, lateral occipital,
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September 2015 469
FIGURE 2
Group mean activation map for the story listening task. Group mean BOLD fMRI activation map (stories . tones) in 3- to 5-year-old children (N = 19). All
voxels significant at P , .05 (FDR corrected), slice thickness 5 mm for contiguous slices. Slices range from z = –28 to z = 74 in MNI coordinate space.
Color scale ranges from t = 1.25 (cooler) to 4 (hotter). Radiologic orientation, left = right, right = left.
engage neural circuitry supporting emotional value to experiences, and subjects, hypoactivation of the
narrative comprehension, prefrontal executive function areas, angular gyrus during reading tasks
a foundational component of each integral for learning.65 has been cited as a biomarker for
emergent literacy.63 Specifically, “Recycling” their role in oral dyslexia, with potential application
children in our study with higher language, areas within the PTO are for early identification and
StimQ-P Reading scores showed recruited for reading, facilitating remediation.27,69
greater activation in the left parietal- efficient assignment of meaning to Importantly, PTO activation in our
temporal-occipital (PTO) association letters and words.41,66,67 The angular subjects associated with home
cortex, a “hub” region facilitating gyrus (located in the inferior parietal reading environment reflects
semantic processing.41,64 Outbound lobe) at the core of the PTO is recruitment of oral language skills
PTO connections include limbic areas particularly noteworthy and plays an supporting context and
involved with long-term memory (eg, integral role in this process.23,41,68 comprehension (semantics), not
hippocampus) and assigning Although not observed in our word-level decoding. This is
consistent with behavioral evidence task in young children.49 Thus, PTO behavioral evidence5 that these skills
for the influence of parent-child activation may offer potential as seem largely dependent on explicit
reading exclusively on “outside-in” a biomarker of oral language ability instruction.15 Additional research in
oral language skills (understanding (the outside-in domain of emergent this area is also needed.
outside of the word itself) described literacy), although further studies are Higher StimQ Reading scores were
by Whitehurst et al.1,5 Vocabulary is needed to clarify how the PTO is associated with particularly robust
among the most important of these integrated into the reading network. activation in occipital areas within the
skills,70 shown to be influenced by That home reading environment was PTO cortex, notably lateral occipital
home reading environment17 and not associated with activation of gyrus and precuneus. Schmithorst
recently found to be positively brain areas supporting phonological et al attributed activation in these
associated with left angular gyrus processing (“inside-out” decoding areas during the story listening task
activation during our story listening skills) in our study reinforces (when no visual stimulus is
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September 2015 471
FIGURE 4
Regression map (stories . tones activation) with StimQ-P Reading subscale score as explanatory variable, controlling for household income. Regression
map for the story listening task (stories . tones) in 3- to 5-year-old children (N = 19), with StimQ-P Reading score as explanatory variable, controlling for
household income. Cluster size 2467 voxels significant at P , .05 (FDR corrected), z score local maxima 3.15 to 3.38. Five-millimeter slices from z = –28 to
z = 74 in MNI coordinate space. Color scale from t = 1.25 (cooler) to 4 (hotter). Radiologic orientation, left = right, right = left.
presented) to mental imagery.35 The Recruitment of left-sided PTO areas mental imagery may better manage
ability to “see” what is being heard during high-imagery tasks has also the transition from picture- to text-
has been extensively shown in been described in adults.72 Thus, our based books as they advance in
behavioral studies to improve results provide a neurobiological school. Conversely, those with less
narrative comprehension and recall.71 correlate to the enchantment often practice seeing and understanding,
This was affirmed in a recent, seen at preschool story time, with consequently underdeveloped
imaging-based study that found especially in children with greater visual-semantic neural infrastructure,
positive association between greater practice at home: activation of PTO may be more likely to struggle.
activation of lateral occipital cortex circuits to visualize and understand Surprisingly, we did not find
during the story listening task in 5- to what is happening. It is intriguing to significant association between
7-year-old children and higher infer that children better able to neural activation and PIDA, PVR, or
reading scores at age 11.40 recruit these circuits and apply Composite StimQ-P scores. We view
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September 2015 473
this as likely a byproduct of subscale Our study has several important reading, its demographic mix is
themes. The StimQ-P Reading subscale strengths. Our sample of 3- to 5-year- diverse by design, and all subjects
measures reading-specific practices, old children is considerably younger who were able to be contacted agreed
assessing frequency, access to books, than most neuroimaging-based to participate, minimizing the
and variety of subject matter. As these studies of emergent literacy,27 with prospect of self-selection. The
opportunities and experiences are ample sample size76 drawn from exclusion of four low-SES families
directly related to story listening, a diverse cohort, applying an was a consequence of unreliable
small variations, even with scores established fMRI paradigm and contact information (ie, phone out of
skewed toward the maximum, seem validated measure of home cognitive service), shifting our demographic
adequate to differentiate neural environment. Our findings are profile toward higher SES, although
activation in subjects performing this consistent with current models of 37% of our sample was low-income.
task. By contrast, PIDA measures the language and reading brain Our high reported StimQ-P subscale
teaching of specific cognitive skills and networks,23 complementary with scores suggest potential ceiling
PVR assesses parent-child behavioral models of emergent effects, although the Reading subscale
conversation, each possibly more literacy,15 and robust in controlling provided sensitivity ideal for our task.
applicable to abilities other than for household income, a common Finally, whereas our results show
narrative comprehension. Any confounder in studies of cognitive robust association between home
composite effect was likely diluted by development.77 Using an innovative reading environment and neural
PIDA and PVR scores. approach, our results also inform activation, our cross-sectional design
Contrary to our hypothesis, age of clinical practice during a foundational cannot establish causation.
initiation of shared reading and stage of development in which Longitudinal studies are needed to
months of reading exposure were not “preventative medicine” may offer discern the influence of shared
associated with neural activation, maximal benefit. For example, reading on emergent literacy skills
although behavioral studies have because there is evidence that the beginning in infancy, especially in
associated these with home literacy Reach Out and Read intervention low-SES populations. Such studies
orientation.9,73 This may be advocated in AAP may help us better understand how
attributable to responses skewed by recommendations13 improves home the developing brain responds to
social desirability and/or recall bias reading environment,13,18 and we various platforms, styles (notably
or, more likely, greater predictive have found that home reading dialogic reading), and interventions at
power of the validated StimQ-P environment is positively associated different developmental stages, as
measure. The Reading subscale with activation of brain circuits well as identify children at-risk as
captures 3 aspects of home reading supporting semantic processing, early as possible to ensure the best
environment: frequency (4 points, logical inference leads us to speculate possible outcome for all.
including for days/week), access to that early home literacy intervention
books (5 points, including for number such as Reach Out and Read,
of books in the home), and variety of consistently applied, has the potential CONCLUSIONS
content (10 points, for different types to enhance the development of these Our study used fMRI to for the first
of books, eg concepts, beliefs, brain circuits. time demonstrate an association
relationships). The relative influence Our study also has several limitations. between home reading environment
of each of these factors on neural Although it used existing imaging and and activation of specific brain
activation supporting narrative behavioral data, the StimQ-P was regions supporting emergent literacy
processing is complex, likely retrospectively administered, with during the prekindergarten period.
involving behaviors and proclivities a variable time from fMRI acquisition. While listening to stories, children
that are more difficult to capture, and Thus, recall and social desirability with greater home reading exposure
merits further study. For example, bias are possible, with parents showed significantly higher activation
greater variety may reflect overreporting reading practices. That in areas within the left-sided,
differences in how books are shared, said, household reading behaviors multimodal association cortex, which
in addition to how many and how have been shown to be stable during facilitates mental imagery and
often. This qualitative aspect of the preschool period, tempering such extraction of meaning (semantic
reading aloud (notably, dialogic recall effects.78 Families agreeing to processing). Critical for oral language,
reading in which the child actively participate in our study may be more this region is later integrated into the
participates) has been shown to likely to constructively engage in reading network,35,54 with
provide a disproportionate share of its their child’s development hypoactivation, a biomarker of
benefits, behaviorally74,75 and possibly (participation bias); although C-MIND reading disability.27 This study
in terms of neurobiological effect. is not advertised in the context of suggests a novel, neurobiological
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September 2015 475
www.pediatrics.org/cgi/doi/10.1542/peds.2015-0359
DOI: 10.1542/peds.2015-0359
Accepted for publication Jun 2, 2015
Address correspondence to John S. Hutton, MD, Division of General and Community Pediatrics, Cincinnati Children’s Hospital Medical Center, 3333 Burnet Ave, MLC
7035, Cincinnati, OH 45229. E-mail: john1.hutton@cchmc.org
PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275).
Copyright © 2015 by the American Academy of Pediatrics
FINANCIAL DISCLOSURE: The authors have indicated they have no financial relationships relevant to this article to disclose.
FUNDING: All phases of this study were supported by National Institutes of Health contract HHSN275200900018C to the Pediatric Functional Neuroimaging Research
Network, a Ruth L Kirschstein National Research Service Award, and an Academic Pediatric Association Young Investigator Award (YIA) for Primary Care Strategies
for the Promotion of Early Literacy and School Readiness Supported by Reach Out and Read.
POTENTIAL CONFLICT OF INTEREST: John Hutton received an Academic Pediatric Association Young Investigator Award supported by Reach out and Read in support
of this project, although this award provided no direct financial or salary compensation. Tom DeWitt has served on the board of directors of Reach Out and Read
from 2009-present but receives no financial compensation. Alan Mendelsohn serves as Senior Research Advisor for Child Development and School Readiness for
Reach Out and Read but receives no financial compensation. The other authors have indicated they have no potential conflicts of interest to disclose.
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Pediatrics is the official journal of the American Academy of Pediatrics. A monthly publication, it
has been published continuously since . Pediatrics is owned, published, and trademarked by the
American Academy of Pediatrics, 141 Northwest Point Boulevard, Elk Grove Village, Illinois,
60007. Copyright © 2015 by the American Academy of Pediatrics. All rights reserved. Print
ISSN: .