Home Reading Environment and BrainActivation in Preschool ChildrenListening to StoriesJohn S. Hutton, MDa, Tzipi Horowitz-Kraus, PhDa,b,c, Alan L. Mendelsohn, MDe, Tom DeWitt, MDa, Scott K. Holland, PhDb,c,d,the C-MIND Authorship Consortium

abstract BACKGROUND AND OBJECTIVES: Parent-child reading is widely advocated to promote cognitivedevelopment, including in recommendations from the American Academy of Pediatrics to beginthis practice at birth. Although parent-child reading has been shown in behavioral studies toimprove oral language and print concepts, quantifiable effects on the brain have not beenpreviously studied. Our study used blood oxygen level–dependent functional magneticresonance imaging to examine the relationship between home reading environment and brainactivity during a story listening task in a sample of preschool-age children. We hypothesized thatwhile listening to stories, children with greater home reading exposure would exhibit higheractivation 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 normalbrain development. All completed blood oxygen level–dependent functional magneticresonance imaging using an age-appropriate story listening task, where narrative alternatedwith 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 homecognitive 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 associationcortex, a “hub” region supporting semantic language processing, controlling for household income.

CONCLUSIONS: In preschool children listening to stories, greater home reading exposure ispositively associated with activation of brain areas supporting mental imagery and narrativecomprehension, controlling for household income. These neural biomarkers may help informeco-bio-developmental models of emergent literacy.

WHAT’S KNOWN ON THIS SUBJECT: The AmericanAcademy of Pediatrics recommends parent-childreading from infancy through at leastkindergarten, the span of maximal brain growth.Home literacy environment, including readingbehaviors and access to books, has been shownto promote oral language and print concepts.

WHAT THIS STUDY ADDS: Home readingenvironment is positively associated with activationof brain areas supporting narrative comprehensionand mental imagery in preschool children. Thisoffers novel insight into the neurobiologicalfoundations of emergent literacy and potentialeffect of shared reading during early childhood.

aDivision of General and Community Pediatrics, bPediatric Neuroimaging Research Consortium, cCommunicationSciences Research Center, and dDivision of Radiology, Cincinnati Children’s Hospital Medical Center, Cincinnati,Ohio; and eDepartment of Pediatrics, New York University School of Medicine and Bellevue Hospital Center, NewYork, New York

Dr Hutton conceptualized and designed the study, performed all data analysis, and drafted theinitial manuscript and subsequent revisions; Dr Horowitz-Kraus provided guidance on study designand analysis, assisted with coordination of data collection, and reviewed and revised themanuscript; Dr Mendelsohn served as national outside facilitator and mentor for this project,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;Dr Holland designed and secured funding for the parent neuroimaging study and acquired imagingand behavioral data in all participants; he was also responsible for image and behavioral dataquality control, database archiving and first-level analysis of fMRI data and participated in the studydesign for addition of reading measures and supervised collection of the StimQ questionnaire; andall authors approved the final manuscript as submitted.

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Emergent literacy is defined as theskills, knowledge, and attitudessupporting reading and writing thataccrue from infancy.1 Although organicreading disability (dyslexia) affects anestimated 5% to 12% of US children,2

the majority of illiteracy is preventable,attributable to inadequate resources,motivation, and/or stimulationrequired to learn to read.3 As parentsare “a child’s first and most importantteachers,”4 the quality of cognitivestimulation in the home, especiallybefore school entry, strongly influencesachievement and health outcomes.5–8

Children’s books are catalysts forparent-child engagement duringsensitive developmental stages whenbrain growth and plasticity aremaximal.9,10 They provide broader,more grammatically correctvocabulary and range of subject matterthan everyday conversation, especiallyin low-socioeconomic status (SES)households.11,12 Given these factors,the American Academy of Pediatrics(AAP) recommends shared readingbeginning at birth, citing direct, lastingbenefits for the developing brain,13

a claim echoed by many advocacygroups.14

While behavioral evidence affirmsmoderate to large benefits of sharedreading on a subset of emergentliteracy skills (oral language and printconcepts) through kindergarten,5,15

quantifiable effects on the brain havenot been previously studied. Similarly,interventions improving homeliteracy environment, a variablydefined measure of reading behaviorsand access to books, have been shownto improve oral language and schoolreadiness,16–20 althoughneurobiological mechanisms have yetto be described. Neuroimaging offersa means to address these knowledgegaps, informing an eco-bio-developmental model of emergentliteracy incorporating genetic,environmental, and neurobiologicalfactors.21–25 Such models have beenadvocated by the AAP and NationalInstitutes of Health25 and are

especially valuable for youngchildren, where behavioral measurescan underestimate the effects oflearning and experience on thedeveloping brain.10,26 Neuroimaginghas been extensively applied indyslexia research (albeit in olderchildren and adults), identifyingactivation patterns associated withreading difficulty and response tointervention,2,27–29 as well as helpingdefine the mature readingnetwork.30,31 Only recently has high-resolution neuroimaging been appliedin younger, preliterate children,32

most often in the context of normallanguage development.33,34 Howlanguage networks become “ready”for reading and to what extent theyare influenced by home literacyenvironment or interventions duringthe critical pre-kindergarten period,however, are unclear.

For our study, a sample of 3- to5-year-old children underwent bloodoxygen level dependent functionalmagnetic resonance imaging (BOLDfMRI) using a story listening task.35,36

This task requires the application ofemergent literacy skills supportingsemantic processing (extraction ofmeaning), including vocabulary andlistening comprehension.37–40 Givenbehavioral evidence,1,5 wehypothesized that children with morestimulating home environments,particularly shared reading exposure,would show more robust activation inbrain areas supporting these skills.The semantic network includes left-sided inferior frontal, middletemporal, inferior parietal, and lateraloccipital lobes.35,39,41 We predictedthat differential activation within thisnetwork would remain significantafter controlling for householdincome, a common confounder instudies of cognitive ability.42–44

METHODS

Participants

All participants in this analysis wereenrolled in a longitudinal study of

normal brain development at ourinstitution (Cincinnati MR Imaging ofNeuroDevelopment; C-MIND).45

Inclusion criteria for C-MIND are asfollows: full-term gestation, healthy,right-handed, native English speakers,and no standard contraindications toMRI. By design, the C-MIND cohort isdemographically diverse (38%nonwhite, 55% female, medianhousehold income $42 500), intendedto reflect the US population. At thetime of our study, 23 childrenbetween 3 and 5 years of age hadcompleted BOLD fMRI whileperforming a story listening task, inaccordance with the C-MIND protocol.Of these, we were able to contact 19families (82.6%) for enrollment andsurvey administration. Despitemultiple attempts, we were unable tocontact the other 4 families, whowere excluded. Informed consent wasobtained from each child’s custodialparent, families were compensatedfor time and travel, and our study wasapproved by the Cincinnati Children’sHospital Medical Center InstitutionalReview Board.

Behavioral Measures

Cognitive stimulation in the homewas assessed using the preschoolversion of the StimQ (StimQ-P),46

which was administered toa custodial parent via telephone orduring C-MIND follow-up visits bya trained clinical researchcoordinator. Time elapsed betweenfMRI scan and StimQ administrationranged from 0 to 20 months (10 68.8). The StimQ-P is validated for ages36 to 72 months47 and involvesmostly “yes/no” questions. Threesubscales were used: (1) Reading,reflecting access to books, frequencyof shared reading, and variety ofbooks read; (2) Parental Involvementin Developmental Advance (PIDA),reflecting the teaching of specificconcepts such as letters; and (3)Parental Verbal Responsivity (PVR),reflecting verbal interaction. Parentswere also asked to report the age of

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initiation of reading to their child,which is not included in the StimQ-P.

fMRI Acquisition Specifications andPreliminary Analyses

Details of techniques used toacclimatize children to the MRIacquisition process are described byVannest et al.32 Details of BOLD MRIacquisition specifications used in theC-MIND study are described inSchmithorst et al.35,48 Details of datapreprocessing for the C-MIND studyare described in Sroka et al.49 Allchildren were awake and nonsedatedduring MRI scans. Voxel size used foracquisition and analysis was 3 3 3 34 mm. We used the FEAT (fMRI ExpertAnalysis Tool) modality of FSL (fMRI-Brain Software Library, Oxford, UnitedKingdom) for all group mean andhigher-level regression analyses.50

fMRI Story Listening Task and GroupMean Analysis

The story listening task consists of 10alternating blocks of active andcontrol conditions (5 each) of 64seconds’ duration. During the “active”condition, a series of 5 recordedstories of 9 to 10 sentences each readin a female voice was presented viaheadphones. The stories weredesigned by a speech pathologist withconsistent vocabulary and syntaxappropriate for young children(download: https://www.irc.cchmc.org/software/pedaudio.php). Thecontrol condition consisted ofnonspeech tones in a range offrequencies simulating human speechto control for baseline acousticprocessing. Subjects closed their eyesor saw a blank screen during scanning.

During task presentation, the MRIscanner continuously acquired BOLD-weighted scans, covering the entirebrain with 24 slices at 4-secondintervals. Image time series data wereentered into a general linear modelfor “first-level,” voxelwise analysis,using the story and tone intervals asthe regressor of interest. Contrastmaps (stories . tones activation)were converted to z score maps with

statistical threshold of P , .05,applying a false discovery rate (FDR)correction for multiple voxelcomparisons across the brain. Usingthese, we obtained a whole-brain,group mean activation map for our 19subjects, representing mean neuralactivation listening to stories, minusactivation listening to tones (ie,activation attributable to the storytask, excluding general acousticprocessing).

Regression With StimQ-P and OtherPredictors

For each subject, the z score maprepresenting the contrast of (stories. tones) was used as the dependentvariable in a series of “higher-level”regression analyses, applying StimQ-Pscores (Reading, PIDA, PVR,Composite) or responses to individualquestions as the explanatory variable.Income category (low/not low) wasapplied as a binary covariate whensignificant neural activation wasfound, with household income,200% of the 2015 Federal PovertyGuidelines,51 adjusted for householdsize, defined as low income (seeTable 1).52 Subject age and genderwere considered as covariates butexcluded because no significantcorrelation was found between neuralactivation and either variable.Regression maps of neural activation(stories . tones), along withsummary statistics for size, intensity,and location of activation clusters,were reported for all significantresults, using a threshold forstatistical significance of P , .05applying FDR correction. TheFSLView50 package was used toidentify brain areas corresponding toactive clusters in normalized, three-dimensional, Montreal NeurologicInstitute (MNI) coordinate space,53

using the Harvard-Oxford CorticalStructural Atlas (2-mm scale).

RESULTS

Demographic characteristics for oursample are described in Table 1.

StimQ-P and Other BehavioralPredictors

A summary of StimQ-P subscale andcomposite scores, and reported age ofinitiation of shared reading aredescribed in Table 2 and Fig 1.

Group Mean Activation for theNarrative Comprehension Task

Group mean activation for thenarrative condition compared withbaseline tones (all voxels P , .05,FDR correction) involved bilateral,left-lateralized cortical andsubcortical regions involved withacoustic, phonological, and semanticlanguage processing (see Fig 2), asdescribed by Karunanayaka et al.54

Regression of Neural Activation WithStimQ-P Scores and Other Predictors

Applying linear regression, StimQ-PReading subscale scores werepositively correlated with higheractivation in a confluent region of left-sided, posterior cortex involving theoccipital fusiform, lateral occipital,

TABLE 1 Demographic Characteristics ofC-MIND Sample Subjects

Characteristic n %

Sample 19 100Age (y)3+ 10 524+ 6 325+ 3 16

GenderMale 8 42Female 11 58

Annual household income (US$),5000 0 05000–10 000 1 510–15 000 1 515 000–25 000 2 1125 000–35 000 1 535 000–50 000 2 1150 000–75 000 4 2175 000–100 000 4 21100 000–150 000 2 11.150 000 2 11

Household income levelBelow 200% poverty (low) 7 37Above 200% poverty 12 63

Children in the household1 3 162–3 12 634–5 3 166 1 5

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posterior inferior temporal, posteriormiddle temporal, posterior cingulate,and angular gyri, and left precuneus,as illustrated in Fig 3 (all voxels P ,

.05, FDR correction). Collectively,these areas reside within the parietal-temporal-occipital (PTO) associationcortex, which supports multimodalsemantic processing, especially forlanguage.41,55 An exception is theposterior cingulate gyrus, which plays

a role in semantic processing andother functions, including memoryencoding41 and visual attention.56

The correlation between StimQ-PReading subscale score and neuralactivation within the left PTO cortexremained consistent and significantwhen expanding the statistical modelto control for household income asa binary covariate (low/not low).Activation clusters were of similar

intensity, with slight to moderatedecreases in size, as shown in Fig 4(all voxels P , .05, FDR correction).The largest decreases were inposterior cingulate, inferior temporal,occipital fusiform, and the mostsuperior lateral occipital areas. Fig 5displays orthogonal sagittal, coronal,and axial slice views (origin x = –34y = –66, z = 14, MNI coordinate space)to more clearly illustrate the anatomicextent of this PTO activation cluster.

No significant correlation was foundbetween brain activation during thestory listening task and other StimQ-Psubscales, StimQ-P composite, age ofinitiation of reading, or months ofreading exposure (initiation to scan).

DISCUSSION

“Biological embedding” describes thelong-term impact on braindevelopment resulting from thequality of cognitive stimulation andnurturing during early childhood.6,57

Learning to read involves theintegration of a formidable array ofskills sequentially and efficiently,5

supported by language, visual, andassociation brain networks, thegrowth and plasticity of which peakin the first few years of life.58,59

During this critical prekindergartenperiod, children are highly vulnerableto disparities in cognitive stimulation,especially spoken language, as well astoys and books promotingconstructive parent-childengagement.12,58,60 Many childrenarrive at school at a significantdisadvantage in reading readiness,and it is clear that those who are poorreaders in first grade61 are unlikely tocatch up with peers, at great societalcost.62 This underscores the need foreffective interventions applied asearly as possible, when brainnetworks are most amenable tochange.10,58,62

Our findings support our hypothesisthat while listening to stories, youngchildren from more stimulating homereading environments more robustly

TABLE 2 StimQ-P and Specific Reading-Related Item Scores

StimQ-P Possible Mean SD Min Max

Reading 19 17.8 2.0 13 19PIDA 15 11.6 2.2 8 15PVR 7 5.8 1.2 3 7Composite 41 35.2 3.7 27 41

Specific ItemsAge (mo) initiation of reading n/a 5.0 5.5 0 24Months of reading exposure n/a 43.0 9.5 30 63Children’s books in the home n/a 162.0 112.8 10 400Reading nights/wk 7 6.0 1.9 2 7

Summary of StimQ-P subscale, Composite, and reading-related item scores. Total possible score (where applicable),mean, SD, minimum (Min), and maximum (Max) are presented. Individual questions other than age of initiation of readingare part of the StimQ-P Reading subscale.

FIGURE 1StimQ-P Subscale and Composite scores. Histograms and density curves for StimQ-P scores. Meanand SD are provided, with a dashed vertical line for each mean. The Reading subscale reflectsparent-child reading materials and behaviors (maximum score 19); PIDA measures parental in-volvement teaching specific skills (maximum 15); PVR indicates parent-child verbal interaction(maximum 7).

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engage neural circuitry supportingnarrative comprehension,a foundational component ofemergent literacy.63 Specifically,children in our study with higherStimQ-P Reading scores showedgreater activation in the left parietal-temporal-occipital (PTO) associationcortex, a “hub” region facilitatingsemantic processing.41,64 OutboundPTO connections include limbic areasinvolved with long-term memory (eg,hippocampus) and assigning

emotional value to experiences, andprefrontal executive function areas,each integral for learning.65

“Recycling” their role in orallanguage, areas within the PTO arerecruited for reading, facilitatingefficient assignment of meaning toletters and words.41,66,67 The angulargyrus (located in the inferior parietallobe) at the core of the PTO isparticularly noteworthy and plays anintegral role in this process.23,41,68

Although not observed in our

subjects, hypoactivation of theangular gyrus during reading taskshas been cited as a biomarker fordyslexia, with potential applicationfor early identification andremediation.27,69

Importantly, PTO activation in oursubjects associated with homereading environment reflectsrecruitment of oral language skillssupporting context andcomprehension (semantics), notword-level decoding. This is

FIGURE 2Group 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). Allvoxels 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.

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consistent with behavioral evidencefor the influence of parent-childreading exclusively on “outside-in”oral language skills (understandingoutside of the word itself) describedby Whitehurst et al.1,5 Vocabulary isamong the most important of theseskills,70 shown to be influenced byhome reading environment17 andrecently found to be positivelyassociated with left angular gyrusactivation during our story listening

task in young children.49 Thus, PTOactivation may offer potential asa biomarker of oral language ability(the outside-in domain of emergentliteracy), although further studies areneeded to clarify how the PTO isintegrated into the reading network.That home reading environment wasnot associated with activation ofbrain areas supporting phonologicalprocessing (“inside-out” decodingskills) in our study reinforces

behavioral evidence5 that these skillsseem largely dependent on explicitinstruction.15 Additional research inthis area is also needed.

Higher StimQ Reading scores wereassociated with particularly robustactivation in occipital areas within thePTO cortex, notably lateral occipitalgyrus and precuneus. Schmithorstet al attributed activation in theseareas during the story listening task(when no visual stimulus is

FIGURE 3Regression map (stories . tones activation) with StimQ-P Reading subscale score as explanatory variable. 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. Cluster size 4087 voxels significant at P , .05(FDR corrected), z score local maxima 3.25 to 3.44. 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.

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presented) to mental imagery.35 Theability to “see” what is being heardhas been extensively shown inbehavioral studies to improvenarrative comprehension and recall.71

This was affirmed in a recent,imaging-based study that foundpositive association between greateractivation of lateral occipital cortexduring the story listening task in 5- to7-year-old children and higherreading scores at age 11.40

Recruitment of left-sided PTO areasduring high-imagery tasks has alsobeen described in adults.72 Thus, ourresults provide a neurobiologicalcorrelate to the enchantment oftenseen at preschool story time,especially in children with greaterpractice at home: activation of PTOcircuits to visualize and understandwhat is happening. It is intriguing toinfer that children better able torecruit these circuits and apply

mental imagery may better managethe transition from picture- to text-based books as they advance inschool. Conversely, those with lesspractice seeing and understanding,with consequently underdevelopedvisual-semantic neural infrastructure,may be more likely to struggle.

Surprisingly, we did not findsignificant association betweenneural activation and PIDA, PVR, orComposite StimQ-P scores. We view

FIGURE 4Regression map (stories . tones activation) with StimQ-P Reading subscale score as explanatory variable, controlling for household income. Regressionmap 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 forhousehold 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 toz = 74 in MNI coordinate space. Color scale from t = 1.25 (cooler) to 4 (hotter). Radiologic orientation, left = right, right = left.

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FIGURE 5Triplanar view of neural activation (stories . tones) with StimQ-P Reading subscale score as explanatory variable, controlling for household income.Orthogonal triplanar view (origin x = –34, y = –66, z = 14, MNI coordinate space) of activation for the story listening task (stories . tones), with StimQ-PReading score as explanatory variable, controlling for household income. Cluster size 2467 voxels significant at P , .05 (FDR corrected). Color scaleranges from t = 1.25 (cooler) to 4 (hotter). All views in radiologic orientation, left = right, right = left, with sagittal plane viewed from the right.

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this as likely a byproduct of subscalethemes. The StimQ-P Reading subscalemeasures reading-specific practices,assessing frequency, access to books,and variety of subject matter. As theseopportunities and experiences aredirectly related to story listening,small variations, even with scoresskewed toward the maximum, seemadequate to differentiate neuralactivation in subjects performing thistask. By contrast, PIDA measures theteaching of specific cognitive skills andPVR assesses parent-childconversation, each possibly moreapplicable to abilities other thannarrative comprehension. Anycomposite effect was likely diluted byPIDA and PVR scores.

Contrary to our hypothesis, age ofinitiation of shared reading andmonths of reading exposure were notassociated with neural activation,although behavioral studies haveassociated these with home literacyorientation.9,73 This may beattributable to responses skewed bysocial desirability and/or recall biasor, more likely, greater predictivepower of the validated StimQ-Pmeasure. The Reading subscalecaptures 3 aspects of home readingenvironment: frequency (4 points,including for days/week), access tobooks (5 points, including for numberof books in the home), and variety ofcontent (10 points, for different typesof books, eg concepts, beliefs,relationships). The relative influenceof each of these factors on neuralactivation supporting narrativeprocessing is complex, likelyinvolving behaviors and proclivitiesthat are more difficult to capture, andmerits further study. For example,greater variety may reflectdifferences in how books are shared,in addition to how many and howoften. This qualitative aspect ofreading aloud (notably, dialogicreading in which the child activelyparticipates) has been shown toprovide a disproportionate share of itsbenefits, behaviorally74,75 and possiblyin terms of neurobiological effect.

Our study has several importantstrengths. Our sample of 3- to 5-year-old children is considerably youngerthan most neuroimaging-basedstudies of emergent literacy,27 withample sample size76 drawn froma diverse cohort, applying anestablished fMRI paradigm andvalidated measure of home cognitiveenvironment. Our findings areconsistent with current models oflanguage and reading brainnetworks,23 complementary withbehavioral models of emergentliteracy,15 and robust in controllingfor household income, a commonconfounder in studies of cognitivedevelopment.77 Using an innovativeapproach, our results also informclinical practice during a foundationalstage of development in which“preventative medicine” may offermaximal benefit. For example,because there is evidence that theReach Out and Read interventionadvocated in AAPrecommendations13 improves homereading environment,13,18 and wehave found that home readingenvironment is positively associatedwith activation of brain circuitssupporting semantic processing,logical inference leads us to speculatethat early home literacy interventionsuch as Reach Out and Read,consistently applied, has the potentialto enhance the development of thesebrain circuits.

Our study also has several limitations.Although it used existing imaging andbehavioral data, the StimQ-P wasretrospectively administered, witha variable time from fMRI acquisition.Thus, recall and social desirabilitybias are possible, with parentsoverreporting reading practices. Thatsaid, household reading behaviorshave been shown to be stable duringthe preschool period, tempering suchrecall effects.78 Families agreeing toparticipate in our study may be morelikely to constructively engage intheir child’s development(participation bias); although C-MINDis not advertised in the context of

reading, its demographic mix isdiverse by design, and all subjectswho were able to be contacted agreedto participate, minimizing theprospect of self-selection. Theexclusion of four low-SES familieswas a consequence of unreliablecontact information (ie, phone out ofservice), shifting our demographicprofile toward higher SES, although37% of our sample was low-income.Our high reported StimQ-P subscalescores suggest potential ceilingeffects, although the Reading subscaleprovided sensitivity ideal for our task.Finally, whereas our results showrobust association between homereading environment and neuralactivation, our cross-sectional designcannot establish causation.Longitudinal studies are needed todiscern the influence of sharedreading on emergent literacy skillsbeginning in infancy, especially inlow-SES populations. Such studiesmay help us better understand howthe developing brain responds tovarious platforms, styles (notablydialogic reading), and interventions atdifferent developmental stages, aswell as identify children at-risk asearly as possible to ensure the bestpossible outcome for all.

CONCLUSIONS

Our study used fMRI to for the firsttime demonstrate an associationbetween home reading environmentand activation of specific brainregions supporting emergent literacyduring the prekindergarten period.While listening to stories, childrenwith greater home reading exposureshowed significantly higher activationin areas within the left-sided,multimodal association cortex, whichfacilitates mental imagery andextraction of meaning (semanticprocessing). Critical for oral language,this region is later integrated into thereading network,35,54 withhypoactivation, a biomarker ofreading disability.27 This studysuggests a novel, neurobiological

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correlate to oral language skillsfostered by parent-child reading inearly childhood, offering insight intohow this practice may shape thedeveloping brain, and informing aneco-bio-developmental model ofemergent literacy and its promotion.

ACKNOWLEDGMENTS

The authors thank Claire Sroka andSarah Finucane for their invaluablehelp conducting the StimQ surveysand organizing behavioral data. Wealso thank Molly Grainger for herassistance with the FSL fMRI analysispackage.

The C-MIND database used for thisstudy can be accessed free of chargeat https://research.cchmc.org/c-mind. The authors thank the C-MINDAuthorship Consortium:

Scott K. Holland, PhD, PediatricNeuroimaging Research Consortium,Department of Radiology, Departmentof Otolaryngology, CommunicationSciences Research Center, CincinnatiChildren’s Hospital Medical Center,University of Cincinnati, Cincinnati,Ohio; Jennifer Vannest, PhD, PediatricNeuroimaging Research Consortiumand Division of Neurology,Department of Pediatrics, CincinnatiChildren’s Hospital Medical Center,University of Cincinnati, Cincinnati,Ohio; Vincent J. Schmithorst, PhD,Pediatric Neuroimaging ResearchConsortium, Cincinnati Children’sHospital Medical Center, University ofCincinnati, Cincinnati, Ohio, andPediatric Imaging Research Center,Department of Radiology, Children’sHospital of Pittsburgh of UPMC,Pittsburgh, Pennsylvania; MekibibAltaye, PhD, Pediatric NeuroimagingResearch Consortium and Division ofBiostatistics and Epidemiology,Department of Pediatrics, CincinnatiChildren’s Hospital Medical Center,University of Cincinnati, Cincinnati,Ohio; Gregory Lee, PhD, PediatricNeuroimaging Research Consortiumand Department of Radiology,

Cincinnati Children’s Hospital MedicalCenter, University of Cincinnati,Cincinnati, Ohio; Luis Hernandez-Garcia, PhD, Functional MRILaboratory, Department ofBiomedical Engineering, University ofMichigan, Ann Arbor, Michigan;Michael Wagner, PhD, PediatricNeuroimaging Research Consortiumand Division of BiomedicalInformatics, Deparment of Pediatrics,Cincinnati Children’s Hospital MedicalCenter, University of Cincinnati,Cincinnati, Ohio; Arthur Toga, PhD,Laboratory of Neuroimaging andDepartments of Ophthalmology,Neurology, Psychiatry, and theBehavioral Sciences, Radiology andEngineering, Keck School of Medicineof USC, Los Angeles, California;Jennifer Levitt, MD, Psychiatry andBiobehavioral Sciences, UCLA, LosAngeles, California; Anna W. Byars,PhD, Pediatric NeuroimagingResearch Consortium and Division ofNeurology, Department of Pediatrics,Cincinnati Children’s Hospital MedicalCenter, University of Cincinnati,Cincinnati, Ohio; Andrew Dimitrijevic,PhD, Department of Otolaryngologyand Communication SciencesResearch Center, Cincinnati Children’sHospital Medical Center, University ofCincinnati, Cincinnati, Ohio; NicolasFelicelli, Division of BiomedicalInformatics, Department of Pediatrics,Cincinnati Children’s Hospital MedicalCenter, University of Cincinnati,Cincinnati, Ohio; Darren Kadis, PhD,Pediatric Neuroimaging ResearchConsortium and Division ofNeurology, Department of Pediatrics,Cincinnati Children’s Hospital MedicalCenter, University of Cincinnati,Cincinnati, Ohio; James Leach, MD,Department of Radiology, CincinnatiChildren’s Hospital Medical Center,University of Cincinnati, Cincinnati,Ohio; Katrina Peariso, MD, PhD,Division of Neurology, Department ofPediatrics, Cincinnati Children’sHospital Medical Center, University ofCincinnati, Cincinnati, Ohio; ElenaPlante, PhD, Deptartment of Speech,

Language, and Hearing Sciences,University of Arizona, Tucson,Arizona; Akila Rajagopal, MS,Pediatric Neuroimaging ResearchConsortium, Cincinnati Children’sHospital Medical Center, University ofCincinnati, Cincinnati, Ohio; AndrewRupert, MS, Division of BiomedicalInformatics, Department of Pediatrics,Cincinnati Children’s Hospital MedicalCenter, University of Cincinnati,Cincinnati, Ohio; Mark Schapiro, MD,Pediatric Neuroimaging ResearchConsortium and Division ofNeurology, Department of Pediatrics,Cincinnati Children’s Hospital MedicalCenter, University of Cincinnati,Cincinnati, Ohio; Karen Crawford,Laboratory of Neuroimaging, KeckSchool of Medicine of USC, LosAngeles, California; Ronald Ly,Psychiatry and BiobehavioralSciences, UCLA, Los Angeles,California; Katherine Narr, PhD,Department of Neurology, UCLA, LosAngeles, California; Petros Petrosyan,Laboratory of Neuroimaging, KeckSchool of Medicine of USC, LosAngeles, California; J.J. Wang, PhD,Department of Neurology, UCLA, LosAngeles, California; and Lisa Freund,PhD, Eunice Kennedy ShriverNational Institute of Child Health andHuman DevelopmentBethesda, Maryland.

ABBREVIATIONS

AAP: American Academy ofPediatrics

BOLD: blood oxygenlevel–dependent

C-MIND: Cincinnati MR Imaging ofNeuroDevelopment

FDR: false discovery ratefMRI: functional magnetic

resonance imagingMNI: Montreal Neurologic InstitutePIDA: Parental Involvement in

Developmental AdvancePVR: Parental Verbal ResponsivityPTO: parietal-temporal-occipitalSES: socioeconomic status

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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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originally published online August 10, 2015; Pediatrics Holland and the C-MIND Authorship Consortium

John S. Hutton, Tzipi Horowitz-Kraus, Alan L. Mendelsohn, Tom DeWitt, Scott K.Listening to Stories

Home Reading Environment and Brain Activation in Preschool Children

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