www.jped.com.br
ORIGINAL
ARTICLE
A
comparison
between
preterm
and
full-term
infants’
preference
for
faces
夽
Silvana
A.
Pereira
a,b,c,∗,
Antônio
Pereira
Junior
b,
Marcelo
F.
da
Costa
a,
Margareth
de
V.
Monteiro
b,
Valéria
A.
de
Almeida
c,d,
Gentil
G.
da
Fonseca
Filho
c,
Nívia
Arrais
b,e,
Francesca
Simion
faUniversidadedeSãoPaulo(USP),InstitutodePsicologia,DepartamentodePsicologiaExperimental,SãoPaulo,SP,Brazil bUniversidadeFederaldoRioGrandedoNorte(UFRN),Natal,RN,Brazil
cUniversidadeFederaldoRioGrandedoNorte(UFRN),FaculdadedeCiênciasdaSaúdedoTrairí(FACISA),Natal,RN,Brazil dHospitalUniversitárioAnaBezerra(HUAB),UniversidadeFederaldoRioGrandedoNorte(UFRN),SantaCruz,RN,Brazil eUniversidadeFederaldoRioGrandedoNorte(UFRN),MaternidadeEscolaJanuárioCicco,Natal,RN,Brazil
fCentroNeuroscienzeCognitive,UniversitadiPadova,DipartimentodiPsicologiadelloSviluppoedellaSocializzazione,
Padova,Italy
Received2March2016;accepted28April2016 Availableonline18July2016
KEYWORDS
Modelofvisual recognition; Visualperception; Newborn;
Preterminfant; Full-terminfant
Abstract
Objective: Visualpreferenceforfacesatbirthistheproductofamultimodalsensory expe-rienceexperiencedby thefetusevenduringthegestationalperiod.Theabilitytorecognize facesallowsanecologicallyadvantageousinteractionwiththesocialenvironment.However, perinataleventssuchasprematurebirth,mayadverselyaffecttheadequatedevelopmentof thiscapacity.Inthisstudy,weevaluatedthepreferencefor facialstimuliinpreterminfants withinthefirstfewhoursafterbirth.
Methods: Thisisacross-sectionalobservationalstudyof59newborns,28pretermand31 full-terminfants.Thebabieswereassessedinthefirsthoursoflife,withtwowhiteboardsinthe shapeofaheadandneck:onewiththedrawingofafacesimilartothehumanface(natural face),andonewiththedrawingofmisalignedeyes,mouth andnose(distortedface).After thenewbornfixatedtheeyesonthepresentedstimulus,itwasslowlymovedalongthevisual field.Therecognitionofthestimuluswasconsideredpresentwhenthebabyhadeyeorhead movementstowardthestimulus.
Results: Thepreterminfants,inadditiontoshowingaloweroccurrenceoforientation move-mentsforbothstimuli,onaverage(1.8±1.1tonaturalfacesand2.0±1.2fordistortedones) alsoshowednopreferenceforanyofthem(p=0.35).Full-termnewbornsshowedadifferent behavior,inwhichtheyshowedapreferencefornaturalfaces(p=0.002)andahighernumber oforientationsforthestimulus,forbothnatural(3.2±0.8)anddistortedfaces(2.5±0.9).
夽 Pleasecitethisarticleas:PereiraSA,Pereira JuniorA,CostaMF,MonteiroMV,Almeida VA,FonsecaFilhoGG,etal.Acomparison
betweenpretermandfull-terminfants’preferenceforfaces.JPediatr(RioJ).2017;93:35---9.
∗Correspondingauthor.
E-mail:apsilvana@gmail.com(S.A.Pereira).
http://dx.doi.org/10.1016/j.jped.2016.04.009
0021-7557/©2016SociedadeBrasileiradePediatria.PublishedbyElsevierEditoraLtda.ThisisanopenaccessarticleundertheCCBY-NC-ND
Conclusion: Pretermnewbornsrecognizefacialstimulianddisclosenopreferencefornatural faces,differentfromfull-termnewborns.
©2016SociedadeBrasileiradePediatria.PublishedbyElsevierEditoraLtda.Thisisanopen accessarticleundertheCCBY-NC-NDlicense(http://creativecommons.org/licenses/by-nc-nd/ 4.0/).
PALAVRAS-CHAVE
Reconhecimento visualdemodelos; Percepc¸ãovisual; Recém-nascido; Prematuro;
Nascimentoatermo
Umacomparac¸ãoentrerecém-nascidosprematuroseatermonapreferênciapor faces
Resumo
Objetivo: Apreferênciavisualporfacesaonascimentoéprodutodeumaexperiência senso-rialmultimodalvivenciadapelofetoaindanoperíodogestacional.Ahabilidadedereconhecer facespossibilitaumainterac¸ãoecologicamentevantajosacomoambientesocial.Entretanto, eventosperinatais,comoonascimentoprematuro,podemprejudicarodesenvolvimento ade-quado dessa habilidade. Nesse trabalho, avaliamos a preferência por estímulos faciais de recém-nascidosprematurosnasprimeirashorasapósonascimento.
Métodos: Trata-sedeumestudoobservacionaltransversalrealizadocom59recém-nascidos, 28prematurose31nascidostermos.Osbebêsforamavaliados,nasprimeirashorasdevida, comduaspranchasbrancasem formatode cabec¸aepescoc¸o: umacomodesenhode uma facesimilarao rostohumano(face natural),eoutra comodesenhodeolhos, bocaenariz desalinhados(facedistorcida).Apósorecém-nascidofixaroolharnoestímuloapresentadoo mesmoeralentamentemovimentado ao longodocampo visual.Oreconhecimentodo estí-mulofoiconsideradopresentequandoobebêapresentoumovimentosdosolhosoucabec¸aem direc¸ãoaoestímulo.
Resultados: Osrecém-nascidosprematurosalémdeapresentaremmenorocorrênciade movi-mentos de orientac¸ãopara ambos os estímulos, em média(1,8±1,1 para facesnaturais e 2,0±1,2parafacesdistorcidas),tambémnãoapresentarampreferênciaporqualquerumdeles (p=0,35).Diferentefoiocomportamentodosrecém-nascidosatermoqueapresentaram prefe-rênciaporfacesnaturais(p=0,002)eumnúmeromaiordeorientac¸õesparaoestímulo,tanto parafacesnaturais(3,2±0,8)quantoparafacesdistorcidas(2,5±0,9).
Conclusão: Recém-nascidos prematuros reconhecemos estímulos faciais e não apresentam preferênciaporfacesnaturais,diferentederecém-nascidosatermos.
©2016SociedadeBrasileiradePediatria.PublicadoporElsevierEditoraLtda.Este ´eumartigo OpenAccesssobumalicenc¸aCCBY-NC-ND(http://creativecommons.org/licenses/by-nc-nd/4. 0/).
Introduction
Despitethevisualcorticalareaimmaturityandthe conse-quentlimitation in visual skills, newborns have an innate preferenceforvisualstimulithatresemblefaces.This abil-ityisessentialtoguidethechild’sinteractionsinthesocial environment.1
Unlike most other objects, faces are processed in a holistic or configural manner in the visual system and are processed in their entirety, while other objects are processed as aggregates of independent elements.2 This
is probably due to the fact that many socially relevant informationsourcesdependontheintegrationfromseveral facialregions,suchasjudgmentsoffacialexpressionsand intentionality.2
The configural processing of faces depends on a sub-cortical system known asCONSPEC, which operates since birth and is sensitive to basic information on the visual characteristicsof faces of thesame species.3 This system
guides the preference for facial patterns (eyes aligned abovethenose andmouth) fromhigh contrastsuptothe first months of life,4---6 before a second system, termed
CONLERN,completesitsmaturation.3,4Thedevelopmentof
theCONLERNsystemdependsonthevisualexperiencewith
human faces.3,4,7 These two systems interact during the
postnataldevelopmentofthevisualsystem.8TheCONSPEC
guides the development of CONLERN;3 any impairment in
its function may affect cortical specialization for faces and,thus,adverselyinfluencethesubsequentprocessingof socialstimuli.4
Experimentsthatinvestigate thesetwosystemsin full-termnewborns withgestationalage >40weeksarewidely foundintheliterature.1,4,5,8---10 However,althoughpreterm
infants are capable of completing all elements of a visual assessment protocol, including thosewith complex answers,6,11nostudyhasassessedthepreferenceforfaces
inpreterminfantsinthefirstfewhoursoflife.
Somestudies12---14 demonstratedanassociation between
preterm birth and several neurocognitive disorders, asso-ciated in one way or another to the processing of facial stimuli,suchasautism12,13andprosopagnosia,14theinability
torecognizefaces.
An orientation by social stimuli maybe a critical con-trolpoint for predicting the trajectoryof social cognitive development.15
experience even during the gestational period,16,17 which
could be hindered in preterm infants due to the lack of intrauterineexperience.Consideringthis perspective,this study aimed toassess thepreference for facialstimuliin pretermnewbornsinthefirsthoursoflife.
Methods
Sample
This wasa pragmatic,cross-sectional,observationalstudy thatmeasured theprevalenceof facialrecognition intwo groups of infants, preterm and full-term. The study was conductedbetweenJuly 2014andDecember2015, witha conveniencesamplefromMaternidadeEscolaJanuárioCicco (Natal, RN, Brazil) and Maternidade Escola Hospital Ana Bezerra (SantaCruz, RN, Brazil).Sample recruitment was carriedoutfromtheadmissionsatthetwohospitalsduring thestudy period.The choiceofa pragmaticexperimental designwasduetoitspracticalityandthepossibilityof sup-plementingthestudy withanepidemiologicalandcultural context.18
Parentsor guardiansof newbornsof both genderswith up to 48h of life, with 33---41 weeks of gestational age, were invited to participate in the study. Gestational age calculatedbythelastmenstrualperiod.Whenthiswasnot possible,datafromtheobstetricultrasonographyperformed inthefirsttrimesterofpregnancywasconsidered.
Infants born between 33and 36 weeksand sixdaysof gestationwere grouped in the preterm group andinfants bornbetween37and41weeksingroupedinthefull-term group.
Hemodynamicallyunstablenewborns(receivinginvasive and/ornon-invasivemechanicalventilation,useof vasoac-tivedrugs),withintraventricularhemorrhagegradeIIIand IV,Apgar score at 5min <5, and whose funduscopicexam presentedabnormalresultswereexcludedfromthestudy. ThestudywasapprovedbytheResearchEthicsCommittee
ofUFRN/FACISA(ProtocolNo.658.852/2014)andallmothers orguardianssignedthefreeandinformedconsentform.
Stimulus
To assess facial recognition, the authors adapted the methodologydescribed by Goren et al., by removing one ofthe boardsfromthe setto reducethe test application timefor pretermbabies,whotendedtofallasleepduring theassessment.19 Therefore, thestimuli consisted of two
whiteboardsshapedasaheadandneck(0.17m×0.19m)
witha blackouter edge.Onecontaineda drawingsimilar tothehumanface(alignedeyesabovethenoseandmouth) andtheother thedrawingofa distortedface(misaligned eyes,mouth,andnose).
Procedure
The test was performed with the participation of two researchersinawell-litandquietroomlocatedinthe hos-pitalandthenewbornswereplacedinthesupineposition ontheexaminer’slap(Fig.1A).Thestimuluswaspresented at15◦ and30◦ angles,totherightandleftofanimaginary
archwitharadiusof0.25mandcenteredonthenewborn’s head.
The examinerwasblindedtothetypeof stimulus pre-sented, which was handed withthe face side (natural or distorted) inverted by the assistant. After the newborn’s gaze was fixated on the stimulus, it was slowly moved along the visual field. The assistant recorded on a form the examiner’s opinion regarding the recognition or not of the stimulus by the newborn. Each board was moved only once to each side; stimulus recognition was consid-eredpresentwhenthebabyshowedeyeorheadmovements towardthepresentedstimulus.19 Theexaminerwas
previ-ouslytrainedtoensurethereproducibilityofthestimulus presentationangles.AblackPVCarchwithangle markings
+30
A
B
+15 –15
–30
Table1 Meanvalues,standarddeviations,andminimumandmaximumvaluesofthesample’sgeneralcharacteristics.
Preterm Full-term p
Totalofnewborns 28 31
---Gender(male/female) 14/14 20/11
---Hoursoflifeattheassessment 30±11.89(10---48) 21±12.13(2---47) 0.55
Gestationalage(weeks) 35±1.11(33---36) 39±1.13(37---41) 0.02
Weight(g) 2044.00±380.54(1260---2904) 3396.13±482.64(2755---4900) 0.37
Apgar1stminute 8±1.91(4---9) 9±0.95(4---9) 0.16
Apgar5thminute 8±0.90(6---10) 9±0.58(7---10) 0.15
p<0.05indicatesastatisticallysignificantdifferencesbetweengroups,Student’sttest.
wasusedduringtraining(Fig.1B)withfivenewbornsthat werenotincludedinthestudy.
The statistical analysis considered the presence or absence of response (1 and 0, respectively) for each of the four positions evaluated. Performance comparison in thetwogroupsregardingrecognitionofstimuli(naturaland distortedface)wasassessedwithpairedt-test,witha sig-nificancelevelof˛=00:05.
Results
During the study period, 73 newborns were assessed; of these, 14 were excluded (four had gestational age <33weeks,threehadmorethan48hof life,fourwereon mechanicalventilation,and threehadApgar at5min<5). Ofthe59infantswhowereincludedinthestudy,28were allocatedinthePRETERMgroup(14girls)and31inthe FULL-TERMgroup(11girls).Table1showsasummaryoftheoverall characteristicsofthesample.
Bothgroupsrecognizedthetwostimulipresented. How-ever, newborns from the preterm group, in addition to showingaloweroccurrence oforientation movementsfor both stimuli, on average (1.8±1.1 for natural faces and
2.0±1.2fordistorted)(Fig.2),showednopreference for
eitherofthem(p=0.35).Inturn,thenewbornsfromthe full-termgroupshowedapreferencefornaturalfaces(p=0.002) and a higher number of orientation movements for the
P=.35
Preterm Full-term
Groups
P=.002 4
3
2
Number of fixations
Natural face
Distorted face
1
0
Figure2 Numberoffixationspernaturalanddistortedfacial stimuliinbothgroupsofinfants:pretermandfull-term.
stimulus, both for natural (3.2±0.8) and distorted faces
(2.5±0.9)(Fig.2).
Discussion
Theresultsindicatethatpretermbabiesdonothaveavisual preferencefornaturalfaces,differentfromnewbornsborn atterm.
Theabilitytoidentifyfacesisanessentialskillfor new-borns, considering their almost complete dependence on theircaregivers.
Turatietal. evaluatedthe facialpreference ofinfants born at term at 3 months of age.20 The results
demon-stratethatthesebabiesshowavisualpreferenceforfacial imagespresentedinacorrectorientation,whencompared withinvertedfaces.Anotherstudyofinfantsbornatterm, assessed within 24h of life, used two stimuli similar to humanfaces,thefirstwiththreeblacksquaresalignedwith the eyes and mouth and a second also with three black squares,butwiththepositionofeyesandmouthinverted. Theresultsshowedapreferenceforthestimulussimilarto thehumanface.5
Goren et al., in their experiments, established that babiesbornat termhave somespecific informationabout the disposition of the features that constitute the face withinonehourafterbirth;morespecifically,infantswith nine minutesof life preferfaces toother stimuli.19
How-ever,allthesestudiesassessedfull-terminfants;4,5,19,20the
interruption of the subcortical system caused by preterm birth may have important consequences for the develop-mentofthemechanisminvolvedinthepreferenceforsocial stimuli.14,21
Studiesof thevisual functionof facialrecognitionalso carriedoutwithpreterminfants, albeitatadifferentage than thatof thepresent study,showed thattheseinfants have an inability to recognize faces, corroborating the presentresults.12,14Theauthorsofthosestudiesdiscussthe
fact thatprosopagnosia canbe aserious neurological dis-orderthatleadstosocialdisability,duetothedifficultyin makingfriendsandparticipatinginsocialactivitiesofdaily living.12,14
Apossiblereasonfortheseresultsisthefactthatpreterm birth exposesasystem withincompletedevelopment.For instance,Takeshitaetal.demonstratedtheimportanceof hapticexplorationby thebabyinbrain maturationduring thelasttrimesterofgestation.22Thestimulifromthetactile
refinethecircuitsresponsibleforthevisualdiscrimination offaces.16 Inthelasttrimesterofpregnancy,fetuseshave
ahigherfrequencyofcoordinatedmovementsoftheupper bodytowardtheface.17
However,inthepresent study,apsychophysical experi-mentwasperformed,withasingleexposureofthenatural facestimulus;theresponsewasnotfilmed,whichmaylimit thediscussionoftheresults.
Therepetitionofthesamestimuluscouldhaveprovided additional information to the newborn and the recording couldhaveassistedinjudgingtheresponse.Consideringthat the repeated presentation of an unknown stimulus could leadtovisualhabituation,theauthorsdecidedforasingle exposure;however,an experimentwiththeorientationof theoculomotorsystemwasperformed.Thisapproachwas chosenbecausethe authorsunderstandthat theCONSPEC mechanism is oriented by the oculomotor system4,19 and
suchprocedure couldbeusedevenin newborns admitted atthehospitalafewhoursafterbirth,beingausefultool forthediagnosisofpossibleneurocognitivealterations.
The video recording of the experimentwas attempted withdifferentcamerapositions, duringthetrainingphase withthefiveinfantsnotincludedinthestudy,butnoneof thepositions wasenoughtocatch eyemovement without arousingthenewborn’sinterest.Then,theauthorsdecided toinclude a second researcher topresent the cards face down to the examiner, which made the examiner’s judg-mentblindedtothetypeofstimuluspresented.However, it is important to emphasize that this is the first study that showed differences in orientations for social stimuli betweenpretermandfull-terminfants,withinafewhours oflifeafterbirth.Frieetal.14demonstratedsimilarresults
with 27 preterm infants, but the latter were assessed at 6monthsof correctedageand10monthsofchronological age.Therefore,theauthorsbelievethatthepresentresults are particularly important in light of the possible conse-quencesthatthislackoforientationinpreterminfantscan have on the development of the system specialization to processsocialstimuli.
Despitethelimitationsofthepresent study,theresults indicatethatpreterminfantsdidnotshowapreferencefor natural faces;however, furtherstudies arerequired,with largersamplesanddifferentprematurityprofiles toreach moredefinitiveconclusions.
Funding
Conselho Nacional de Desenvolvimento Científico e Tecnológico ---CNPQ.UniversalEdict, ProcessNo.484997/ 2013-0
Conflicts
of
interest
Theauthorsdeclarenoconflictsofinterest.
Acknowledgements
The authorswouldliketothanktheConselhoNacionalde DesenvolvimentoCientíficoeTecnológico---CNPQ.
References
1.deHeering A, TuratiC,RossionB,Bulf H,Goffaux V,Simion F.Newborns’facerecognitionisbasedonspatialfrequencies below0.5cyclesperdegree.Cognition.2008;106:444---54.
2.FrankMC,AmsoD,JohnsonSP.Visualsearchandattentionto facesduringearlyinfancy.JExpChildPsychol.2014;118:13---26.
3.JohnsonMH,SenjuA,TomalskiP.Thetwo-processtheoryofface processing:modificationsbasedontwodecadesofdatafrom infantsandadults.NeurosciBiobehavRev.2015;50:169---79.
4.SimionF,GiorgioED.Faceperceptionandprocessinginearly infancy: inborn predispositions and developmental changes. FrontPsychol.2015;6:969.
5.NakanoT,NakataniK.Corticalnetworksforfaceperceptionin two-month-oldinfants.ProcBiolSci.2014;281,pii:20141468.
6.RicciD,RomeoDM,SerraoF,GalliniF,LeoneD,LongoM,etal. Earlyassessmentofvisualfunctioninpreterminfants:howearly isearly.EarlyHumDev.2010;86:29---33.
7.PascalisO,KellyDJ.Theoriginsoffaceprocessinginhumans: phylogenyandontogeny.PerspectPsycholSci.2009;4:200---9.
8.Bednar JA,Miikkulainen R.Neonatal learningof faces: envi-ronmentalandgeneticinfluences.In:Proceedingsofthe24th AnnualConferenceoftheCognitiveScienceSociety.2002.p. 107---12.
9.Heron-Delaney M, Wirth S, Pascalis O. Infants’ knowledge of their own species. Philos Trans R Soc Lond B Biol Sci. 2011;366:1753---63.
10.CraigheroL,LeoI,UmiltàC,SimionF.Newborns’preference forgoal-directedactions.Cognition.2011;120:26---32.
11.Atkinson J, Anker S, Rae S, Hughes C, Braddick O. A test battery ofchilddevelopmentfor examiningfunctional vision (ABCDEFV).Strabismus.2002;10:245---69.
12.LampiKM,LehtonenL,TranPL,SuominenA,LehtiV,Banerjee PN,etal.Riskofautismspectrumdisordersinlowbirthweight andsmallforgestationalageinfants.JPediatr.2012;161:830---6.
13.JohnsonS,MarlowN.Pretermbirthandchildhoodpsychiatric disorders.PediatrRes.2011;69,11R-8R.
14.FrieJ,PadillaN,ÅdénU,LagercrantzH,BartocciM.Extremely Preterm-borninfantsdemonstratedifferentfacialrecognition processesat6---10monthsofcorrectedage.JPediatr.2016;172, 96-102.e1.
15.GomesPT,LimaLH,BuenoMK,AraújoLA, SouzaNM. Autism inBrazil:asystematicreviewoffamilychallengesandcoping strategies.JPediatr(RioJ).2015;91:111---21.
16.ShibataM,FuchinoY,NaoiN,KohnoS,KawaiM,Okanoya K, etal.Broadcorticalactivationinresponsetotactilestimulation innewborns.Neuroreport.2012;23:373---7.
17.KurjakA,AzumendiG,VecekN,KupesicS,SolakM,VargaD, etal.Fetal handmovements andfacialexpressioninnormal pregnancystudied byfour-dimensional sonography. JPerinat Med.2003;31:496---508.
18.PatsopoulosNA.Apragmaticviewonpragmatictrials.Dialogues ClinNeurosci.2011;13:217---24.
19.Goren CC,Sarty M,Wu PY.Visual followingand pattern dis-criminationofface-likestimulibynewborninfants.Pediatrics. 1975;56:544---9.
20.TuratiC,ValenzaE,LeoI,SimionF.Three-month-olds’visual preferenceforfacesanditsunderlyingvisualprocessing mech-anisms.JExpChildPsychol.2005;90:255---73.
21.Zhao K, YanWJ, ChenYH, ZuoXN, FuX. Amygdalavolume predictsinter-individualdifferencesinfearfulfacerecognition. PLOSONE.2013;8:e74096.
