Early Left-Planum Temporale Asymmetry in newborn monkeys (Papio anubis): A longitudinal structural MRI study at two stages of development

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Early Left-Planum Temporale Asymmetry in newborn

monkeys (Papio anubis): A longitudinal structural MRI

study at two stages of development

Yannick Becker, Julien Sein, Lionel Velly, Laura Giacomino, Luc Renaud,

Romain Lacoste, Jean-Luc Anton, Bruno Nazarian, Cammie Berne, Adrien

Meguerditchian

To cite this version:

Yannick Becker, Julien Sein, Lionel Velly, Laura Giacomino, Luc Renaud, et al..

Early

Left-Planum Temporale Asymmetry in newborn monkeys (Papio anubis): A longitudinal

struc-tural MRI study at two stages of development.

NeuroImage, Elsevier, 2021, 227, pp.117575.

ContentslistsavailableatScienceDirect

NeuroImage

journalhomepage:www.elsevier.com/locate/neuroimage

Early

Left-Planum

Temporale

Asymmetry

in

newborn

monkeys

(

Papio

anubis

):

A

longitudinal

structural

MRI

study

at

two

stages

of

development

Yannick

Becker

_,

_Julien

_Sein

_,

_Lionel

_Velly

_,

_Laura

_Giacomino

_,

_Luc

_Renaud

_,

Romain

Lacoste

_,

_Jean-Luc

_Anton

_,

_Bruno

_Nazarian

_,

_Cammie

_Berne

_,

Adrien

Meguerditchian

a Laboratoire de Psychologie Cognitive, UMR 7290, Université Aix-Marseille / CNRS, 13331 Marseille, France b Institut des Neurosciences de la Timone, UMR 7289, Université Aix-Marseille / CNRS, 13005 Marseille, France c Station de Primatologie, CNRS, UPS846, 13790 Rousset, France

a

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t

i

c

l

e

i

n

f

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The“language-ready” braintheorysuggeststhattheinfantbrainispre-wiredforlanguageacquisitionprior tolanguageexposure.Asapotentialbrainmarkerof suchalanguagereadiness,a leftwardstructuralbrain asymmetrywasfoundinhumaninfantsforthePlanumTemporale(PT),whichoverlapswithWernicke’sarea.In thepresentlongitudinalinvivoMRIstudyconductedin35newbornmonkeys(Papioanubis),wefoundasimilar leftwardPTsurfaceasymmetry.Follow-uprescanningsessionson29juvenilebaboonsat7-10monthsshowedthat suchanasymmetryincreasesacrossthetwoagesclasses.Theseoriginalfindingsinnon-linguisticprimateinfants stronglyquestiontheideathattheearlyPTasymmetryconstitutesahumaninfant-specificmarkerforlanguage development.SuchasharedearlyperisylvianorganizationprovidesadditionalsupportthatPTasymmetrymight berelatedtoalateralizedsysteminheritedfromourlastcommonancestorwithOld-Worldmonkeysatleast 25–35millionyearsago.

1. Introduction

Languageanditstypicalfunctionalandstructuralasymmetricbrain organizationwereinitiallyconsideredasuniquetoHomosapiens evolu-tion(Crow,2004),suggestingaspecific“language-ready” braindating backto350000ago.Therefore,brainlateralizationinseveralregions washypothesizedasoneofthekeyfeaturesofthelanguage-readybrain, asmosthumansshowagreatercorticalactivationinthelefthemisphere formostlanguagefunctions(Vigneau etal.,2006).Forinstance,the leftPlanumTemporale(PT)-aregionwhichoverlapswithWernicke’s area-wasfoundparticularlyactivatedinavarietyofauditorylanguage processingtaskslikephonologicalauditorydecoding(Shapleskeetal., 1999)andincludingthemainperceptioncomponentoftheaudio-motor loopforphonologicalprocessing(Vigneauetal.,2006).Inthe pioneer-ingworkofGeschwindandLevitsky(1968),aleftward PT asymme-trywasalsofoundattheanatomicallevel,suggestingitsrelationship withfunctionalbrainasymmetryforlanguagetasks(Josseetal.,2006;

Tzourio-Mazoyeretal.,2018).

Abbreviation:PT,PlanumTemporale.

∗_{Correspondingauthorat:LaboratoiredePsychologieCognitive,UMR7290,Université Aix-Marseille/CNRS,13331Marseille,France.}

E-mailaddress:adrien.meguerditchian@univ-amu.fr(A.Meguerditchian).

Additionally, the“language-ready” braintheory suggeststhatthe infant brain is pre-wired for language acquisition (e.g. Dehaene-Lambertz etal.,2002).Indeed,studieshave reportedthatallhuman infantsseemtohaveaninnate,inheritedreadinessforlanguage acqui-sition,independentlyfromculture.Forinstance,newbornsareinitially abletodistinguisheveryphonemebeforeselectivelydiscriminatingonly phonemesrelatedtothelanguagetheyareexposedtoKuhletal.(2008). During their first year, infants will be also sensitive to vocal sounds,their nativeprosodyandvowels,infertheabstractstructure ofspeechandconnectwordstotheirreferents(Dehaene-Lambertzand Spelke,2015).

Theneuralstructureforsuchalanguagereadinessremainsunclear. Nevertheless,whiteandgreymatterorganizationininfantsreveals sim-ilararchitectureincomparisonwithadults(Duboisetal.,2010). Inter-estingly,similartoadults,three-month-oldinfants’BOLDresponsesto speechshowedamorepronouncedactivationofthePTintheleft hemi-sphere(Dehaene-Lambertzetal.,2002),rasingthequestionwhetheror not thePTmightbefunctionallylateralizedfrombirthon.

Addition-https://doi.org/10.1016/j.neuroimage.2020.117575

Received27July2020;Receivedinrevisedform8October2020;Accepted16November2020 Availableonline4December2020

1053-8119/© 2020TheAuthor(s).PublishedbyElsevierInc.ThisisanopenaccessarticleundertheCCBY-NC-NDlicense (http://creativecommons.org/licenses/by-nc-nd/4.0/)

Y. Becker, J. Sein, L. Velly et al. NeuroImage 227 (2021) 117575 ally,structuralPTleftwardasymmetrywasalsoshowninpost-mortem

fe-tusesorinfantbrainsinearlydevelopment(WitelsonandPallie,1973;

Wada,1975;Chietal.,1977)andwithin-vivostructuralMRIimages (Duboisetal.,2010;Hilletal.,2010;Glaseletal.,2011).Sucha struc-turalPTleftasymmetrymaybestablishedduringthelasttrimesterof fetallife(Chietal.,1977)andarelaterincreasingduringdevelopment, suggestingitslinkswithlanguagedevelopment(Chietal.,1977).

However, several studies in nonhuman primates questioned the structural PT asymmetry as a human-specific marker for the brain specialization for language.Manual delineation of post-mortembrain (Gannon et al., 1998) and in-vivoMRI scans(Hopkins etal., 1998;

HopkinsandNir,2010;Marieetal.,2018),showedlargerleftPTsin bothapesandbaboons,suggestingthatthisneuroanatomicalfeatureis sharedalsowithOld-Worldmonkeys.

Whethersuchanearlyneuroanatomicalfeatureextendedtoother nonhumanprimateinfantsisunknownalthoughthiscomparative ques-tionremainscriticalfordetermining itssupposedhumanuniqueness troughevolutionanditsrelationtoapre-wiredbrainforlanguage ac-quisition.

Therefore,theaimofthepresentlongitudinalin-vivoMRIstudyin nonhumanprimatesistoinvestigate,thestructuralneuroanatomicalPT

asymmetriesin35babooninfants(Papioanubis)andits development acrossagethroughmanualdelineationoftheregion’ssurface.The ear-liestpost-natalageclassincludes33newbornsatthecritical neurodevel-opmentalperiodbelow3months(aswellastwo5-monthsoldoutliers) inwhichthesynaptogenesisismaximalandthemyelin,synapsesand cellbodiesarethusnotfullymature(Scottetal.,2016).Thefollow-up MRIlongitudinalscanningandPTdelineationincludes29ofthose35 baboonsattheolderjuvenileageclass(i.e.,from7to10months). 2. Methods

2.1. Subjects

Subjectsrangedfrom4to165daysofage(Mean:32.63;SD:6.13) andincluded21males and14 females.Outofthose35baboons,29 werelaterrescannedasecondtime,rangingfrom218to362daysof age(Mean=278.62;SD=30.11)(seetableinsupplementarymethods withsubjects’details).

AllmonkeysarehousedinsocialgroupsattheStationde Primatolo-gieCNRS(UPS846,Rousset,France)andhavefreeaccesstooutdoor areasconnectedtoindoorareas.Allsubjectsarebornincaptivityfrom 1(F1)or2generations(F2).Woodenandmetallicstructuresenrichthe enclosures.Feedingtimesareheldfourtimesadaywithseeds,monkey pelletsandfreshfruitsandvegetables.Waterisavailableadlibitum.

2.2. Animalhandling

Minimallyinvasivemedicationwasrealized,andnopremedication wasneeded.Mothers fromthenewbornsubjectswerecaptured with theirinfantthenightbeforethescanattheStationdePrimatologiefor check-upsandweretransportedtogetherthefollowingdayoftheMRI session.

Upon arrival at the MRI center, the mother of the focal subject wassedatedwithanintramuscularinjectionofketamine(3mg/kg)and medetomidine(30𝜇g/Kg)aswellastheirfocalinfantifabove5months old. Focal newborn below 5 months were not sedated anddirectly broughttothepreparationroom forthefollowingprocedures. Focal infantswerethenanesthetizedunder6-8%sevofluraneinductionwith amask.Acatheterwastheninsertedintothecaudalarteryforblood-gas sampling,andtrachealintubationwasperformedforsteadycontrolled ventilationusingananestheticventilator(Cato,Drager,Germany). End-tidalcarbondioxidewasmonitoredandusedtoadjustventilationrate (0.2to0.3Hz)andend-tidalvolume.TheanesthesiainsidetheMRI machinewasthenmaintainedusing 3%sevofluranevia acalibrated

vaporizerwithamixtureofair0.75L/minandO20.1L/min).

Periph-eraloxygensaturation,heartrateandbreathingrate,weremonitored throughoutexperiments.

All animal procedures were approved by the “C2EA -71 Ethi-cal Committee of neurosciences” (INTMarseille) under the number APAFIS#13553-201802151547729v4,andhasbeenconductedatthe StationdePrimatologieunderthenumberagreementC130877for con-ductingexperimentsonvertebrateanimals(Rousset-Sur-Arc,France). All methodswereperformedinaccordance withtherelevantFrench law, CNRSguidelinesandtheEuropean Unionregulations(Directive 2010/63/EU).

2.2.1. Imagingprotocol

FromSeptember2017toMarch2020,in-vivoimagingwasperformed usinga3TclinicalMRIscanner(MAGNETOMPrisma,Siemens, Erlan-gen,Germany)equippedwith80mT/mgradients(XR80/200gradient systemwithslewrate200T/m/s)anda2-channelB1transmitarray (TimTX TrueForm).Forthesessionsatt0(“newborn” ageclass)and att1(i.e.,from7to10monthsold),theanimalswerescannedinthe supineposition,withtwo11cmreceive-onlyloopcoils:oneunderthe headandanotheronearoundthefaceoftheanimal.Theholdingofthe twocoilsandtheanimalheadwasprovidedthroughtheuseofa pearl-tecbag(VacFixSystem)andsomestraps.Protectionfornoisereduction wasattachedaroundtheears.AttheendoftheMRIsession,whenfully awakedfromanesthesia, baboonswerecarefully putbackwiththeir motherandthentransportedbackattheStationdePrimatologiefor im-mediate(ordelayed)reintroductionintotheirsocialgroupsunderstaff monitoring.

2.2.2. Structuralacquisitionprotocol

T1w images were acquired using a 3D Magnetization Prepared Rapid Acquisition Gradient Echo (MPRAGE) (Mugler and Brooke-man, 1990) sequence(0.4 mmisotropic, FOV= 103×103×102.4 mm,matrix=256×256slicesperslab=256,sagittalorientation, read-outdirectionofinferior(I)tosuperior(S),phaseoversampling=10%, averages=3,TR=2500ms,TE=3.01ms,TI=900ms,flip-angle=8°, bandwidth=300Hz/pixel,nofatsuppression,pre-scannormalization). T2wimageswereacquiredusingaSamplingPerfectionwithApplication optimizedContrastusingdifferentangleEvolutions(SPACE)sequence (Mugleretal.,2000)(0.4mmisotropic,FOV=154×115.5×102.4 mm,matrix=384×288,sliceperslab=256,sagittalorientation, read-outdirectionItoS,phaseoversampling=0%,averages=2,TR=3200 ms,TE=393ms,bandwidth=566Hz/pixel,nofatsuppression,echo trainlength=790msandpre-scannormalization).Thetotalacquisition timeforstructuralscanswas65min(35minforT1wand30minfor T2w).

2.3. PreprocessingofanatomicalMRI

AnatomicalT2wimagesofthefirstscanningsessionandanatomical T1wimagesofthesecondscanningsessionwerenoisecorrectedwiththe spatiallyadaptivenonlocalmeansdenoisingfilter(Manjónetal.,2010) implementedinCat12toolbox(http://www.neuro.uni-jena.de/cat/) in-cludedinSPM12(http://www.fil.ion.ucl.ac.uk/),whichrunson MAT-LAB(R2014a).

Next,eachimagewasmanuallyorientedusingITK-Snap3.6 accord-inganteriorandposteriorcommissuresplaneandtheinterhemispheric fissureplane.

2.4. ManualdelineationofthePT

ManualdelineationofthePTinthepresentstudyfollowedthesame procedurethanthepreviousMRIstudyonthePTasymmetryofadult baboons(Marieetal.,2018).However,becauseoftheimmaturebrains ofthenewbornsubjects,T2wMRIsignalwasusedinsteadofT1wMRI signalformanualdelineationforthefirstlongitudinalscans.

Infact,theT2wMRIsignalissensitivetothefreewaterpresentin voxels.Theproliferationofmembranesduetosynaptogenesisandthe processofmyelinationwilldecreasetheproportionoffreewaterinthe graymattervoxelsandthusdarkentheimagesduringmaturationofthe firsthumanyearpost-natal.Therefore,ahighercontrastisgeneratedin comparisontoT1wimagesinearlyimmaturebrains,whichhelpsfor betterdelimitation(Dehaene-LambertzandSpelke,2015).

Followingtheproceduresusedinhumans(Larsenetal.,1989),great apes(Hopkinsetal., 1998;HopkinsandNir,2010; Cantalupoetal., 2003)andOld-Worldmonkeys(Marieetal.,2018;Lyn etal.,2011), thesurfaceofthePThomologwasmeasuredinthecoronalplane.

TheT2w imagesof every subject wereimported in ITK-Snap.In there,theregionofinterestwasmanuallytracedinthecoronalplanon theindividualnativespacewiththeITK-Snaptool“Paint-BrushMode” withfeatureroundbrushsize1,usingatouchpad-drivenpointer (Wa-comCintiq® 13HD).

Coronalplaneswereusedbecausetheydisplaythefulldepthofthe sylvianfissure,ofwhichthePlanumTemporaleisitsfloor.Asdescribed byMarieetal.(2018),delineationofthePTwasperformedasfollowed: TheposteriorborderofthePTwascharacterizedbythelastcaudalslice displayingtheSylvianfissure.Theanteriorborderwasdefinedbythe fullclosureof theInsulasulcusandgreymatter.This techniquewas chosenduetotheinconsistencyofthepresenceoftheHeschl’sgyrus (seeMarieetal.,2018;Lynetal.,2011 fordiscussions).

Foreachslice,thedelineationwastracedonthemostventral bound-arybetween thesulcusandthegreymatter.Inorder tobalancethe rater’spossiblehandednessbias,tracingforeachsubjectwasrandomly undertakeneitherfromthemostmedialtothemostlateralpixelofthe Sylvianfissureorfromthemostlateraltothemostmedialpixel.This stepwasrepeatedonthenextslice,movingposteriorlyuntiltheSylvian fissurefelloutofview.

Next,asurfaceareawasgeneratedacrossallslicesforeach hemi-sphereindependentlyinagivensubject(seeFig.1.A).Foreachsubject, anAsymmetryQuotient(AQ)oftheleft(L)andtheright(R)surface areaswascomputedAQ=(R– L)/[(R+L)×0.5]withthesign in-dicatingthedirectionofasymmetry(negative:leftside,positive:right side)andthevalue,thestrengthofasymmetry.Further,asreportedby

HopkinsandNir(2010)forhumansandgreatapes,theAQwasalsoused toclassifythesubjectsasleft-hemisphericbiased(AQ≤–0.025),right biased(AQ≥0.025),ornonbiased(–0.025<AQ<0.025).Athreshold of0.025representsa2.5%differenceinsurfaceareabetweenleftand rightPT.

Asecondrater,blindtotheside,confirmedthemeasuresofthePT

inasubsampleof15individualsforbothhemispheres(interrater corre-lationcoefficientfor30PTtracingwasr(30)=0.94,p<0.0001).

2.5. Statistics

StatisticswereconductedwithR3.6.1(RCoreTeam(2017).R:A lan-guageandenvironmentforstatisticalcomputing.RFoundationfor Sta-tisticalComputing,Vienna,Austria.URLhttps://www.R-project.org/.)

3. Results

3.1. PTstructuralasymmetry

WefoundasignificantleftwardasymmetryofthePTsurfaceata group-levelin35newbornbaboons(t0)accordingtoaonesamplet-test inthe35subjects’AQscores(seeFig.1.B),MeanAQ=-0.058±0.067 SD;t(34)=-5.15,p<0.0001.CategorizationofindividualAQshowed alsoamajorityofleftwardPT-biasedindividuals(seeFig.1.C):25 ba-boonsexhibitedaleftwardhemisphericPTbias(71.4%)whereas2 ex-hibitedarightwardPTbias(5.7%)and8noPTbias(22.9%),a distribu-tionquasi-identicalthantheonefoundinhumaninfants(Wada,1975). Wefoundnodifferenceofdistributionbetweeninfantbaboonsand in-fanthumans accordingtochi-square(p=0.25forthreegroups“Left

bias,Rightbias,nobias” andp=0.20fortwogroups“Leftbias,Right bias”). Thenumber of leftward PT-biased baboonswas significantly greaterthanthenumberofrightwardPT-biasedsubjectsaccordingto chi-squaretest(𝜒2=19.59,p<0.0001).

3.2. Ageclasses’comparisonofPTlateralization’sstrength

Follow-upanalysisamongthe29rescannedbaboonswhenreaching 7to10monthsofage(t1)showedasignificantincreasedstrengthof thePTasymmetry(MeanAbsoluteAQscore,M.=0.105±0.065SD) incomparisontotheirearliestageclassaccordingtoapairedsample t-test(MeanAbsoluteAQscore,M.=0.073±0.049SD),t(28)=-2.39,

p=0.024(seeFig.1.D)aswellasasignificantcorrelationbetweenthe twoMRIsessions,r(29)=0.55,p<0.002.

3.3. Left,rightPTsurfaceareas

At t0, the mean PT surface areas were in the left hemisphere:

M.= 50.34mm2 _{±9.27SD(inmales M. =51.07 mm}2 _{± 9.80SD;}

inFemalesM.=49.24mm2_{±9.17SD);andintherighthemisphere:} M.=47.44mm2_{±8.93SD(inmalesM.=48.53mm}2_±9.35SD;in

FemalesM.=45.79mm2_±7.78SD).

At t1, the mean PT surface areas were in the left hemisphere:

M.=58.48mm2 _{±8.0SD(inmalesM.=59.23mm}2_±8.07SD;in

Females M. =57.67 mm2 _{±7.75SD); andin therighthemisphere:} M.=55.73mm2_{±8.65SD(inmalesM.=57.07mm}2_±9.99SD;in

FemalesM.=54.28mm2_±6.64SD). 3.4. Age,sex,brainsizeeffect

MultiplelinearregressionanalysesshowedthattherightPTsurface (p=0.001),theleftPTsurface(p=0.02)andage(p=0.033)predict

PTasymmetrystrengthbutnotthesubject’ssexandbrainvolume.At t0andt1,nosignificantdifferencesofmeanAQs,meanLeftPTsurface, andofmeanRightPTsurfacewerefoundbetweenmalesandfemales. 4. Discussion

Ourresultsshowedthatearlypost-natalnonhumanprimateinfants present a significant human-like neuroanatomical asymmetry of the Planum Temporalesurface(PT) infavor ofthelefthemisphere.This findingisclearlyconsistentwithearlyPTasymmetryfoundinhuman newbornsandinfants(Chietal.,1977;Duboisetal.,2010;Glaseletal., 2011;Hilletal.,2010;Wada,1975;WitelsonandPallie,1973)although measurementmethods,Left-Right-Ambiclassificationthresholdand sta-tisticalpowerintermsofsamplesizedifferaswellasageclass equiva-lencewhichoverallmakeinterspeciescomparisonchallenging. Never-theless,thedistributionisquasi-identicaltotheonesreportedinboth humaninfantsandhumanadults(GeschwindandLevitsky,1968)but alsoinadultchimpanzees(HopkinsandNir,2010)andadultbaboons (Marieetal.,2018).Ourfindings arealsosomewhatconsistentwith averaged-brainleftwardasymmetriesfoundininfantRhesusmacaques withinlargetemporalclusterswhichseemtooverlapwithPTaccording toanautomatedsource-basedmethod(Xiaetal.,2019).Sucha sim-ilarage-relatedphenomenonwasalsodescribed inhumaninfantsby

Wada(1975).Interestingly,wefoundthatthedirectionofindividualPT

asymmetryisconsistentacrossageclasseswhileitsstrengthisincreasing withage.Incontrast,nosexorbrainsizeeffectswerefoundon direc-tionorstrengthofPTasymmetry.Thisfindingisnotconsistentwiththe ideathatincreaseinPTasymmetryinHominidaeevolutionwasdueto increaseinbrainvolume(Pilcheretal.2001).Additionally,ifstrength ofPTasymmetryisaffectedbysexinhumanadults(Hirnsteinetal., 2019),itseemsnotthecaseinadultbaboons(Marieetal.,2018), in-fantbaboonsandhumaninfants(Duboisetal.2010).

Thisfindinginanon-linguisticspeciesclearlyquestionsthe histori-calideathatsuchamaturationaleffectofthePTasymmetry’sstrength

Y. Becker, J. Sein, L. Velly et al. NeuroImage 227 (2021) 117575

Fig.1. (A)RepresentationoftheasymmetricPlanumTemporale(PT)inthebaboonbrainonaT2wimageaccordingtoacoronalsection,3Dbrainrenderand obliquesectionorientedalongtheSylvianFissure(theleftPTisinredandtherightPTingreen).(B)MeanAsymmetryquotient(AQ)forthePlanumTemporale surfaceofthenewborninfantbaboons(N=35).NegativeMeanAQscoreindicatesleftwardhemisphericasymmetryatapopulation-level.Thelongblackline representsthemedian,thewhiteshortlinethemean.∗∗∗_{p<0.0001(C)Subjectsdistribution(inpercentage)asafunctionofthedirectionoftheirPTasymmetryin}

babooninfants(N=35,inred)versusinhumaninfants(N=100,inblue,fromWada,1975).(D)VariationofstrengthofthePlanumTemporalesurface’sasymmetry (MeanabsoluteAQscore)amongthe29baboonsscannedlongitudinallyattwoearlystagesofdevelopment:Newborn(inred)versusJuveniles(i.e.,from7to10 monthsinblue).∗_p<0.05.

is relatedtolanguagedevelopment in humaninfants (Wada, 1975). One couldask whethertheexistence oftheasymmetry shortlyafter birthhasaninnate,andthus,geneticcomponentashypothesizedfor humaninfants(Hilletal.,2010)or towhat extentitisrather influ-encedbypre-andpost-natalexperience.Inanycase,thecollective find-ings clearlyprovide additionalsupportfor thephylogenetic continu-itybetweenhumanandnonhumanprimatespeciesaboutsuchabrain asymmetricfeature.Suchacontinuityextendedattheearliest postna-talstageofdevelopmentacrossbothspeciesmayquestiontheearlyPT

asymmetryasahumannewborn-specificmarkerofthelanguage-ready brain.

Structurallateralizationofsuchalanguageareamaynotsolely ac-countforapre-wiredbrainforlanguageacquisitionasitwassupposed forhumanbabies(Dehaene-Lambertzetal.,2002).

However,itremainsunclear which factoris drivingsucha com-monearlyasymmetricfeatureofthebrainanatomyamonghumanand nonhumaninfants. One potential explanation is that earlyPT struc-turalasymmetrymighthavenothingtodowithdevelopmentof lan-guagelateralization,givensomestudiesinadultsreportednomatch be-tweenstructuralandfunctionalasymmetryofthisregion(Keller,2011;

Greve,2013).

Nevertheless,themostrecentstudyaddressingthisquestioninadults contradictssuchahypothesis(Tzourio-Mazoyeretal.,2018).Although the lackof matchwas confirmed between structural and functional asymmetryofthePTinalanguagetask,structuralPTasymmetrywas foundassociatedwithfunctionallateralizationofanadjacentauditory areaattheendoftheSylvianfissure,suggestingitslinkswithlanguage lateralization.

Therefore,anotherpotentialexplanationisthattheearlyPT struc-turalasymmetryinbothhumanandnonhumaninfantsmightpredict thedevelopmentofhomologcommunicativefunctions,whichstillform a foundationfor coreaspectsof thehumanlanguagesystem. Deter-mining such commondeveloping functionsbetween speciesremains highlyspeculative,giventhelackoflongitudinalstudiesininfantson theemergenceofbrain-behaviorrelationships.Nevertheless,basedon neuroimagingstudiesinnonhumanprimatefocusingonadults,itmight benotexcludedthatsharedpropertiesofcommunicativesystemsin hu-manandnonhumanprimatescouldberelatedtoPTstructural asym-metry. For instance,previous studiesin monkeys andapes have re-portedhuman-likefunctionallateralizationforprocessing conspecific calls.However,itsoverlapwithPTanatomicalregionremainsunclear aswellasthedirectionofthefunctionallateralization(i.e.,towardleft

versus right hemisphere) which are inconsistent across the liter-ature (e.g. Poremba et al.; 2004; Gil-da-Costa and Hauser 2006;

Petkovetal.2008;Jolyetal.,2012).Alternatively,someauthorshave proposedthatpropertiesofthecommunicativegesturalsystemin non-humanprimates couldconstitute anotherpotential functional candi-dateof PTspecialization.Infact,whereas productionof communica-tivemanualgestureshavebeenfoundhighlylateralizedinfavorofthe right-handinboth baboonsandchimpanzees(Meguerditchianetal., 2013),acontralateralrelation betweenPTstructuralasymmetryand handpreferencesforcommunicativegesturewasreportedinadult chim-panzees(HopkinsandNir,2010;Meguerditchianetal.,2012).These lat-terfindingshavethussuggestedthatsharedpropertybetweengesture signalinginapesandlanguagesystemin humansmightbeboth ulti-matelyrelatedtothisasymmetryfeatureofthetemporallobeanatomy (Meguerditchianetal.,2012).Whethersimilargesturalfunctional spe-cializationofthestructuralPTasymmetryexistsinbaboonshasbeennot investigatedyetalthoughbothchimpanzeesandbaboonshaveshown similarleftwardstructuralasymmetryofthePTaswellassimilar right-wardpatternsofgesturalcommunication’smanuallateralization.

Furtherstudiesinoursampleofinfantbaboonswouldhelpus de-terminatethepotentialrelationshipbetweentheseearlyPTstructural asymmetryanddevelopmentofmanuallateralizationofcommunicative gestures.

Inconclusion, the presentfinding in nonhuman infants provides additionalsupporttothehypothesisof acontinuity between nonhu-manandhumanprimatesconcerningleftwardstructuralPTasymmetry. Sharingsuchananatomicalfeatureofthebrainatthisearlier postna-talstageofdevelopmentreinforcedthustheideaofitscommonorigins fromourdistantevolutionaryancestor,datedback25–35millionyears ago,althoughitspotentiallinkwiththelanguage-readybrainremains anopenquestion.

Declaration of Competing Interest Authorsdeclarenocompetinginterests. Acknowledgments

General: WeareverygratefultothevetMarieDumasyfor supervis-ingthefirsthealthandanesthesiamonitoring,EmilieRaphaforgreat assistanceandanimalcare,FredericCharlin,aswellasthecarestaff of theStationdePrimatologie,suchasValérieMoulin,BrigitteRimbaud, RichardFrancioly,thevetsPascalineBoitelle,AlexiaCermolacce& Jan-nekeVerschoor,andthebehavioralmanagerPauMolina.Wethankalso KepKeeLohforEnglishcorrections.

Funding

TheprojecthasreceivedfundingfromtheEuropeanResearch Coun-cilundertheEuropeanUnion’sHorizon2020 researchandinnovation programgrantagreementNo716931 -GESTIMAGE-ERC-2016-STG (P.I.AdrienMeguerditchian),fromtheFrench“AgenceNationaledele Recherche” ANR-16-CONV-0002(ILCB)andtheExcellenceInitiativeof Aix-MarseilleUniversity(A∗_{MIDEX).ThisMRIacquisitionsweredone}

attheCenterIRM-INT(UMR7289,AMU-CNRS),platformmemberof FranceLifeImagingnetwork(grantANR-11-INBS-0006).

Author contributions

Y.BandA.Mpreparedthepaperandtherevision. Y.B.performed the tracing andanalyses. C.B. performed the interrater tracing. J.S. parametrized theMRI sequences andoptimizedthe MRI acquisition setup.B.N.designedthebaboons’monitoringprograms.L.V.,L.R.,R.L. andL.G.designedthespecificproceduresofwelfare,anesthesia, mon-itoringandpreparationof baboonsin theMRImachine. J.L.A super-visedandcoordinatedtheMRIsession.A.M.designedandsupervised thestudyandMRIacquisitions.

Data and materials availability

Alldataisavailableinthesupplementarymaterials. Data availability statement

Ourdatawillbeavailableonlineuponpublicationandisattached tothissubmissioninthesupplementarymaterial.

Supplementary materials

Supplementarymaterialassociatedwiththisarticlecanbefound,in theonlineversion,atdoi:10.1016/j.neuroimage.2020.117575. References

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