Developmental changes in the linguistic brain after puberty
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2 164 Updat TRENDS in Cognitiv Scincs Vol.9 No.4 April 2005 Rsarch Focus Dvlopmntal changs in th linguistic brain aftr pubrty Alic M. Provrbio 1 and Albrto Zani 2 1 Univrsity of Milano-Bicocca, Piazza dll Atno Nuovo 1, Milan, Italy 2 Institut of Molcular Bioimaging and Physiology, National Rsarch Council (CNR), Via Fratlli Crvi 93, Sgrat (Milan), Italy Th dvlopmnt of rading skills is a complx and vry long-lasting procss. In an influntial study Booth t al. dmonstratd ag-rlatd changs in th activation of a ntwork of lft hmisphr rgions, including th infrior frontal ara, th suprior tmporal gyrus, and th angular gyrus. Intrstingly, thy found that th angular gyrus, which is involvd in th mapping btwn phonological and orthographic rprsntation, is automatically activatd in adults during visual orthographic tasks not rquiring this opration. Corrsponding authors: Provrbio, A.M. (mado.provrbio@unimib.it), Zani, A. (albrto.zani@ibfm.cnr.it). Rading rlis on th fast and accurat convrsion of orthographic charactrs into thir phonological rprsntations. As a rsult of yars of training and xposur to writtn and spokn languag, skilld radrs hav fastr and automatic accss to phonology whn rading and to orthography whn listning [1,2]. Although this might sm obvious, th mchanisms involvd in th dvlopmnt of rading skills hav still not bn thoroughly invstigatd. Nuroimaging rsarch has providd usful information about which brain rgions ar activ during rading in adults (s Figur 1). Ths sam aras sm to b abnormally activatd in dyslxic childrn [3]. Howvr, th ffcts of post-pubrtal brain maturation and xtnsiv ducation rmain largly
3 Updat TRENDS in Cognitiv Scincs Vol.9 No.4 April Angular gyrus (BA 39) Tabl 1. Exampls of words (with phontic transcription) usd in th various tasks in th study by Booth t al. [5] Task: visual or auditory Similar orthography Dissimilar orthography Rhyming SEAT [sit] HOME [h cm] HEAT [hit] FOAM [f cm] Splling VOTE [v ct] SOAP [s cp] NOTE [n ct] HOPE [h cp] IFG (BA 44,45) STG (BA 22) Fusiform gyrus (BA 19) TRENDS in Cognitiv Scincs Figur 1. Localization of lft hmisphr rgions activ during rading: th visual word form ara (VWFA) in th fusiform gyrus is involvd in orthographic procssing, th suprior tmporal gyrus (STG) is involvd in phonological procssing (input), th infrior frontal gyrus (IFG) is involvd in phonological procssing (output), and th angular gyrus (AG) is involvd in th mapping btwn phonological and orthographic rprsntation. unxplord. This gap has bn partly filld by Booth and collagus. Thy carrid out a sris of xprimnts to invstigat dvlopmntal diffrncs in th nurocognitiv ntworks for linguistic procssing in adults, and pubscnt childrn with wll-stablishd linguistic comptnc. Thy found substantial ag-rlatd diffrncs in th activation of svral lft hmisphr rgions, among which th angular gyrus (AG), most intrstingly, showd dvlopmntal incrass in functional activation and automaticity. Th sam authors prvious studis had shown that childrn activat phonological information latr and lss automatically than adults during rading [1,2]. In addition, childrn show fwr intraction ffcts btwn orthographic and phonological rprsntations of words [4] (for xampl, whn making dcisions about whthr visually similar or dissimilar pairs of lttrs rhym). Bcaus thy had prviously shown that bttr prformanc on tasks rquiring graphm-to-phonm convrsion was associatd in adults with a gratr activation of th supra-marginal/angular gyrus, th authors assumd that childrn, bing lss skilld than adults, would show lss activation of th sam rgions. Nural circuitry involvd in rhym and splling tasks To shd som light on this mattr, Booth t al. [5] carrid out an fmri study in which 15 adults and 15 childrn (9 12-yar-olds) prformd tasks involving phonological procssing (splling and rhyming judgmnts) and nonlinguistic control tasks in ithr th visual or auditory modality. Tabl 1 shows som xampls of words usd in th various conditions. Th visual orthographic tasks did not rquir accss to phonological information, and th rhyming auditory ons did not rquir orthographic information (hnc ths ar intramodal tasks). Convrsly, th visual orthographic rhyming tasks rquird accss to phonological information and th auditory splling tasks rquird orthographic information ( crossmodal tasks). Th authors hypothsizd that thr would b substantial diffrncs btwn adults and childrn, in particular in th crossmodal tasks, which rquir activation of a mchanism providing a strict mapping btwn phonological and orthographic information. Ovrall, th adults showd gratr activation of th lft infrior frontal gyrus (IFG) than did th childrn in all linguistic tasks. This is consistnt with th litratur showing ag-rlatd incrass in th activation of this ara during various tasks of noun or vrb gnration, fluncy and rading (.g. [6]). Nuroimaging studis suggst that th lft IFG has a rol in procssing word phonology in tasks involving rhym judgmnts [7] or word vs. psudo-word rading [8]. Th right IFG was also mor activatd in adults than in childrn during th visual and auditory splling tasks (consistnt with Booth t al. [9]), and th visual rhyming task. Morovr, both adults and childrn showd gratr activation of th lft than th right fusiform gyrus during th visual tasks, thus supporting th viw that this ara might corrspond to th visual word form ara (VWFA) [10], and of th lft than th right suprior tmporal gyrus (STG) during th auditory tasks, compatibl with th ida that this ara is crucial in phonological procssing [11,12]. Th angular gyrus mdiats accss to htromodal linguistic information Intrstingly, both childrn and adults showd activation of th lft STG during th visual rhyming task that rquird accss to phonological information, and activation of th VWFA during th auditory splling task that rquird accss to orthographic information. Scalp lctrophysiological rcordings rval a slctiv rspons of th VWFA to phonmic incongruity at about 185 ms poststimulus [13]. This finding provids th possibl timing for th activation of VWFA in th auditory splling task. Morovr, Booth t al. [5] showd a manifst gratr activation of th lft AG in adults than in childrn in crossmodal tasks (auditory splling and visual rhyming), indicating that th lft AG is involvd in ths procsss (s Figur 2). Bfor concluding this sction it must b notd that although som authors hav obsrvd incrasd activation of th AG during combind procssing of visual and phonological word-form information [5,9,14], othr groups hav faild to provid supporting vidnc for this hypothsis (.g. [8,15]).
4 166 Updat TRENDS in Cognitiv Scincs Vol.9 No.4 April 2005 (a) (b) Z scor Voxls x,y,z 8:24 8:09 7:55 7:40 7:26 7:12 6:57 6:43 6:28 6:14 6: Visual Auditory Splling BA 39/7 BA 39/37 BA 39 BA 39/7 Visual Auditory Rhyming TRENDS in Cognitiv Scincs Figur 2. Significant diffrncs in brain activation btwn adults and childrn during th auditory and visual tasks usd by Booth t al. [5], shown as (a) voxls; (b) Z scors; avragd adult minus child scors in th activation of th AG and nighboring aras (i.. suprior parital lobul and middl tmporal gyrus). Th tasks involvd th squntial prsntation of thr stimuli and subjcts wr rquird to dtrmin whthr th third stimulus matchd on of th prvious ons on th basis of ithr splling (visual) or rhym (auditory). Crbral maturation lads to th automatization of rading routins Undoubtdly th most important rsult found by Booth t al. [5] is that in adults th lft AG was mor activatd in crossmodal than in intramodal tasks, thus suggsting that this ara is involvd in phonm graphm mapping. Furthrmor, in intramodal tasks not rquiring accss to htromodal information (.g. in th visual splling task, s Figur 2, first column) th AG was significantly mor activatd in adults than in childrn. Altogthr, ths data indicat that skilld radrs hav automatic accss to phonological information during rading [1,2]. Th vidnc providd by Booth t al. [5] that th phonm graphm mapping systm is activatd in adults indpndntly of snsory modality and task rquirmnts also indicats a prvalnc of automatic vrsus controlld procsss in adults compard with young radrs. This may corrlat with maturational diffrncs in synaptognsis, glucos mtabolism, mylination and cortical whit mattr incrass occurring btwn pubrty and adulthood (10 20 yars), spcially in prfrontal aras. Booth t al. [16] hav suggstd a strict corrlation btwn th dvlopmnt and spcialization of nural systms dvotd to rading aftr pubrty, which would lad to an improvmnt in th transmission of nural signals and in th intrconnction of brain rgions involvd in rading. According to this hypothsis, brain maturation, along with practic and xposur to appropriat inputs, would lad to spcialization of a ntwork of lft brain rgions involvd in rading. Within this ntwork, th angular or supramarginal gyrus might play a crucial rol in th intrconnction btwn htromodal rgions in th matur radr [5]. Dos th dvlopmnt of th visual word form ara nd at pubrty? Th findings of Booth t al. [5] dmonstrat dvlopmntal changs in brain activation aftr pubrty. On of th qustions still lft opn is whthr ths changs homognously concrn all nural structurs or whthr thr ar ag-rlatd functional diffrncs btwn aras. In this rgard, Turkltaub t al. [17] carrid out an fmri study on subjcts agd btwn 6 and 22 yars. Thy found a linarly progrssiv incras in th activation of th lft IFG and middl tmporal cortics, as wll as a disngagmnt of th right infrior tmporal cortx as ag and rading ability incrasd from arly childhood to adulthood. Howvr, thy did not obsrv significant changs in th activity of VWFA across ags. By contrast, othr studis hav suggstd a dramatic dvlopmnt and spcialization of this rgion in th first yars of larning to rad (5 9 yars). Morovr, studis on dyslxic childrn [18,19] dmonstratd that rading skills ar positivly corrlatd with th magnitud of activation in th lft occipito-tmporal rgion. Evidnc for th dvlopmnt of th VWFA aftr pubrty is unclar. For xampl, Booth t al. [16] rportd a gratr activation of lft BA 19 and 37 in adults than in young adolscnts for procssing writtn word forms, but wr unabl to rplicat ths findings in th latr studis. Thrfor, it is still unclar at this point whthr th maturation of VWFA nds with pubrty or undrgos subsqunt functional modifications du to crbral maturation or xprtis. Summary and futur prspctivs An important issu in dvlopmntal cognitiv nuroscinc is whthr th activation of brain systms spcializd in rading changs throughout or aftr th priod of acquisition of this skill. Booth t al. [5] hav dmonstratd that ths changs continu vn aftr pubrty, accompanying th rfinmnts of rading ability throughout adolscnc. In nural trms ths changs ar associatd with a gratr activation of a ntwork of lft hmisphr rgions, including th IFG and STG. Furthr rsarch is ndd to clarify th rol of ag- and skill-rlatd changs in VWFA functionality. For xampl, Shaywitz t al. [18] found that rading skill was associatd with mor activation in th lft fusiform gyrus, but thy did not find an association with ag. Indd, th ral challng is to disntangl skill from ag ffcts. On way this qustion could b addrssd is to masur brain activation of radrs with a diffrnt dgr of ducation (for quivalnt crbral maturation), or of diffrnt ags but a similar dgr of ducation. Anothr aspct that nds furthr invstigation is th prcis rol of th AG in linguistic procssing. Indd, bsids phonmic orthographic mapping, AG sms dply involvd in smantic procssing [15]. Th gnral qustion is whthr th ag-rlatd incras in activation of AG (as wll as of IFG) might b rlatd to significant changs in th concptual systm and lxical knowldg of adults compard with childrn. To tap into diffrnt rprsntational systms across ags on might us multipl tasks with paramtric manipulations (such as th word/psudoword contrast).
5 Updat TRENDS in Cognitiv Scincs Vol.9 No.4 April Acknowldgmnts W wish to thank th Editor, Shbana Rahman, and th anonymous rfrs, for thir vry hlpful and prcptiv suggstions. W ar also vry gratful to Patricia Klaas for hr valuabl commnts on th manuscript. Rfrncs 1 Booth, J.R. t al. (1999) Quick, automatic, and gnral activation of orthographic and phonological rprsntations in young radrs. Dv. Psychol. 35, Booth, J.R. t al. (2000) Th association of rapid tmporal prcption with orthographic and phonologic procssing in rading impaird childrn and adults. Sci. Stud. Rading 4, Shaywitz, B.A. t al. (1998) Functional disruption in th organization of th brain for rading in dyslxia. Proc. Natl. Acad. Sci. U. S. A. 95, Zckr, S.G. (1991) Th orthographic cod: dvlopmntal trnds in rading-disabld and normally-achiving childrn. Ann. Dyslxia 41, Booth, J.R. t al. (2004) Dvlopmnt of brain mchanisms for procssing orthographic and phonologic rprsntations. J. Cogn. Nurosci. 16, Schlaggar, B.L. t al. (2002) Functional nuroanatomical diffrncs btwn adults and school-ag childrn in th procssing of singl words. Scinc 296, Shaywitz, B.A. t al. (1995) Sx diffrncs in th functional organization of th brain for languag. Natur 373, Hagoort, P. t al. (1999) Th nural circuitry involvd in th rading of Grman words and psudowords: a PET study. J. Cogn. Nurosci. 11, Booth, J.R. t al. (2003) Rlation btwn brain activation and lxical prformanc. Hum. Brain Mapp. 19, Cohn, L. and Dhan, S. (2004) Spcialization within th vntral stram: th cas for th visual word form ara. Nuroimag 22, Rumsy, J.M. t al. (1997) Phonological and orthographic componnts of word rcognition. A PET-rCBF study. Brain 120, Poldrack, R.A. t al. (2001) Rlations btwn th nural bass of dynamic auditory procssing and phonological procssing: vidnc from fmri. J. Cogn. Nurosci. 13, Provrbio, A.M. and Zani, A. (2003) Tim cours of brain activation during graphmic/phonologic procssing in rading: an ERP study. Brain Lang. 87, Howard, D. (1992) Th cortical localization of th lxicons: positron mission tomography vidnc. Brain 115, Bindr, J.R. t al. (2003) Nural corrlats of lxical accss during visual word rcognition. J. Cogn. Nurosci. 15, Booth, J.R. t al. (2001) Th dvlopmnt of spcializd brain systms in rading and oral languag. Nuropsychol. Dv. Cogn. C Child Nuropsychol. 7, Turkltaub, P.E. t al. (2003) Dvlopmnt of nural mchanisms for rading. Nat. Nurosci. 6, Shaywitz, B.A. t al. (2002) Disruption of postrior brain systms for rading in childrn with dvlopmntal dyslxia. Biol. Psychiatry 52, Shaywitz, B.A. t al. (2004) Dvlopmnt of lft occipitotmporal systms for skilld rading in childrn aftr a phonologically-basd intrvntion. Biol. Psychiatry 55, /$ - s front mattr Q 2005 Elsvir Ltd. All rights rsrvd. doi: /j.tics
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