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The X-Trials: Neural Correlates of an Inhibitory Control Task in Children and Adults

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The X-Trials: Neural Correlates of an Inhibitory Control Task in Children and Adults The X-Trials: Neural Correlates of an Inhibitory Control Task in Children and Adults The Harvard community has made this article openly available. Please share how this access benefits you. Your story matters Citation Davis, Elysia Poggi, Jacqueline Bruce, Kelly Snyder, and Charles A. Nelson. 2003. “The X-Trials: Neural Correlates of an Inhibitory Control Task in Children and Adults.” Journal of Cognitive Neuroscience 15 (3) (April): 432–443. Published Version doi:10.1162/089892903321593144 Citable link http://nrs.harvard.edu/urn-3:HUL.InstRepos:13497071 Terms of Use This article was downloaded from Harvard University’s DASH repository, and is made available under the terms and conditions applicable to Other Posted Material, as set forth at http:// nrs.harvard.edu/urn-3:HUL.InstRepos:dash.current.terms-of- use#LAA The X-Trials:Neural Correlates of an Inhibitory Control Task in Children and Adults Elysia Poggi Davis,Jacqueline Bruce,Kelly Snyder, andCharles A.Nelson Abstract & Event-related potentials (ERPs)were used to examine between the fMRI and ERPfindings was informallyexamined. developmental differences between adults and 6-year-old Theresults indicate that latency and amplitude ofthe P3 children inthe neural processes involved inan inhibitory differentiated the differenttypes oftrials. However, the control task. Twenty adults and 21 children completed atask pattern ofevent-related neural activity differedfor adults and that required them to selectively respond to target stimuli children.These results, whichsuggest that adults and whileinhibiting responses to equally salient non-target children may be using differentprocesses to performthis stimuli.Because thistask had been previously studied using task, have implications forthe interpretation ofthe previous functional magnetic resonance imaging (fMRI),the relation fMRI findings. & INTRODUCTION monkeyinfants to succeed ontasksrequiring theinhibi- The control of action and thoughtplays an important tionof prepotent responses.Moreover, dysregulation role inthe organization of humanbehavior. Inhibitory inthe development of these frontal regions hasbeen control isthe capacity for active inhibitionor modula- implicatedin a significant numberof childhoodpsychi- tionof aprepotent responseand isviewed as falling atric disorders,such as attention deficit–hyperactivity under thegeneral rubric of executive functions.Studies disorder (ADHD), thatseem to involvea failure of ofinhibitorycontrol have found thatareas of thefrontal the abilityto inhibitresponses (van Leewen et al., cortex playa role ininhibition of aprepotent motor 1998; Gorenstein, Mammato, &Sandy, 1989; Chelune, response(Mishkin, 1964). Poorperformance on tasks Ferguson, Koon, &Dickey,1986). involvinginhibition of amotorresponse has been found The ContinuousPerformance Task(CPT) isone task to be associated withdysfunction in the frontal lobes thathas frequently been used to assessinhibitory con- (van Leewen et al.,1998). Furthermore, animalsand trol.A versionof thistask, designed byCasey et al. humanswith frontal lobe lesionsexhibit deficits inthe (1997), hasbeen used infMRI studiesto assessthe abilityto inhibita motorresponse (Chao &Knight,1995; neural substratesinvolved in the inhibition of amotor Iversen &Mishkin,1970). Additionally,studies using response.The taskrequires theexecution of an antici- positronemission tomography (PET) and functional pated motorresponse or itsactive inhibition.Partici- magnetic resonance imaging (fMRI) have indicated that pantsare primedto respondto target stimuliand are acortical network of frontal areas, includingthe anterior thenrequired to inhibittheir response to equallysalient cingulate cortex (ACC) and theorbital prefrontal cortex non-target stimuli.More specifically,participants are (OFC), subservethe ability to inhibitresponses (Carter asked to pressa buttonas quicklyas possiblein et al.,2000; Casey et al.,1997; Pardo,Pardo, Janer, & responseto thepresentation of every letter, except for Raichle, 1990). theletter ‘‘X,’’ withoutmaking mistakes. In thisversion The abilityto inhibitprepotent responseshas been of the task,there are two blocksof trials.Block 1 found to improvewith age. Ithas been argued that consistsof the first42 trialscontaining 100% target maturation of theprefrontal cortex (PFC) accounts for stimuli(i.e., Block 1 go trials).These trialsprime partic- the developmental improvementsseen ininhibitory ipantsto respond to the target stimuli.Block 2 isthe control (Dempster,1992). Diamond(1989) and Dia- responseinhibition condition. It consists of 42 trials mondand Goldman-Rakic (1989) have found thatfron- containing 50% target stimuli(i.e., Block 2 go trials) tal lobe development isnecessary for bothhuman and and 50% non-target stimuli(no-go trials). In aneuroimaging studyemploying this task, activa- tionof theinferior frontal gyrus,middle frontal gyrus, University ofMinnesota OFC, and ACC was observed for bothadults and 7- to © 2003Massachusetts Institute ofTechnology Journal ofCognitive Neuroscience15:3, pp. 432– 443 12-year-old children inthe response inhibitioncondi- the participant(Tekok-Kili c, Schucard, &Schucard, tion(Casey et al.,1997). Thus,adults and children 2001; Keifer et al.,1998). Ithas been suggested that showedgreater activation of these regions during theamplitude of theP3 isgreater for no-go stimuli Block2, whichcontained 50% target and 50% non- thango stimuliwhen the responsepreparation ishigh target stimuli,as compared toBlock1, whichcontained (Cohen, Porjesz, Begleiter, &Wang, 1997). Thismay be 100% target stimuli.Furthermore, children showed related tothe attention (Overtoom et al.,1998) or greater activation of these regions thanadults did. magnitude of inhibition(Cohen et al.,1997) elicited by Activation of two regions,the ACC and theOFC, was thestimuli. associated withperformance. Greater activationof the Itwas agoal of thisstudy to use ERPsto examine the ACC was associated witha greater numberof false alarms task-relevant neural processes of an inhibitorycontrol (i.e.,pressing the button to anon-target stimulus)where- taskpreviously studied using fMRI and tocompare these as greater activation of theOFC was associated with processes inadults and children.Based on theresults fewer false alarms. from the fMRI study(Casey et al.,1997), itwas predicted fMRI isan extremely useful technique thathas vastly thatgreater activation wouldbe seen for bothadults and improvedour understanding of theneural structures children on trialsthat required response inhibition involvedin cognitive processing,but there are limita- (i.e.,no-go trials).Second, itwas predicted thatchildren tionsinherent to thismeasure. First,largely because of wouldshow greater activation on these trialsthan thetime course of thehemodynamic response, fMRI has adults.Additionally, based on priorERP studies,it was poortemporal resolutionon the order of seconds. predicted thatgreater amplitudeof theN2 and theP3 Event-related potentials(ERPs), on the other hand, wouldbe seen on trialsrequiring inhibitionof amotor provideinformationon the order of milliseconds response(Fallgatter &Strik,1999; vanLeewen et al., regarding themental chronometryof informationpro- 1998; Eimer,1993). cessing (Keifer, Marzinzik, Weisbrod,Scherg, &Spitzer, Whereas itis important to understand neural pro- 1998; vanLeewen et al.,1998). Thus,this method can be cesses involvedin a cognitive task,it is equally impor- used to further our understanding of theneural pro- tant to understandfactorsrel ated to individual cesses involvedin cognitive functioning. In contrast to differences inperformance onsuchtasks. A second goal fMRI, whichtends to be mostsuitable for older children of thisstudy, then, was to investigate factors thatmight whocan remain stillfor long periodsof time,ERPs can predict behavioralperformance on thistask. There are be usedwith children of anyage. Thus,it is an excellent two relevant componentsof behavior,speed and accu- toolby which to study developmental change. Collec- racy. There isevidence from taskssimilar to theone tively,whereas use of fMRI withthe CPT has furthered used inthis study that greater amplitudeof the N2 our understanding of neural structures involvedin the (Falkenstein, Hoormann,& Hohnsbein,1999; Verbaten abilityto inhibit a motorresponse, our understanding of et al.,1994) and P3 (Verbaten et al.,1994) isassociated temporal sequencing inthe processing of thetask is withgreater accuracy. Furthermore, increases inpro- limited.Using fMRI, we are not able to determine cessing speed,as indicated bylatency of theN2, were whether thefrontal structures found to be involvedin alsofound tobe related to increased accuracy (Falken- thisresponse inhibition task are responsiblefor different steinet al.,1999). However, previousresearch has aspects ofthe processing of thistask. Second, because of suggested thatfor tasksthat emphasize speed as well the blockdesign used withthis task in the previous fMRI as accuracy, suchas thetask used in this study, reaction study,it is not possible to differentiate between the timeand latency are notrelated (Donchin,Karis, neural processes involvedin the go trialsof Block2 as Bashiore,Coles, & Gratton, 1986). compared tono-go trialsof Block2. Thus,although it is Insum,there were several goals of thecurrent study. clear thatgreater inhibitionis required inBlock 2 thanin The primarygoal of thisstudy was to use ERPsto examine Block1, itis likely that different processes wouldbe theneural processes of an inhibitorycontrol taskpre- used to regulate the response
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