Supplemental Information

22 Pages·2014·1.98 MB·English

Effects of the FITKids Randomized Controlled Trial on Executive Control and
Brain Function
Charles H. Hillman, Matthew B. Pontifex, Darla M. Castelli, Naiman A. Khan,
Lauren B. Raine, Mark R. Scudder, Eric S. Drollette, Robert D. Moore, Chien-Ting
Wu and Keita Kamijo
Pediatrics; originally published online September 29, 2014;
DOI: 10.1542/peds.2013-3219

The online version of this article, along with updated information and services, is
located on the World Wide Web at:
http://pediatrics.aappublications.org/content/early/2014/09/24/peds.2013-3219

PEDIATRICS is the official journal of the American Academy of Pediatrics. A monthly
publication, it has been published continuously since 1948. PEDIATRICS is owned,
published, and trademarked by the American Academy of Pediatrics, 141 Northwest Point
Boulevard, Elk Grove Village, Illinois, 60007. Copyright © 2014 by the American Academy
of Pediatrics. All rights reserved. Print ISSN: 0031-4005. Online ISSN: 1098-4275.
DDoowwnnllooaaddeedd ffrroomm ppeeddiiaattrriiccss..aaaappppuubblliiccaattiioonnss..oorrgg aatt MMiicchhiiggaann SSttaattee UUnniivv oonn OOccttoobbeerr 1133,, 22001144
ARTICLE
Effects of the FITKids Randomized Controlled Trial on
Executive Control and Brain Function
AUTHORS: CharlesH.Hillman, PhD,aMatthewB.Pontifex, WHAT’S KNOWN ON THIS SUBJECT: Physical activity programs
PhD,bDarlaM.Castelli, PhD,cNaimanA.Khan,PhD,RD,a have been shown to have positive implications for children’s
LaurenB.Raine,BS,aMarkR.Scudder,BS,aEricS. cognitiveperformanceandbrainstructureandfunction.However,
Drollette,BS,aRobertD.Moore,MS,aChien-TingWu,PhD,d additional randomized controlled trials are needed to determine
andKeitaKamijo,PhDe whetherdailyphysicalactivityinfluencesexecutivecontrolandits
aDepartmentofKinesiologyandCommunityHealth,University neural underpinnings.
ofIllinoisatUrbana-Champaign,Urbana-Champaign,Illinois;
bDepartmentofKinesiology,MichiganStateUniversity,East
WHAT THIS STUDYADDS: The randomized controlled trial,
Lansing,Michigan;cDepartmentofKinesiologyandHealth
designed to meet daily physical activity recommendations, used
Education,UniversityofTexasatAustin,Austin,Texas;
dDepartmentofExerciseScience,SchreinerCollege,Kerrville, behavioralandelectrophysiologicalmeasuresofbrainfunctionto
Texas;andeSchoolofSportSciences,WasedaUniversity, demonstrate enhanced attentional inhibition and cognitive
Tokorozawa,Saitama,Japan flexibility among prepubertal children.
KEYWORDS
cognition,physicalactivity,aerobicfitness,randomizedcontrolled
trial
ABBREVIATIONS
abstract
ANOVA—analysisofvariance
CI—confidenceinterval
ERP—event-relatedbrainpotential OBJECTIVE:Toassesstheeffectofaphysicalactivity(PA)intervention
FITKids—FitnessImprovesThinkinginKids
onbrainandbehavioral indicesofexecutivecontrolinpreadolescent
HR—heartrate
MVPA—moderatetovigorousphysicalactivity children.
SES—socioeconomicstatus METHODS:Twohundredtwenty-onechildren(7–9years)wererandomly
RT—reactiontime
VO2peak—maximaloxygenconsumption assigned to a 9-month afterschool PA program or a wait-list control. In
addition to changes in fitness (maximal oxygen consumption), electrical
DrHillmanconceptualizedanddesignedthestudy,draftedthe
initialmanuscript,andcriticallyreviewedthemanuscript; activityinthebrain(P3-ERP)andbehavioralmeasures(accuracy,reaction
DrPontifexcoordinatedandsuperviseddatacollectionand time)ofexecutivecontrolwerecollectedbyusingtasksthatmodulated
reduction.Heassistedinrevisingtheinitialmanuscriptand
attentional inhibition and cognitive flexibility.
criticallyreviewedthemanuscript;DrCastelliconceptualized
anddesignedthephysicalactivityintervention,assistedin RESULTS:Fitnessimprovedmoreamonginterventionparticipantsfrom
revisingtheinitialmanuscript,andcriticallyreviewedthe
pretest to posttest compared with the wait-list control (1.3 mL/kg per
manuscript;DrKhan,MsRaine,MrScudder,MrDrollette,
MrMoore,DrWu,andDrKamijocoordinatedandsupervised minute, 95% confidence interval [CI]: 0.3 to 2.4; d = 0.34 for group
datacollectionandreduction.Theyalsoassistedinrevisingthe difference in pre-to-post change score). Intervention participants
initialmanuscriptandcriticallyreviewedthemanuscript;and
exhibitedgreaterimprovementsfrompretesttoposttestininhibition
allauthorsapprovedthefinalmanuscriptassubmitted.
(3.2%, 95% CI: 0.0 to 6.5; d = 0.27) and cognitive flexibility (4.8%, 95%
Thistrialhasbeenregisteredatwww.clinicaltrials.gov
CI:1.1to8.4;d=0.35forgroupdifferenceinpre-to-postchangescore)
(identifierNCT01334359).
compared with control. Only the intervention group increased atten-
www.pediatrics.org/cgi/doi/10.1542/peds.2013-3219
tional resources from pretest to posttest during tasks requiring in-
doi:10.1542/peds.2013-3219
creased inhibition (1.4 mV, 95% CI: 0.3 to 2.6; d = 0.34) and cognitive
AcceptedforpublicationJul25,2014
flexibility (1.5mV, 95% CI: 0.6to2.5;d = 0.43). Finally, improvementsin
AddresscorrespondencetoCharlesH.Hillman,PhD,Department
brainfunctionontheinhibitiontask(r=0.22)andperformanceonthe
ofKinesiologyandCommunityHealth,UniversityofIllinoisat
Urbana-Champaign,317LouiseFreerHall,906SouthGoodwin flexibility task correlated with intervention attendance (r = 0.24).
Ave,Urbana,IL61801.E-mail:[email protected]
CONCLUSIONS:Theinterventionenhancedcognitiveperformanceand
PEDIATRICS(ISSNNumbers:Print,0031-4005;Online,1098-4275). brainfunctionduringtasksrequiringgreaterexecutivecontrol.These
Copyright©2014bytheAmericanAcademyofPediatrics findingsdemonstrateacausaleffectofaPAprogramonexecutivecon-
(Continuedonlastpage) trol,andprovidesupportforPAforimprovingchildhoodcognitionand
brain health. Pediatrics 2014;134:e1063–e1071
PEDIATRICSVolume134,Number4,October2014 e1063
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The pandemic of physical inactivity is beassessedrelativetoitssize(measured notinvolvedinthedatacollection.The
aseriousthreattoglobalpublichealth1 inamplitude)anditstiming(measuredin randomization procedure was per-
accounting for ∼10% of all premature latency). That is, larger P3 amplitude formed only afterall participants had
deaths from noncommunicable dis- reflects greaterallocation of attentional been recruited and group allocation
eases.2 Despite evidence that such in- resources,10 and faster P3 latency re- wasconcealedfromtheresearch/data
activitydetrimentallyaffectsbrainhealth flectsfastercognitiveprocessingspeed.11 collectionteam.Duetotheinclusionof
and aspects of cognition known as ex- Our laboratory has previously demon- siblings among 10 families, noninde-
ecutivecontrol(alsocalledcognitive strated fitness-related differences in pendentobservationswereincluded.As
control)inolderadultpopulations,3,4this P3 such that higher-fit children exhib- such, analyses were rerun by using a
area remains understudied in children. ited larger P3 amplitude and shorter randomly selected sibling from each
Thisisconcerningbecausechildhoodis P3 latency, indicating greater atten- family.Thefindingsremainedunchanged
characterized by extensive changes in tional resource allocation and faster fromthoseincludedintheresultssection.
brain structure, function, and connec- cognitive processing speed, respec- After baseline testing, pairs of partic-
tivity.5 Thus, an active lifestyle during tively.7,8Therefore,differencesinfitness ipants were matched for age, gender,
childhoodmayhaveprotectiveeffectson account fora portion of the variability race, socioeconomic status (SES), and
brainhealthacrossthelifespan,asisthe observed in executive control and un- VO2max, and a coin was flipped by the
derlyingbrainfunctioninpreadolescent independentresearchertodetermine
case for physical health. However, the
specific effects of physical activity (PA) children. groupassignment.Allparticipantscom-
pleted a 2-day protocol of testing at
on key cognitive processes and their Despiteavailablecorrelationalevidence,
neuralunderpinningsremainunknown. few have manipulated PA or aerobic baseline (pretest) and postintervention
fitness among children to investigate (posttest).Thestudywasconductedover
Executive control, which consists of in-
theireffectsonexecutivecontrolandits the fall and spring semesters of the
hibition(resistingdistractionsorhabits
neuralunderpinnings.12–15Inaddition,it schoolyearsbetween2009and2013.The
to maintain focus), working memory
institutionalreviewboardattheUniver-
remainsunknownwhetherattendance
(mentally holding and manipulating
sity of Illinois approved the study pro-
information), and cognitive flexibility in a PA program correlates with mea-
tocol.Parentsprovidedwritteninformed
suresofexecutivecontrol.Consequently,
(multitasking),isvitaltosuccessinschool,
consent,andparticipantsprovidedwrit-
weinvestigatedtheeffectsofa9-month
vocation,andlife.6Cross-sectionalstud-
tenassent.
randomized controlled PA trial (Fitness
ies7,8 have demonstrated that aerobic
Improves Thinking in Kids [FITKids]) on
fitnessispositivelyrelatedtoexecutive
brain and behavior during tasks re- Participants
control,withmorefitchildrenexhibiting
quiringattentionalinhibitionandcogni-
superiorattention,decision-makingabil- Eligible participants were 8- to 9-year-
tive flexibility. We hypothesized that,
ity, and differential brain function com- olds residing in East Central Illinois.
relativetothewait-listcontrolgroup,the
pared with their lesser-fit peers. In This age range was chosen based on
FITKids intervention would result in (1) preliminary research investigating fit-
particular,event-relatedbrainpotentials
improvements in behavioral perfor-
nessandpreadolescentcognition,which
(ERPs), derived from an EEG, allow for
mance,(2)increasedattentionallocation
found reliable differences in neuro-
the real-time measurement of changes
(measured via P3 amplitude), and (3)
imaging, behavioral, and academic
in electrical activity in brain function
fastercognitiveprocessingspeed(mea-
achievementtestperformanceoccurat,
whilechildrenperformedcognitivetasks.
sured via P3 latency). Finally, we pre-
orbefore,thisagerange.Fourhundred
The most common way that brain ac-
dicted a positive correlation between seventy-fivechildrenwerescreened,and
tivity is captured in an ERP is through
participation in the intervention and
221childrenwererandomlyassignedto
themeasurementofthevariouspeaks
improvementsinthecognitiveoutcomes.
eitherstudygroup(Fig1).Theexclusion
of the waveform. A peak commonly
criteria included special educational
usedtoassessbrainactivityistheP3,
METHODS services related to cognitive or atten-
whichhasbeenrobustindemonstrat-
ing differences between individuals of Study Design tional disorders, neurologic diseases,
andphysicaldisabilities.
higherand lower fitness during tasks Participants were randomly assigned
that tap executive control. The P3 re- to either the FITKids afterschool PA
flects neuronal activity thought to be program(interventiongroup)orawait- Study Procedures
associated with the processes of at- list control group. Randomization was Outcome assessors were blinded to
tentionandworkingmemory,9andcan performedbyastaffmemberwhowas groupassignmentthroughoutalltesting.
e1064 HILLMANetal
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ARTICLE
Attentionalinhibitionwasassessedby
using a modified flanker task,22,23 and
cognitive flexibility was assessed by
using a color-shape switch task.24 A
modified flanker task is a method to
measure inhibition in which children
areengagedinaseriesoftrialsthat,in
thiscase,havearraysoffishthateither
match(ie,congruentarrays)ordonot
match(ie,incongruentarrays).Thetask
istopresseithertherightorleftbutton
as quickly and accurately as possible
based on the direction in which the
middle fish is facing. Task difficulty is
manipulated by whether the flanking
fish face the same direction or the op-
posite direction to the middle fish. The
color-shapeswitchtaskisameasureof
cognitiveflexibility,inwhichchildrenare
shown characters of different shapes
FIGURE1 (ie, square, circle) and color (ie, blue,
FlowdiagramoftheFITKidsintervention. green),andareaskedtomakeasingle
judgment(ie,homogeneoustaskcondi-
On the first visit, demographic infor- NC). Participants were then randomly tion) via a button press about either
mation, including age, gender, race/ assigned to the FITKids intervention or shape or color. Next, they are asked to
ethnicgroup,andSESwerecollected.16 the wait-list as described earlier. After flexibly switch their decisions around
SES was determined by using a tri- completion of the intervention, partic- both shape and color creating a more
chotomousindexbasedonthefollowing: ipants returned to the laboratory for difficult decision process (ie, heteroge-
(1)participationinfreeorreduced-price their posttest assessments, which was neous task condition). The task con-
mealprogramatschool,(2)thehighest identicaltothebaselineassessment. ditionsthatrequirethegreatestamount
level of education obtained by the ofexecutivecontrolaretheincongruent
mother and father, and (3) number of Aerobic Fitness Assessment condition in the flanker task and the
parentswho worked full-time.16 Partic- heterogeneous condition in the switch
Aerobicfitnesswasassessedbyusing
ipantscompletedtheKaufmanBriefIn- task(seeSupplementalInformation).In
a test of maximal oxygen consumption
telligence Test17 to assess IQ, a Tanner addition to behavioral measures, EEG
StagingSystemquestionnairetoassess (VO2peak;seeSupplementalInformation). activitywascollectedduringthecognitive
This test employed a computerized in-
pubertalstatus,18andthePAReadiness tasksfrom64electrodesitestoderivethe
directcalorimetrysystemwhilepartic-
Questionnaire19 to screen for health is- P3amplitudeandlatencymeasures(see
ipants ran/walked on a motor-driven
sues exacerbated by physical exercise. SupplementalInformation).
treadmill at a constant speed with in-
ParticipantswerethenfittedwithaPo-
cremental grade increases every 2 PA Intervention
lar heart rate (HR) monitor (Model A1,
minutes until volitional exhaustion.20
PolarElectro,Finland),hadtheirheight The2-hourPAinterventionoccurredat
Aerobic fitness percentiles were de-
andweightmeasuredbyusingaTanita arecreationalfacilityontheUniversity
terminedbyusingnormativevaluesfor
WB-300Plusdigitalscaleandstadiometer ofIllinoiscampusaftereachschoolday,
(Tanita Corp, Tokyo, Japan), and com- VO2peak.21 andfocusedonimprovementofaerobic
pleted a maximal exercise test to as- fitnessthroughengagementinavariety
sess aerobic fitness. On the second Cognitive Tasks of age-appropriate physical activities.
visit,participantsperformedcognitive Response accuracy and reaction time Children intermittently participated in
tasks assessing attentional inhibition (RT) were collected to assess behav- at least 70-minutes of moderate-to-
and cognitive flexibility while fitted with ioral performance on the attentional vigorous PA (recorded by E600 Polar
anEEGcap(Compumedics,Inc,Charlotte, inhibitionandcognitiveflexibilitytasks. HRmonitors;PolarElectro).Specifically,
PEDIATRICSVolume134,Number4,October2014 e1065
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the intervention included ∼30 to 40 (congruency: congruent, incongruent) significantdifferencesbetweeninterven-
minutesatPAstations.Next,ahealthy for the flanker task and within 2 con- tionandwait-listcontrolgroupsrelative
snackandeducationalcomponentwere ditions (switch: homogeneous, hetero- to age (20.08 years, P = .32), pubertal
providedasarestperiod,andchildren geneous) for the switch task. The P3 timing (20.05, P = .48), aerobic fitness
then engaged in low organizational ERP component was assessed sepa- (21.73 mL/kg per minute, P = .07), BMI
games (45–55 minutes) centered on a ratelyforamplitudeandlatencywithin (0.2,P=.73),orIQ(22.5,P=.17).
skill theme (see Supplemental Infor- thesame2conditionsforeachtask.To
mation). The activities were aerobically accountformissingdata,multipleim- Intervention Participation
demanding,butsimultaneouslyprovided putationwasperformedbyusingPASW
Participants in the FITKids afterschool
opportunitiestorefinemotorskills.The Statistics,19.0toimpute20valuesfor
programattended80.6%(615.1)ofthe
program was offered 150 days of the each missing observation. Analyses
sessions.MeanHRduringthesesessions
170-dayschoolyear. wereperformedbyusingthecombined
was∼137beatsperminute(68.3)with
multivariable modeling estimates. All
Statistical Analysis childrentaking∼4246steps(61039.9;
statistical analyses were conducted
seeSupplementalInformation).
Assumingasmalleffectsize(d=0.3), witha=0.05byusingtheGreenhouse-
reliabilityofthewithin-subjectsfactor Geisser statistic with subsidiary uni-
(r = 0.8), 2-sided a of 0.05, and 80% variate ANOVAs and Tukey’s honest Changes in Aerobic Fitness and
Weight Status
power, the required sample size was significantdifferencetestsforposthoc
90 to 100 participants per group. The comparisons.Findingsreportedherein Although both groups increased in
primary outcomes assessed were be- are restricted to only those related to aerobicfitness,theinterventiongroup
havioral and brain function indices of the intervention. Fora more complete demonstrated a greater improvement
performanceinresponsetotheflanker statisticalsummary,pleaserefertothe frompretesttoposttestthanthewait-
and switch tasks. Analyses were con- SupplementalInformation. list control group (1.5 mL/kg per min-
ductedbyusinga2(group:intervention, ute,95%confidenceinterval[CI]:0.5to
wait-list) 3 2 (time: pretest, posttest) 2.5,d=0.39forgroupdifferenceinpre-
RESULTS
multivariate repeated measures analy- to-post change score). Furthermore,
sis of variance (ANOVA)withadditional Participants pre-toposttestchangeinaerobicfit-
variables nested within the primary Demographic data are provided in ness percentile was significant only
analyticalprocedure based onthe out- Table1.Overhalfoftheparticipantsin amonginterventionparticipants(5.5per-
come variable. Analysis of behavioral bothgroupswerewhite,andover40% centile,95%CI:1.9to9.1,d=0.42forinter-
measures(responseaccuracy,RT)was of the participants were categorized ventiongrouppre-to-postchangescore)
conductedseparatelywithin2conditions as low SES. At baseline, there were no and not among wait-list participants
TABLE1 Mean(95%CI)ValuesforParticipantDemographicData
Measure Intervention Wait-list
Pretest Posttest Change Pretest Posttest Change
N 109 — — 112 — —
Gender(%girls) 53(49)a — — 49(44)a — —
Race,n(%)
Asian 17(15)a — — 12(11)a — —
AfricanAmerican 25(23)a — — 28(25)a — —
White 51(47)a — — 59(53)a — —
Otherormixed-race 16(15)a — — 13(11)a — —
Hispanic 10(9.2)a — — 5(4.5)a — —
LowSES 43(39.5)a — — 49(43.8)a — —
Age,y 8.8a(8.7to8.9) 9.5b(9.4to9.6) 0.7a(0.6to0.7) 8.8a(8.7to8.9) 9.5b(9.4to9.7) 0.7a(0.7to0.8)
Pubertaltiming 1.4a(1.3to1.5) 1.5b(1.4to1.6) 0.1a(0.0to0.2) 1.5a(1.4to1.6) 1.6b(1.5to1.7) 0.1a(0.0to0.2)
IQ(K-BITcomposite) 109.8a(107.2to112.4) 111.8b(109.2to114.3) 2.0a(0.3to3.6) 112.6a(109.9to115.4) 116.5b(113.7to119.3) 3.9a(2.0to5.8)
Attention-deficit/hyperactivity 42.8a(37.0to48.5) 42.3a(36.6to47.9) 20.5a(25.8to4.8) 44.3a(38.7to49.8) 46.2a(40.4to51.9) 1.9a(22.7to6.5)
disorder-IVcomposite
BMI 19.1a(18.3to19.9) 19.3a,b(18.4to20.2) 0.2a(0.0to0.5) 18.9a(18.1to19.7) 19.8b(18.9to20.7) 0.9b(0.6to1.2)
VO2peak(mL/kg/min) 37.5a(36.2to38.8) 39.5b(38.2to40.8) 2.1a(1.2to2.9) 39.2a(37.9to40.5) 39.9b(38.6to41.3) 0.7b(0.1to1.4)
VO2peakpercentile 17.5a(13.8to21.3) 23.2b(18.5to27.8) 5.6a(2.0to9.3) 21.9a,c(17.7to26.2) 22.8b,c(18.5to27.0) 0.8b(21.8to3.4)
K-BIT,KaufmanBriefIntelligenceTest.Dataarepresentedasmean(95%CI)unlessnotedotherwise.Valuessharingacommonsuperscriptarenotstatisticallydifferentata=0.05.
e1066 HILLMANetal
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ARTICLE
(0.5percentile,95%CI:22.0to3.0,d=0.06 8)0)3) 3)
for wait-list group pre-to-post change 223.222.223. 224.8.1)
sBcMoIr;eh)o.wBoevtherg,rthoeupwsaaitl-sliostingcrroeuapseddemin- Change 1.0to5.5)2.0to6.7)1.6to5.9) 264.5to266.1to265.0to 1.1to3.7)3.3to8.6) 290.2to298.9to1
onstrated a greater increase than the ((( ((( (( ((
b2a3b8 a2a1a2 a4b0 a2a4
intervention group (0.5 kg/m2, 95% CI: 3.4.3. 44.44.44. 2.6. 57.40.
222 22
0.2to0.9,d=0.37forgroupdifference
inpre-to-postchangescore).
0)
CPrhea-nagnedspionstAtetstetnpteirofnoraml aInnhceibiistiosnum- Wait-list Posttest 83.5to87.6)77.5to82.2)80.6to84.8) 459.5to496.7)489.0to527.5)473.7to511.2) 89.1to91.3)72.6to77.4) 730.6to788.5)1389.2to1481.
marized in Table 2. Although response ((( ((( (( ((
b6b9b7 b1b2b5 b2b0 b5a1
accuracy increased in both groups, the 85.79.82. 78.08.92. 90.75. 59.35.
454 74
1
interventiongroupdemonstratedgreater
improvement from pretest to posttest
1)
t9fFhei5gra%en2n)Cc.tIhe:He0o.i0wnwetaopvietr6-rle.i,5s-tt,tohd-ecpro=oens0twtr.2oa7clshfgonarrnoogguinerpflousu(cp3eo.n2drc%iefe-;, Pretest 80.2to84.5)73.5to77.6)77.0to81.0) 501.8to542.7)529.9to574.7)515.5to557.8) 86.4to89.1)66.6to71.4) 786.0to847.6)1426.8to1524.
((( ((( (( ((
ofgroupassignmentonRT(P$.18). c2.3c5.5c9.0 a2.2a2.3a6.7 a7.8a9.0 a6.8a5.4
877 253 86 17
555 84
Only the intervention group demon- 1
strated increased P3 amplitude from
isp(n1crt.oe4ertreemvs;eVtnF,ttio9igo5pn%3o;sgCtartIelo:ssu0otp.3oSnptuoripnep2c-t.lo6oen,m-pgdoersnu=ttean0cl.th3Ft4aringiafgol9esr Change 4.7to9.6)4.2to9.5)4.6to9.4) 2254.6to19.3)2249.7to9.2)2251.9to14.7) 0.7to3.8)8.2to13.3) 2270.1to4.7)239.2to82.7)
((( ((( (( ((
in the Supplemental Information), and a1a8a0 a9a5a3 a2a7 a4a7
7.6.7. 6.9.3. 2.0. 7.1.
323 1 32
a greater change in P3 amplitude on 222 2
incongruenttrialsfrompretesttopost-
test relative to the wait-list group 9)
(gss1tcrr.oo9aurtempe)dV.d,fTia9fhfs5eet%reeirnnCPtceI3:erl0vai.en3tnenttpiocoryen3-f.to5go,rr-pdoinouc=spotn0dcg.eh3rm1auneofgonnert- ntervention Posttest (84.0to87.5)(76.9to81.0)(80.6to84.2) (450.9to483.3)(484.8to519.5)(467.2to500.4) (88.7to91.0)(74.3to78.9) (721.2to788.7)(1362.4to1451.
trialsatposttestrelativetopretest(20.1 I b85.8b78.9b82.4 b467.1b502.2b483.8 b89.9b76.6 b754.9a407.1 0.05.
1 =
milliseconds,95%CI:2.6to37.6,d=0.31 a
dfstt9oehc5irfneo%fceirnywreCte)feaIrn,r:iocvat6-meenl.in9sdiptntitroaopegnrgtr5egeor7sr-uet.ot2aoput,-topped(opr3pso=2rcts.eh0tc0-atth.oe3mna-s4pgnitloelgrfsioeseitrnleacscghtcPoiraov3noenrduelgtas)poe-,. orTaskPerformance Pretest a(76.3to80.9)8.6a(69.8to74.5)2.1a5.4(73.2to77.6) a4.0(481.8to526.3)a(507.4to555.9)1.6a7.2(494.2to540.1) a7.7(86.3to89.0)a5.9(63.2to68.6) a(760.5to824.2)2.3a5.4(1328.7to1442.1) enotstatisticallydifferentat
Changes in Cognitive Flexibility Valuesf 777 505351 86 79138 erscriptar
Atnihimnoloetttuphepesrroroovuosevgagtnethneemtdnibsoeetonnohtphputeeastgirerntrfartooioscprugkimeppewrsaanfanoneinsrtocscmgeurr(sea4eoan.an8tsctr%eeeihdar,o9loaismn5nm,%opottgrnhhCeegeeI--: TABLE2Mean(95%CI) Measure FlankertaskResponseaccuracy(%)CongruenttrialsIncongruenttrialsAlltrialsRT(ms)CongruenttrialsIncongruenttrialsAlltrialsSwitchtaskResponseaccuracy(%)HomogeneoustrialsHeterogeneoustrialsRT(ms)HomogeneoustrialsHeterogeneoustrials Valuessharingacommonsup
PEDIATRICSVolume134,Number4,October2014 e1067
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of inhibitory control. No such relation-
shipwasobservedforcongruentflanker
task trials requiring lesser amounts of
inhibitorycontrol.Asimilarrelationship
was observed for behavioral indices of
the task-switching task, such that at-
tendancewaspositivelycorrelatedwith
change in task performance on the
moredemandingheterogeneouscondi-
tion necessitating increased inhibition,
FIGURE2 working memory, and cognitive flexibil-
Changeinresponseaccuracy(mean6SE)frompre-toposttestasafunctionofgroupandcognitive
task. ity(r=0.24,P=.01),withnosucheffect
realizedforthehomogeneouscondition
requiring lesser amounts of executive
control(Fig4).
DISCUSSION
Theprovisionofa9-monthrandomized
controlled PA intervention, directed
toward increasing aerobic fitness, sig-
nificantly improved brain and behav-
ioralindicesofexecutivecontrol.More
importantly, these effects were selec-
tivetoaspectsofcognitionthatrequired
extensive inhibition and cognitive flexi-
bility,withnochangesobservedfortask
components requiring lower-order (ie,
nonexecutive) aspects of cognition. Fur-
ther,thefitness-relatedbenefitsappear
to follow a dose–response relationship,
ashigherattendancerateintheFITKids
program was associated with larger
FIGURE3
TopographicscalpdistributionofthechangeinP3amplitude(spectrumscale:bluetored)duringthe changesinneuralindicesofattention(ie,
flankertask(top)andswitchtask(bottom)isillustratedfortheinterventiongroup(left)andwait-list P3 amplitude), processing speed (P3 la-
group(right).Asshown,P3amplitudewasgreaterintheinterventiongroupatposttestonlyforthe
tency), and improved performance dur-
conditionsthatrequiredthegreatestamountofexecutivecontrolacrossbothtasksasdenotedbythe
greateramountofreddepictedintheelectrophysiologicalplotsrepresentingbrainfunction. ingtheexecutivecontroltasks.Giventhat
nosignificantdifferenceswereobserved
1.1to8.4,d=0.35forgroupdifference Information). No influence of group for children assigned to the wait-list
in pre-to-post change score; Fig 2). An assignment was observed for homo- control, the key implication from this
increase in P3 amplitude to the het- geneoustrialsorP3latency(P$.06). study is that participating in a daily,
erogeneous trials from pretest to afterschool PA program enhances ex-
Attendance and Cognitive Task ecutivecontrol.
posttestwas observedonlyfor the in-
terventiongroup(1.5mV,95%CI:0.6to Performance Previous randomized controlled trials
2.5,d=0.43forinterventiongrouppre- Attendance in the FITKids intervention in this area have varied in outcomes
to-post change score), with a greater was positively correlated with change studied,methodologies,andparticipant
changeinP3amplituderelativetothe inP3amplitude(r=0.22,P=.02)and characteristics.12–15 Among overweight
wait-list group (1.4 mV, 95% CI: 0.0 to negativelycorrelatedwithchangeinP3 children, Davis et al12 demonstrated
2.7,d=0.27forgroupdifferenceinpre- latency(r=20.22,P=.02)frompre-to dose–response benefits of exercise on
to-post change score; Fig 3; also Sup- posttest, only for incongruent flanker executivefunctionandmathachievement.
plemental Fig 10 in the Supplemental task trials requiring greater amounts Further,functionalMRIresultsrevealed
e1068 HILLMANetal
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ARTICLE
attendanceinan8-monthexercisepro-
gram was positively associated with
improvedwhitematterintegrityamong
a group of sedentary and overweight
(BMI $ 85th percentile) 8- to 11-year-
olds (94% African American). However,
the findings from the current study
provide further support for the impor-
tance of PA program attendance for
cognitivebenefitamongalargehetero-
geneoussampleofchildrenwithvarying
weightstatus.Giventhathealthfactors
(physical inactivity, excess adiposity)
havebeenrelatedtoabsenteeism,26the
findings herein indicate that increased
timespentengaginginPAimprovesboth
physical and brain health, which has
broad public healthimplications foref-
fectivefunctioningacrossthelifespan.
Although children in the FITKids inter-
ventionexhibitedgreaterimprovements
inexecutivecontrolrelativetotheirwait-
FIGURE4 listcontrolcounterparts,therearesome
ScatterplotsoftherelationshipbetweenattendanceattheFITKidsafterschoolPAprogramandpre-to
limitationsofthecurrentstudy.Theuse
posttestchangeinP3amplitudetotheincongruentconditionoftheflankertask(A),changeinP3latency
totheincongruentconditionoftheflankertask(B),changeinresponseaccuracyforthehomogenous of a wait-list control renders it difficult
conditionoftheswitchtask(C),andchangeinresponseaccuracyfortheheterogeneousconditionofthe to attribute the observed group differ-
switchtask(D).
ences entirely to the PA participation
because other aspects of the program
increased prefrontal and reduced pos- associated with improvements in the
such as the educational component,
teriorparietalcortexactivityduringan executive control of working memory
social interaction with peers and inter-
antisaccade task. In a similar sample, after a 9-month PA intervention. The
vention staff, and refining motor skills
Krafft et al15 found that an exercise results from the current study are
may have contributed to the results.
intervention increased activationin re- broadlyconsistentwiththeaforemen-
However, it is unlikely that the educa-
gions involved in flanker accuracy in- tioned studies revealing that daily PA
tionalcomponentwasthecauseofgroup
cluding the anterior cingulate cortex not only improves aerobic fitness but
differences, given that it was brief and
and the superior frontal gyrus. Among also enhances brain function and be-
tookplaceaspartoftheinstructionfor
a sample that varied in weight status, havioral sequelae during tasks that
the PA intervention (see Supplemental
Chaddock-Heymanetal14observedthat requireextensiveamountsofexecutive
Information). Another limitation of the
children receiving a PA intervention controlamongprepubertalchildren.In
study was that nonintervention PA was
improved performance on a flanker addition, the current study extends
notmeasured.Therefore,weareunable
taskandshowedanteriorfrontalbrain these findings to electrophysiological toadjustforanyinfluenceofhabitualPA
patterns and incongruent task perfor- indices of cognitive flexibility, a novel on the findings. Future research would
mance similar to that of college-aged contributiontotheliterature. benefitfromstudydesignsthatinclude
adults after the intervention. This pat- Furthermore, the dose–response re- active control groups and account for
ternofresultswasnotobservedinthe lationshipobservedbetweenattendance thepotentialinfluenceoflifestylefactors
preadolescent wait-list control group. rate, brain function, and executive con- suchashabitualPA.
In a similar sample, Kamijo et al13 ob- trol demonstrates that brain and be-
servedthatdailyPA improvedworking havioralchangesresultedasafunction
CONCLUSIONS
memory performance and increased of the degreeof participationinthePA
frontal electrophysiological indices (ie, program. These results are consistent ParticipationintheFITKidsintervention
initial contingent negative variation) with Krafft et al25 who observed that improved aerobic fitness, as well as
PEDIATRICSVolume134,Number4,October2014 e1069
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brain and behavioral indices of ex- may have unintended effects.27 In- educational environment, and the con-
ecutive control among prepubertal deed, the current data not only textoflearning.
children. Importantly, these effects provide causal evidence for the ben-
wereselectivetoaspectsofcognition eficial effects of PA on cognitive and ACKNOWLEDGMENTS
thatrequiredextensiveinhibitionand brain health, but they warrant mod- Wethanktheparticipants,theirfamilies,
cognitive flexibility. Given the rapid ification of contemporary educa- and the Urbana School District 116 for
decline in PA opportunities for chil- tional policies and practices, and participating in the study. We thank
dren at school, the dissemination of indicate that youth should receive BonnieHemrickforherassistanceinpar-
ourfindingsisparticularlyimportant more daily PA opportunities.28 Fi- ticipantrecruitmentandrandomization.
for educators and policy makers. nally,giventhatscholasticsuccessin WealsothankDominikaPindusforpro-
Specifically, policies that reduce or reading and mathematics is heavily vidingvaluableinsightonthediscussion
replace PA opportunities during the reliant upon effective executive con- and analysis of the data, andwe thank
schoolday(eg,recess),inanattempt trol,29,30 our findings have broad the students and staff who aided in the
to increase academic achievement, relevance for public health, the implementationoftheFITKidsintervention.
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FINANCIALDISCLOSURE:Theauthorshaveindicatedtheyhavenofinancialrelationshipsrelevanttothisarticletodisclose.
FUNDING:AllphasesofthisstudyweresupportedbytheEuniceKennedyShriverNationalInstituteofChildHealthandHumanDevelopment(NICHD),National
InstitutesofHealth(NIH)grantRO1HD055352(toDrHillman).FundedbytheNationalInstitutesofHealth(NIH).
POTENTIALCONFLICTOFINTEREST:Theauthorshaveindicatedtheyhavenopotentialconflictsofinteresttodisclose.
PEDIATRICSVolume134,Number4,October2014 e1071
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