Swimming as a Positive Moderator of Cognitive Aging: A Cross-Sectional Study with a Multitask ...

12 Pages·2012·0.66 MB·English

HindawiPublishingCorporation
JournalofAgingResearch
Volume2012,ArticleID273185,12pages
doi:10.1155/2012/273185
Research Article
Swimming as a Positive Moderator of Cognitive Aging:
A Cross-Sectional Study with a Multitask Approach
AmiraAbou-Dest,Ce´dricT.Albinet,GeoffroyBoucard,andMichelAudiffren
UMRCNRS7295,UniversityofPoitiers,SportSciencesFaculty,Baˆt.A5,5rueTh´eodoreLefebvre,86000Poitiers,France
CorrespondenceshouldbeaddressedtoCe´dricT.Albinet,[email protected]
Received6August2012;Revised31October2012;Accepted14November2012
AcademicEditor:TeresaLiu-Ambrose
Copyright©2012AmiraAbou-Destetal. This is an open access article distributed under the Creative Commons Attribution
License,whichpermitsunrestricteduse,distribution,andreproductioninanymedium,providedtheoriginalworkisproperly
cited.
Thisstudyexaminedwhetherregularswimminginolderadultswasrelatedtobettercognitivefunctioningandwhetherthere
were any global or selective positive effects of this physical activity (PA) on cognition. The cognitive performances of three
groupsofsixteenvolunteerparticipants(youngadults,sedentaryolderadults,andolderadultswhoregularlypracticeswimming)
wereevaluatedusingamultitaskapproach.Allparticipantsperformedabatteryoftentasks:tworeactiontimetasksassessing
information processing speed and eight experimental tasks assessing three executive functions (EFs), (behavioral inhibition,
workingmemoryupdating,andcognitiveflexibility).Theresultsshowedthatyoungadultsperformedsignificantlybetterthan
olderadultsonallexaminedcognitivefunctions.However,inolderadults,regularswimmingwasrelatedtobetterperformance
onthethreeEFs,butnotoninformationprocessingspeed.Moreprecisely,fiveexperimentaltasksoutoftheeighttappingEFs
wereshowntobesensitivetopositiveeffectsfromswimmingpractice.Finally,thedemonstratedbenefitsofswimmingonEFswere
notnecessarilylinkedtobettercardiorespiratoryfitness.Thepresentfindingsillustratethevalidityofusingamultitaskapproach
inexaminingthepotentialbenefitsofregularPAoncognitiveaging.
1.Introduction swimming (one of the most popular and accessible forms
ofPAforolderadults)—onEFperformanceinapopulation
Thegrowthoftheproportionofthepopulationaged65and aged65to80yearsold.
older in the industrialized world, as well as in developing Executive functions involve higher-order functions of
countries, has profound implications for public health and control and coordination allowing behavioral adaptation
the economic costs of medical care. Cerebral and cognitive to complex or novel situations for which automatisms
decline, as a function of aging, represents a predominant or routines are inappropriate. As such, EFs refer to a
cause of autonomy loss in aging populations. According set of cognitive processes involved in goal and strategy
to the prefrontal-executive theory [1], executive functions formulation, planning and monitoring, mental flexibility,
(EFs) and their underpinning prefrontal and frontal brain and behavioral inhibition [7, 8]. This multicomponent or
structures are particularly sensitive to the effects of normal fractionated view implies that EFs may be composed of
andpathologicalaging[2,3].Therefore,thepreservationof different executive processes that are at least partially inde-
thesebrainareasandtheirassociatedcognitivefunctionsisof pendent,yetaresufficientlycorrelatedtorepresentaunique
particularimportance.Chronicphysicalactivity(PA),aimed construct.Inthisline,anauthoritativemodelwasdeveloped
atimprovingcardiorespiratoryhealth,hasbeenproposedto byMiyakeandcolleagues[9],whoproposedthatEFscanbe
be a good, practical, and powerful candidate to overcome fractionatedintoatleastthreeseparableprocesses;cognitive
cerebral and behavioral declines [4–6]. Accordingly, the flexibility (shifting between multiple tasks or mental sets),
principal aim of the present study was to examine the behavioralinhibition(suppressionofdominant,automatic,
potential benefits of an understudied form of PA—regular or prepotent responses when necessary), and updating of
2 JournalofAgingResearch
working memory (substitution of old information by new improvementincognitiveperformance,wheneffective,was
morerelevantinformationinworkingmemory).Thisthree- not related to the improvement in cardiorespiratory fitness
factorstructureofEFshasbeenfrequentlypostulatedinthe [21, 25]. Finally, Liu-Ambrose et al. [30] recently reported
literature and replicated in older populations [2, 10, 11]. the results of a randomized controlled study showing that
Although caution is still needed when choosing the tasks a12-monthresistancetrainingprogram(involvingstrength
used to assess this construct, all three EFs have been quite exercises twice a week) induced the same improvements
constantlyshowntobeimpairedinolderpeople,evenafter in EF performance and functional plasticity as an aerobic
having controlled for other confounders such as level of program.Thesefindingsemphasizetheneedtofurtherstudy
educationandinformationprocessingspeed[2]. the relationships between PA and cognitive performance in
In contrast to the prefrontal-executive theory, the pro- the aged population. In the present study, we wereparticu-
cessingspeedtheory[12]assumesthatage-relatedcognitive larlyinterestedinoneunderstudiedaerobicphysicalactivity:
declinesareaccountedforbygeneralizedslowingofcognitive swimming.Tothebestofourknowledge,onlyonestudywas
processing due to a diffuse or global deterioration of white designatedtoexplicitlytestthespecificrelationshipbetween
matter integrity throughout the whole brain with aging. A water aerobics and cognitive improvements in older adults
meta-analysis by Colcombe and Kramer [13] showed that [31].Inthisstudy,Hawkinsandcollaboratorsexaminedthe
the effect size of the positive effects of chronic exercise is influence of a 10-week program of basic swimming skills
significantly smaller on information processing speed than onvariationsoftwoexperimentaltasksinvolvingprocessing
onexecutivefunctions.Itisthenveryinterestingtocompare speed, attentional switching, and dual-task time-sharing.
the effects of aging and physical activity on these two They found that subjects who trained in water aerobics
functionsinthesameexperiment. showed significantly larger improvements on the executive
In contrast to this negative view of cognitive aging, a controltasksthananontrainedcontrolgroup.Interestingly,
new line of research has developed works that examine similar performance improvements were demonstrated for
how keeping a physically active lifestyle can maintain or bothgroupsinthenonexecutivetasks.Thus,itisimportant
evenimprovecognitionandbrainfunctions.Inrecentyears, toverifywhetherthisisolatedfindingcanbegeneralizedand
using various methodologies, several studies have shown to determine if swimming benefits are global or selective
that older adults who maintain a physically active way to some executive processes given the fractionated reality
of life by participating in regular PA or chronic exercise of EFs. To that end, we employed a clear theoretically
outperform their sedentary counterparts in cognitive per- drivenframeworktoexaminethepotentialmediatorroleof
formance, exhibit higher brain plasticity [14, 15] and are VO maxinthisrelationship.
2
more efficiently protected against neurological diseases and The objectives of the present study were twofold. First,
dementia [16, 17]. Moreover, randomized controlled trials we wanted to replicate our team’s previous results on age-
have demonstrated that short physical training programs relateddeclinesinEFandprocessingspeedperformance[2]
(from 3 months to 1 year) improve cognitive performance, bycomparingtheperformancesofyoungerandolderadults
particularlyEFs,insedentaryolderadultswithnopathology on various tasks that assess information processing speed
ofthecentralnervoussystem[18–21]ordementia[22,23]. and the three postulated EFs, inhibition, working memory
Narrative and meta-analytic reviews tend to show that this updating, and shifting. Second, assuming these age-related
positive effect may be particularly selective to attentional, cognitive declines, we wanted to determine the selectivity
controlled cognitive functions involving EFs (see [4, 13, of the relationship between swimming and the three EFs
24]) and that the PA programs should involve a strong and information processing speed, in our sample of older
proportion of aerobic exercises (see [4, 13, 25]). Moderate- adults. An important feature of this experiment was to
to-vigorous PA induces improvements in cardiorespiratory combinetheuseoftwoorthreecognitivetasksthatarewell-
fitness (indexed by maximal oxygen uptake, VO max) and knownfortappingeachofthecognitivefunctionsofinterest
2
leadstoacascadeofneurophysiologicalmechanismssuchas with a multivariate approach. This procedure was shown
thereleaseofneurotrophicfactorsthatfacilitateneurogenesis to accurately assess the construct of EF and to reveal age-
and/orangiogenesis[19,26–28],twomechanismsknownto related executive declines in a previous pool of participants
be associated with higher brain plasticity, which ultimately [2]. Swimming was chosen for three main reasons. (1) It
leadstoimprovementsincognitiveperformance.Itisimpor- is an understudied aerobic activity in the field of cognitive
tanttonotethat,ontheonehand,theputativelinksbetween aging, and it solicits all the muscle groups and increases
neurophysiological mechanisms and efficiency of cognitive cardiorespiratoryfitness.(2)Itisoneofthemostaccessible
processes are not yet fully understood and, on the other and practiced PAs in the elderly and is rated as the second
hand, the possible mechanisms explaining these links are most popular PA in France for the age range 65 and older
mostlikelynotexclusive.Anumberofreviewsonthistopic [32]. (3) It is less traumatic on joints than walking or
suggest a concomitant increase in cardiorespiratory fitness, jogging.Severalreviewshavedescribedthebeneficialeffects
brainplasticity,andcognitiveperformance,butinconsistent ofwater-basedexerciseonphysicalfitnessparameters,such
results have been reported concerning the last point. For asaerobiccapacityandstrengthintheelderly[33–35].The
instance, some authors have been unable to show cognitive elderly take a particular interest in water activity because
improvements after an aerobic exercise program that was it reduces the fear of falling, limits tolerance for weight-
sufficienttoincreaseVO max[29].Othershaveshownthat bearingactivities,andenhancesadherenceandparticipation
2
not all EFs are enhanced after a PA program and that the [36].
JournalofAgingResearch 3
2.Methods 2.4.EvaluationofExecutiveFunctions. EachofthethreeEFs
wasassessedvia2or3differentexperimentaltasks.Alltasks
2.1.Participants. Thirty-twoolderadultsaged65to80years were the same as those used in a previous study from our
(16 sedentary people and 16 swimmers) and 16 younger laboratory that involved a different sample of younger and
adults (18–30 years), all of whom were free of neurological older adults [2]. We refer the reader to this paper for a full
and cardiovascular disease, participated to this study. The descriptionoftheprocedureandtasksused.
older participants were recruited from senior community
centers, civic groups, and aquatic centers through the use
2.4.1.Inhibition
of flyers and newspapers. All the older participants were
screened by their personal physicians who rated them as TheStroopTask. InthiscomputerizedversionoftheStroop
beingingoodhealthandsignedamedicalcertificateindicat- task,thedependentvariablewasthedifferenceinmeanRTs
ingnocontraindicationsforcardiorespiratoryfitnesstesting. (ms)betweenincongruenttrials(e.g.,thewordREDwritten
Younger participants were recruited from the University of inblue)andneutraltrials(e.g.,XXXXXwritteninblue)for
Poitiers. correctresponses.Theerrorrateinincongruentandneutral
Inclusion criteria for older adults were as follows: (a) conditions was also controlled to check for any possible
being aged between 65 and 80 years; (b) having adequate speed-accuracytradeoffs.
mentalstatusasindicatedbyascorestrictlygreaterthan25
on the Mini Mental State Examination (MMSE) [37]; (c) TheStop-SignalTask. Inthistask,participantswererequired
forthesedentarygroup,leadingasedentarylifestylewithno to respond as quickly as possible to a visual stimulus by
participationinanystructuredPAasassessedbyavalidated pressing the corresponding key, unless an auditory tone
PA questionnaire, the Dijon Score of Physical Activity rang out requiring to abort (or inhibit) the prepotent
(DSPA) [38]; (d) for the active group, leading a physically motor response. The dependent variable selected for the
active lifestyle as assessed first by a history of regularly multivariate analyses of variance (MANOVAs) was the rate
swimmingatleasttwiceaweekforatleasttwoyearsbutno of successful inhibition calculated as the probability (P,
otherregularPA.Secondly,theDSPAwasalsoadministered between 0 and 1) of successful inhibition. The stop-signal
for the active group to ensure a significant difference in reaction time (SSRT) has also been calculated according to
the amount of physical activity between the two groups. Logan’s race model [41]. This variable was not included
Inclusion criteria for younger adults were being aged from in the MANOVAs for two reasons: (1) SSRT correlated
18 and 30 years. The exclusion criteria were the following: moderately with SRT and CRT (r = .41 and .50, resp.),
(a)usingmedicationthatcouldaffectcardiovascularhealth whileP(I)didnot(seeTable2);(2)SSRTdidnotcorrelate
orcognitivefunctions;(b)cardiorespiratoryorneurological withtheinterferencescoremeasuredintheStrooptaskand
disease;(c)majorsurgerywithinoneyearpriortotesting.All theadjacencyscoremeasuredintheRNGtask,twovariables
participantsgavewritteninformedconsentandthestudywas reflecting inhibition (r = .13 and r = −.06, resp.), while
approved by the local ethics committee. The demographic P(I) correlated significantly with the adjacency score (see
and physical characteristics of all participant groups are Table2).
displayedinTable1.Theactiveolderadults(swimmers)had
been practicing swimming for two to 43 years (M = 2.56
The Random Number Generation (RNG) Task. In this task,
years;SD=0.79),twotofivetimesaweek.Themeansession
participantswererequiredtogenerateandsayaloudseriesof
durationwasbetween45and100minutes(M=64.38min;
randomnumbersfromonetonineattherateofonedigitper
SD=15.37).
second.Thedependentvariablethatreflectedinhibitionfor
thistaskwastheAdjacencyscore(Ain%),rangingfrom0%
2.2. Evaluation of Cardiorespiratory Fitness. For the older (noneighboringpairs,i.e.,goodperformance)to100%(only
participants,VO2maxwasestimatedbytheRockportFitness neighboring pairs, i.e., poor performance). The RNG task
Walkingtest[39].Thissubmaximalfieldtesthasbeenshown necessitatesinhibiting countingin ascendantordescendant
toaccuratelyestimateVO2maxinpopulationssimilartothe series,andtheAdjacencyscoremeasuresthetendencyofthe
oneinthepresentstudy[39,40].Participantswererequired participantstocountbyone.
towalkonemile (1609m)asquicklyaspossible, and heart
rate was continuously recorded by a Polar RS 800 beat-to-
2.4.2.Updating
beatrecorder(PolarElectro,Oy,Kempele,Finland).VO max
2
was calculated using the equation developed by Kline and The Verbal Running Span Task. In this computerized task,
collaborators. participants were required to recall serially the last four
letters of a list of six, eight, ten, or twelve consonants
2.3.EvaluationofInformationProcessingSpeed. Information that were presented visually. The dependent variable was
processing speed was measured through two reaction time the number of letters correctly recalled in the right order
tasks: an auditory simple reaction time (SRT) task and a (max.=48).
visual2-ChoiceReactionTime(CRT)task[2].SRTandCRT
wereusedasthemaindependentvariablesandtheerrorrate ThespatialRunningSpanTask. Likefortheprevioustask,in
intheCRTtaskenabledcheckingforpossiblespeed-accuracy this computerized task, participants were required to recall
tradeoffs. serially the last four spatial locations of a dot in a 4 × 4
4 JournalofAgingResearch
Table1:Characteristicsofthethreegroupsofparticipants.
Activeolder Sedentary Youngversus Activeversus
Characteristics Youngadults
adults olderadults olderadults Sedentary
n 16 16 16 P=1 P=1
GenderM/F 9/7 9/7 9/7 P=1 P=1
Age(years) 23.56(2.56) 69.13(3.88) 69.25(3.25) P<.05 P=.92
MMSE(max=30) 29.31(0.01) 28.75(0.93) 28.69(1.08) P=.06 P=.86
Education(years) 16.09(1.25) 13.75(3.11) 13.56(1.93) P<.05 P=.84
DPAS(max=30) — 24.25(1.48) 15.17(4.37) — P<.05
VO max(mL/min/kg) — 29.35(5.13) 25.27(4.94) — P<.05
2
Note.M:Male,F:Female,MMSE:MiniMentalStateExamination,DPAS:DijonPhysicalActivityScore.
matrix. The dependent variable was the number of dots periodically. The dependent variable that reflected shifting
correctlyrecalledintherightorder(max.=48). forthistaskwasthenumberofperseverativeerrors.
For the processing speed construct and for each EF
component, a standardized Cronbach alpha was computed
2.4.3.Shifting
to assess how well the selected tasks measured a latent
construct.Alphasforeachpostulatedcognitivefunctionwere
The Dimension-Switching Task. In this computerized task,
low to good (standardized Cronbach alphas were .77, .60,
participants watched on the computer screen the French
.78, and .59 for Information processing speed, Inhibition,
wordsforLEFTorRIGHTenclosedinaleftorrightarrow,
Updating,andShifting,resp.).Table2presentstheresultsof
anddisplayedaboveorbelowthecenterofthewhitescreen.
the bivariate correlations between all cognitive tasks within
Depending on instructions, they were required to respond
thewholesample.
tothewordortothedirectionofthearrowbypressingthe
correct corresponding key. The dependent variable selected
forthistaskwastheglobalswitchcostforcorrectresponses, 2.5. Procedure. After careful screening for inclusion and
calculated as the difference in RT (ms) between trials from exclusioncriteria,olderparticipantswerefirstevaluatedfor
the simple blocks and task-repeat trials from the mixed cardiorespiratory fitness on one day. Second, each partici-
blocks. The error rate in simple and mixed blocks of trials pantwastestedindividuallyinaquietexperimentalroomin
was calculated to check for any possible speed-accuracy two sessions on different days separated by a minimum of
tradeoffs. The local switch cost was also calculated but was twodaysandamaximumofsevendays.Eachsessionlasted
notincludedforfurtheranalysesbecauseitdidnotcorrelate approximately 1.5–2 hours. The two sessions were counter-
with the number of perseverative errors in the Wisconsin balanced across participants and, within each session, all
CardSortingTask(r = .18)whiletheglobalswitchcostdid taskswerecounterbalancedacrossparticipants.Participants
(r =.32,seeTable2). weregivenshortbreaksbetweeneachexperimentaltask.
2.6.StatisticalAnalyses. Thedataoncognitiveperformance
Stimulus-Response Compatibility Switching Task. In this
were analyzed in three ways. First, a series of one-way
computerized task, participants watched an arrow pointing
multivariate planned analyses of covariance (MANCOVAs)
leftorright,surroundedbyaframeonthecomputerscreen.
wasconductedoneachsetofdependentvariablesreflectinga
Depending on the color of the frame, participants were to
specificcognitivefunction(speedofinformationprocessing,
presstheresponsekeylocatedeitheronthesidepointedby
behavioral inhibition, updating of working memory, and
the arrow (green or blue frame), or on the opposite side
shifting), contrasting young adults and seniors with level
(redororangeframe).Thedependentmeasureforthistask
of education (number of years) as a covariate. This first
was the local switch cost for correct responses, calculated
series of planned MANCOVAs was conducted in order to
as the difference in RT (ms) between task-repeat trials and
testtheeffectofageoneachcognitivefunction.Thelevelof
task-switchtrialsduringthemixedblocks.Theerrorratefor
educationwasenteredasacovariatebecauseyoungeradults
repetitionandalternationtrialswasalsocomputedtocheck
showed a higher level of education than older adults (see
foranypossiblespeed-accuracytradeoffs.Theglobalswitch
Table 1). When the effect of age on a cognitive function
costhasnotbeencomputedinthistaskbecausethenumber
was significant, we conducted a series of planned analyses
oftrialsinthesimpleblockswastoosmall;thesimpleblocks
of covariance (ANCOVAs) on each cognitive function task,
haveonlybeenusedtofamiliarizeparticipantstotherulesof
contrastingyoungadultsandseniorswithlevelofeducation
mappingbetweenstimuliandresponses.
as a covariate. Second, a series of one-way multivariate
plannedanalysesofvariance(MANOVAs)wasconductedon
TheWisconsinCardSortingTest(WCST). Inthiscomputer- the same sets of dependent variables only in older adults,
izedversionoftheWCST,participantswererequiredtosort contrasting regular swimmers and sedentary people. This
asetofcardsaccordingtothreedifferentrulesthatchanged secondseriesofplannedMANOVAswasconductedinorder
JournalofAgingResearch 5
Table2:Matrixofcorrelationsbetweentheindicesofcognitiveperformance,oneindexpercognitivetask,forthewholesample.
Dependentvariable/Task 1 2 3 4 5 6 7 8 9 10
(1)AuditorySRT 1.00
(2)VisualCRT .63∗ 1.00
(3)P(I) −.05 −.02 1.00
(4)Interferencecost .42∗ .43∗ .18 1.00
(5)Adjacencyscore .16 .34∗ .31∗ .51∗ 1.00
(6)NOcorrectletters −.18 −.29∗ .10 −.26 −.56∗ 1.00
(7)NOcorrectlocations −.30∗ −.69∗ −.03 −.51∗ −.63∗ .64∗ 1.00
(8)NOperseverativeerrors .23 .30∗ .04 .40∗ .58∗ −.52∗ −.55∗ 1.00
(9)Globalswitchingcost .08 .54∗ −.03 .20 .49∗ −.51∗ −.69∗ .32∗ 1.00
(10)Localswitchingcost .25 .46∗ .01 .20 .46∗ −.40∗ −.44∗ .22 .42∗ 1.00
Note.SRT:Simplereactiontime,CRT:Choicereactiontime,P(I):Rateofsuccessfulinhibitions,∗:P<.05,bold:Correlationswithinthesamecognitive
function.
to test the effect of physical activity level on each cognitive AfirstANOVAwasconductedonerrorrateintheCRTtask
function.WhentheresultoftheMANOVAwassignificant, withageasbetween-subjectsfactor.Therewasnosignificant
we performed a series of planned analyses of variance effect of age (F(1, 45) = 0.22; P > .63); error rate = 2.81%
(ANOVAs) on each of the individual tasks composing and 2.44% for younger and older adults, respectively. A
cognitivefunction.Finally,fortheolderadultsample,simple second ANOVA with age as between-subjects factor and
regression analyses were performed between VO max and typeoftrials(neutralversusincongruent)aswithin-subjects
2
EF scores when there was a significant correlation between factor was then conducted on error rate in the Stroop task.
these variables. The level of significance was set at P < .05 The interaction between age and type of trials was close to
and Cohen’s d was reported for pairwise comparisons as a significance(F(1,45)=3.40;P>.07),thesimpleeffectofage
measureofeffectsize.AsproposedbyCohen[42],a“small” wasnotsignificant(F(1,45)=0.98;P>.32)whilethesimple
effect is when d = 0.2, a “medium” effect when d = 0.5, effectoftypeoftrialsreachedsignificance(F(1,45)=12.10;
and a “large” effect when d = 0.8. For the MANOVAs P <.002).Participantsmadesignificantlymoreerrorsinthe
and MANCOVAs, partial eta squared (Partial η2) was also incongruentcondition(2.43%)thanintheneutralcondition
reportedasameasureofthepercentage(whenmultipliedby (0.35%).AthirdANOVAwithageasbetween-subjectsfactor
100)ofvarianceexplainedbythetreatmentfactors. andtypeofblockoftrials(simpleversusmixed)aswithin-
subjectsfactorwasconductedonerrorrateinthedimension-
switchingtask.Theinteractionbetweenageandtypeofblock
3.Results
oftrialswasclosetosignificance(F(1,45)=3.60;P>.06),as
3.1.GroupDifferencesinDemographicsandGlobalCognition. wellasthesimpleeffectofage(F(1,45)=3.18;P>.08),but
theeffectoftypeofblockoftrialsreachedsignificance(F(1,
As seen in Table 1, young adults attended more years of
education than older participants (F(1, 46) = 12.97; P < 45)=26.25;P<.0001).Participantsmadesignificantlymore
0.05).Inaddition,asexpected,olderactiveparticipantswere errorsinthemixedblockoftrials(5.07%)thaninthesimple
blockoftrials(1.61%).AfourthandlastANOVAwithageas
more physically active than their sedentary counterparts as
revealed by a higher score on the DPAS (F(1, 30) = 60.75; between-subjectsfactorandtypeoftrials(alternationversus
P < 0.05), and a higher level of VO max (F(1, 29) = 5.13; repetition)aswithin-subjectsfactorwasconductedonerror
2
P<0.05),butthetwogroupsdidnotdifferinMMSEscores. rate in the mixed blocks of trials of the stimulus-response
compatibility switching task. The interaction between age
and type of transition did not reach significance (F(1, 45)
3.2. Effects of Chronological Age on Cognitive Functions. = 1.89; P > .17), but the simple effects of age and type
Resultsofthestatisticalanalysesandbehavioralperformance of transition did (F(1, 45) = 6.07; P < .02 and F(1, 45) =
as a function of age group for each cognitive function and 37.10; P < .0001, resp.). All participants made more errors
eachcognitivetaskaredetailedinTable3.Asseen,therewas when they had to alternate (9.27%) rather than when they
a significant effect of age on each cognitive function, even had to repeat the stimulus-response mapping (3.33%) and
afterhavingcontrolledforthelevelofeducation.Subsequent olderadults(7.63%)mademoreerrorsthanyoungeradults
ANCOVAs on each individual dependent measure revealed (3.63%). These results on error rate and those concerning
thattheage-relatedeffectwassignificantforeachexperimen- RTs (see Table 3) showed that there was no speed-accuracy
taltask(seeTable3)exceptforthree:thestop-signaltask,the tradeoffsfortheeffectofageoncognitivefunctionsassessed
letterrunning-span,andtheWCST,forwhichtherewasno throughRTtasks.
significantdifferencebetweenyoungerandolderadultsafter
havingcontrolledforeducationlevel.
Theeffectofagewasalsoexaminedonerrorrateforall 3.3. Effects of Swimming Practice on Cognitive Functions
the tasks that included choice reaction time measurements. Performance in Older Adults. The results of the statistical
6 JournalofAgingResearch
n
ate,andmea OlderadultsM(SD) 257(52) 475(53) 0.44(0.21) 291(115) 42.27(11.29) 34.28(7.35) 23.31(10.30) 12.81(7.22) 606(299) 184(135)
ri
a
cationascov YoungadultsM(SD) 194(26) 335(28) 0.41(0.15) 189(63) 33.50(7.04) 39.19(4.62) 41.25(4.84) 8.50(2.68) 192(154) 71(57)
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le he 1 4 6 0 3 0 3 9 4 9
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performanc ANCOVAF(1,44) 23.06<(P.0001) 94.89<(P.0001) 1.13=.29)(P12.46<(P.001)5.96<(P.02)2.69=.11)(P36.81<(P.0001) 3.69=.06)(P15.65<(P.0003)9.86<(P.0031)
e
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ntrasting MANCO 47.98<(P.000 4.29<(P.001 19.77<(P.000 8.37<(P.000
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c
ffoftheMANCOVAs,ANCOVAs,andeect-sizesmanceforeachagegroup(SD). DependentCognitivetasksvariables AuditorysimpleReactiontimereactiontimetask(ms) VisualchoicereactionReactiontimetimetask(ms) RateofsuccessfulStop-signaltaskinhibitionInterferencecostStrooptask(ms) RNGtaskAdjacencyscore NOcorrectLetterrunning-spantaskresponsesyNOcorrectSpatialrunning-spanresponsestaskWisconsincardsortingNOperseverativetesterrorsDimensionswitchingGlobalswitchcosttask(ms)Stimulus-ResponseLocalswitchcostswitchingtask(ms)ffmNumberGeneration,inbold:Significanteect.
ultsrfor mor ndo
Table3:Resbehavioralpe Cognitivefunctions Speedofinformationprocessing Behavioralinhibition Updatingofworkingme Shifting Note.RNG:Ra
JournalofAgingResearch 7
analyses and behavioral performance as a function of level 3.4.RelationshipbetweenCardiorespiratoryFitnessandExec-
ofactivityforeachcognitivefunctionandeachexperimental utive Function. To examine the relationships between car-
task are detailed in Table 4. The MANOVAs revealed a diorespiratory fitness and EF performance in older adults,
significant effect of swimming activity on each of the three we performed a series of bivariate correlations (Spearman
EF components but no significant effect on information coefficients of correlation) between each cognitive task
processingspeed.SubsequentANOVAsoneachtasktapping performance and VO max level. The performance of only
2
EFs showed that older participants who swim regularly two tasks significantly correlated with VO max level: the
2
performedsignificantlybetterinfiveoutofeighttests.More updating of verbal information (r = .56; P < .05) and
precisely,swimmersoutperformedsedentaryparticipantson the global switch cost (r = .46; P < .05). Figure 1
thetwotaskstappingUpdating,ontwoofthreetaskstapping depicts the scatter plots of executive performance on these
Shifting, and on the RNG task tapping Inhibition. When it taskswithVO maxlevelwiththeirrespectivecoefficientsof
2
wassignificant,theeffectsizeofswimmingwaslarge(mean determination(R2).
Cohen’sd=1.05).
Theeffectofswimmingwasexaminedonerrorrateforall
the tasks that included choice reaction time measurements. 4.Discussion
A first ANOVA was conducted on error rate in the CRT
task with PA level as between-subjects factor. There was Ashasbeenextensivelydocumented,age-relatedcerebraland
a significant effect of PA level on error rate (F(1, 45) = cognitive declines are not uniform but quite differentiated
8.24; P < .007); sedentary older adults made more errors (see [43, 44] for reviews). Similarly, most of the recent
in the CRT task (3.75%) than older swimmers (1.13%). literature on aging, fitness, and cognition has shown that
A second ANOVA with PA level as between-subjects factor chronic exercise would result in selective improvements in
and type of trials (neutral versus incongruent) as within- executive functions rather than general benefits [13, 20,
subjects factor was conducted on error rate in the Stroop 21].However,contemporarytheoreticalmodelsofexecutive
task. There was a significant interaction between these two functions posit that the construct of EF is not uniform
factors (F(1, 45) = 8.07; P < .007). A post hoc test but encompasses fractionated executive subprocesses [2,
showed that sedentary older adults made more errors in 8, 9]. It is then important to examine whether chronic
the incongruent condition than in the neutral condition exercise benefits are homogeneous or selective to some
(3.39% versus0%, respectively; P < .02) while older adults particular executive subprocesses. Using this established
whopracticedswimmingdidnot(1.24%versus0.26%resp.; theoretical and methodological framework, the aim of this
P > .45).AthirdANOVAwithPAlevelasbetween-subjects study was to examine differences in cognitive performance
factor and type of block of trials (simple versus mixed) as a function of chronological age and long-term regular
as within-subjects factor was conducted on error rate in practice of swimming by measuring younger and older
the dimension-switching task. The interaction between PA adults’ information processing speed and performance on
level and the type of block of trials was significant (F(1, three well-known EFs, inhibition, updating, and shifting.
45) = 10.81; P = .002). A post hoc test showed that Globally, the results revealed a clear pattern of age-related
older swimmers made more errors in the mixed than in decline in all cognitive functions. On the other hand, older
the simple block of trials (8.68% versus 1.61%; P < .0002) adultswhopracticeregularswimmingwereshowntohavea
while sedentary older adults did not (3.26% versus 1.67%; positiverelationwithimprovedperformanceonfiveofeight
P > .34). The examination of RT and error data in the experimental tasks and all EF components. VO max level
2
dimension-switching task suggests that the two groups of wasonlypositivelyrelatedtoexecutiveperformancefortwo
older adults did not use the same strategy in the more tasks. These results provide a clear argument for the use of
difficultcondition:swimmerspreferredtoemphasizespeed a multitask approach when studying the effects of chronic
whereas sedentary people preferred to emphasize accuracy. exerciseoncognitivefunctions.
AfourthandlastANOVAwithPAlevelasbetween-subjects Before examining the effects of aging and swimming
factor and type of trials (alternation versus repetition) as practiceoncognitiveperformance,itisimportanttodiscuss
within-subjects factor was conducted on error rate in the the multitask approach used in this study. Because it is
mixedblocksoftrialsofthestimulus-responsecompatibility impossibletofinda“pure”tasktoassessanisolatedcognitive
switching task. The interaction between PA level and type function,particularlyanEF,multiplemeasureswereusedto
of transition did not reach significance (F(1, 45) = 0.61; ruleout“taskimpurity”(see[2,7–9]).Assuch,wewanted
P > .43), but the simple effects of PA level and type to assess the EF construct at the level of a general or latent
of transition did (F(1, 45) = 12.43; P < .001 and F(1, variable, which reflects the postulated cognitive function
45) = 33.25; P < .0001, resp.). Older adults made more morestronglythaneachindividualexperimentaltaskalone.
errors when they had to alternate (11.07%) rather than However, as revealed by the standardized Cronbach alphas
when they had to repeat the stimulus-response mapping andthematrixofcorrelationsdisplayedinTable2,itappears
(4.19%)and,overall,olderswimmers(10.94%)mademore that the construct validity of our three EFs was quite low.
errorsthansedentaryolderadults(4.33%).Onemoretime, Indeed,thecorrelationsbetweentaskssupposedtoreflecta
swimmers preferred to emphasize speed while sedentary particularEFcomponentwereoftenloworevennonsignif-
participants preferred to emphasize accuracy in the more icant and sometimes smaller than the correlations between
difficultcondition. two tasks thought to assess different EF components. Such
8 JournalofAgingResearch
e
g )
ceforeacha ActiveolderadultsM(SD) 262(64) 482(57) 0.44(0.20) 285(99) 37.82(9.91) 38.63(5.88) 27.19(10.80 8.63(2.36) 508(306) 135(126)
n
oralperforma SedentaryolderadultsM(SD) 252(40) 468(49) 0.44(0.23) 297(132) 46.72(11.09) 29.94(6.08) 19.44(8.39) 17.00(8.05) 704(267) 232(129)
vi
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performa ANOVAF(1,45) — — 0.00=.96)(P0.10=(P.76)7.04<(P.011 19.50<(P.0007.04<(P.013 21.70<(P.0002.65=.11)(P6.24<(P.017
e
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ntson Parti .02 .16 .30 .42
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contrastinga MANOVAF 0.43=.73)(P 2.79=(P.05) 9.61<(P.0004) 10.24<(P.0001)
ffNOVAs,andeect-sizes Dependentvariable Reactiontime(ms) Reactiontime(ms) Rateofsuccessfulinhibition Interferencecost(ms) Adjacencyscore NOcorrectresponses NOcorrectresponses NOperseverativeerrorsGlobalswitchcost(ms)Localswitchcost(ms)ffinBold:Significanteect.
Table4:ResultsoftheMANOVAs,Agroup(SD). CognitiveCognitivetaskfunction AuditorysimpleSpeedofreactiontimetaskinformationVisualchoicereactionprocessingtimetask Stop-signaltask BehavioralStrooptaskinhibition RNGtask Letterrunning-spanUpdatingoftaskworkingSpatialrunning-spanmemorytask WisconsincardsortingtestDimensionswitchingShiftingtaskStimulus-Responseswitchingtask Note.RNG:RandomNumberGeneration,
JournalofAgingResearch 9
50
1400
45
mber of correct responses in theverbal running span task 43320505 obal switch cost (ms) in thedimension switching task11208640000000000 R2=0.2138
u Gl
N 20 200
R2=0.3146
15 0
10 20 30 40 10 20 30 40
VO2max(mL·min−1·kg−1) VO2max(mL·min−1·kg−1)
(a) (b)
Figure1:ScatterplotsrelatingVO maxlevelandupdatingperformanceofverbalinformation(a)andglobalswitchcost(b)intheolder
2
participants.
resultshavealreadybeenreportedbypreviousstudiesfrom processingspeed,asassessedbytheSRTandtheCRTtasks
ourownteam[2]andothers[11,45]andraiseaquestionof (seeTable4).Thisresultcontrastswithsomepreviousresults
thelowspecificityofthetasksusedtoassessEFs,whichwill [48, 49] but agrees with others [20, 21, 24], particularly
bediscussedinthelimitationssection. with those of Hawkins and coworkers [31] in the same
Consistent with a large body of research on cognitive contextofswimmingpractice.Thesecontradictingfindings
and cerebral aging, we found that chronological age has a may be due to specific differences between particular PAs
detrimental effect on information processing speed and on practicedbydifferentsamplesofparticipants.Theimpacton
the three evaluated EFs. The age-related decline in the RT processing speed may be different between racket sports or
tasksisinagreementwithnumerousstudiesontheeffectof hand-ball, such as in Spirduso’s study [49], and swimming
agingonprocessingspeed[2,12].Theperformancedeficits such as in our study. Another, more likely possibility is
observed in our older adults in the three EF domains also linked to the assertion that chronic exercise exerts selective
agree with the literature examining this question with a effectsoncognitiveprocessesinvolvingexecutivecontroland
similar approach [2, 10, 11]. Our results also suggest that notonless-controlledprocesses,suchasthestimulus-driven
the deleterious effects of aging are more pronounced for informationprocessinginvolvedinbasicreactiontimetasks
processingspeed(69%oftheexplainedvariance,seepartial (see [13, 20, 24]). Our results favor this second possibility
η2 in Table 3) than for updating (48% of the explained andstrengthenthisselectivebenefitofPAonEFprocesses.
variance), shifting (37% of the explained variance), and Second,ourresultsindicateprimafaciethattheimpact
inhibition (23% of the explained variance). However, it is of swimming practice was quite homogeneous across all
important to note that taking into account the educational threeEFcomponents,assumingthatourgroupsonlydiffered
level(asmeasuredbythenumberofyearsofacademicedu- at the level of swimming practice. All three MANOVAs
cation)decreasedtheage-relatedeffectsonallthecognitive contrasting the performance between older swimmers and
tasks and even eliminated the effects of chronological age sedentary participants were significant for these cognitive
ontheletterrunning-spantaskandtheWCST.Thisfinding functions. However, the percentage of variance explained
strengthenstheimportanceoftakingintoaccounteducation by swimming practice was more important for Shifting
asanimportantmoderatorofcognitiveagingwhichcanbe (42%) than for Updating (30%) and Inhibition (16%), as
interpretedinthemoregeneralcontextofcognitivereserve revealed by partial eta squared (see partial η2 in Table 4).
[46,47].Aswewilldiscussbelow,itmaybethatPA(inthe Our results of a strong relationship between swimming
presentstudy,swimming)couldalsobeviewedasaproxyof practice and Shifting confirm the previous conclusions of
cognitivereservebeyondeducationallevel. Hawkins et al. [31] on the positive effect of water aerobics
In the older population, the differences in cognitive on attentional flexibility. However, as pointed out in the
performancebetweenswimmersandsedentarypeoplewere Results section, the examination of speed and accuracy
nothomogeneousacrossallthestudiedcognitiveprocesses. measures in the two switching tasks underscores that the
First, there was no significant difference between active two groups of participants may not have used the same
and sedentary participants in the measures of information strategiestoperformthesetasks.Theswimmersmademore
10 JournalofAgingResearch
errors and emphasized speed to the detriment of accuracy. Table4).Thus,thereisonlyonetask(theverbalrunningspan
Consequently, the speed-accuracy tradeoffs observed in the task)showingPA-relatedbenefitsthatcouldbemediatedby
two switching tasks weaken the strength of the positive cardiorespiratoryfitnesslevelandonetask(thedimension-
relationshipbetweenswimmingpracticeandShifting. switching task) showing no relationship with swimming
Moreover, five out of eight tasks were strongly sensitive practice but a significant relationship with VO max level.
2
todifferencesbetweenswimmersandsedentaryparticipants, These results underscore the differences between a behav-
but the performance of two tasks out of three (Stroop task ioral measure assessed through questionnaires (PA) and
andsignal-stoptask)assessinginhibitionandonetaskoutof an estimated physiological measure assessed through field
three (dimension-switching task) assessing shifting did not test (VO max), and their different influences on different
2
significantlydifferbetweenregularswimmersandsedentary cognitivefunctions[21,25,51].DistinguishingbetweenPA
participants. As previously stated, we think that this result andcardiorespiratoryfitness,whichwereweaklyrelated(r =
underscores the importance of using a multitask approach .35; P = .054) in the present study, seems of particular
when studying the effects of chronic exercise on cognitive importance because they may exert their influence on
functions and may help to resolve some discrepant results cognitive functioning by different mechanisms. A challenge
in this domain. For example, the absence of significant for future studies will be to understand and characterize
effect of exercise training reported by other researchers themechanismsunderlyingtheseselectiveeffects.Onemay
on some cognitive tasks [21, 29, 50] may not reflect an hypothesizethatPAcouldbeviewedqualitativelyasaproxy
absence of real effects but instead a lack of sensitivity of of cognitive reserve, as defined by Stern and collaborators
the experimental tasks. For instance, our results conflict [46, 47], allowing physically active older adults to make
with those reported by Smiley-Oyen et al. [21], because flexible and efficient use of available brain reserve and to
they found an effect of aerobic exercise on the Stroop demonstratebettercognitiveperformance.Inotherrespects,
task and no effect on the WCST. Several reasons can be bettercardiorespiratoryfitnesscouldinduceanatomicaland
hypothesizedtoexplainthediscrepancies,suchasdifferences neurophysiological changes in the brain [6, 14, 26–28] that
instudydesign,experimentaltasks,modesofresponse,and couldreflectandenhancebrainreserve[46,47].
selected dependent measures, but it is always difficult to There are potential limitations in the present study
definitively conclude which is the correct explanation. One that should be addressed. First, the low specificity of the
of the strengths of the present study is to combine the tasks used to assess the construct of EF in this study
use of several different experimental tasks to examine the limitsthegeneralizabilityofourconclusionsandstrengthens
influence of PA within the same sample not only at the the importance of looking for and using well-designed
level of individual tasks but also at the more general level tasks to reflect the postulated cognitive functions. Sec-
oftheexploredcognitivefunctions.Thisprocedureallowed ond, our cross-sectional design precludes inferences about
us to show that regular swimming was clearly related to causality in the relationship between chronic engagement
better executive performance on the three examined EFs, in swimming and executive performance. Well-designed
despitetheabsenceofsignificanteffectonthreeoftheeight randomized-controlled trials are now needed, using the
tasks. This may indicate that some tasks could be more same multitask approach, before a definitive conclusion
sensitive to the effects of PA than other tasks. Additional can be made. Third, the level of education of the partic-
work should verify the consistency of our results, as our ipants has been taken into account as a covariate in the
findings are far from conclusive. A recent study from our statistical analyses of the present study. However, other
group [51] used different measures of PA and explored the important moderators of aging related to lifestyle, such as
same executive functions with different tasks or variations income,socioeconomicstatus,foodhabits,previouscareers,
of the same tasks as used in the present study and showed and lifelong leisure activities, have not been measured in
that PA exerted a selective effect on inhibition but not on our experiment. These different variables can explain part
updating or shifting and only for the oldest adults of the of the variance in cognitive aging and may lead to an
sample(71yearsandolder).Thesedifferentresultshighlight overestimation of the relationship between present level
thelabilityoftheeffectsofexerciseoncognitiveperformance of physical activity and cognitive performance in cross-
according to tasks and characteristics of the participants. sectionaldesigns,ascouldhavebeenthecaseinthepresent
Clearly,moreworkisneededtodrawadefinitiveconclusion study.
ontheselectivityoftheeffectsofchronicexerciseeffectson Tosummarizetheprincipalfindings,thisstudydemon-
EFs. stratedthevalidityofusingamultitaskapproachinexamin-
The role of cardiorespiratory fitness in the relationship ingthepotentialbenefitsofregularswimmingontheaging
between PA and cognitive performance in older adults ofcognitivefunction.Suchatheoreticalandmethodological
remainsunderdebate(see[4,21,25]).Accordingly,wewere approachallowedustoshowthatchronicswimmingpractice
interested in examining the relationships between VO max isrelatedtobetterexecutivefunctionsinolderadultsandthat
2
level and cognitive performance. As shown in Figure 1, thesebenefitsareseenonthethreeEFsstudiedbutthatsome
only performance on the verbal running span task and the tasks are less sensitive to detecting these benefits. Finally,
dimension-switching task was significantly correlated with thedemonstratedbenefitsofPAwerenotnecessarilylinked
VO max level. Of particular interest, one must remember to better cardiorespiratory fitness, showing the potential
2
that there was no significant effect of PA on the global relative independence of these behavioral or physiological
switch cost of the dimension-switching task (P = .11, see moderatorsonexecutiveperformance.