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Visual target processing in high- and low-performing older subjects indexed by P3 component

Abstract

Aim: To explore the possible changes in the parameters of the P3 event-related potential (ERP) component among groups of young and older healthy subjects characterized as either high- or low-performers in a visual attention task. Methods: Both conventional and single-trial analyses of the visual P3 component were performed on each group of subjects. Results: P3 component significantly increased in latency as a function of age. The high-performing older subjects showed the posterior predominance of P3, as in young subjects. However, the low-performing older subjects showed a significant P3 amplitude reduction at posterior locations and topographically more widespread activity. Furthermore, single-trial analysis showed that low-performing older subjects presented higher intertrial variability in P3 latency, few trials with P3 generation, and a reduced P3 amplitude in these trials in whom P3 was generated. Conclusion: These data suggest a specific decline in visual target processing in the low-performing older subjects, which would imply a reduction in these attentional brain resources that are allocated to correctly select the relevant stimuli. The implications of this finding for the actual compensation versus dedifferentiation debate in normal aging are discussed

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Visual target processing in high- and low-performing older subjects indexed by P3 component

Author: Lorenzo López, Laura; Amenedo Losada, María Elena; Pazo Álvarez, Paula; Cadaveira Mahía, Fernando
Publisher: Elsevier
Year: 2007
DOI: 10.1016/j.neucli.2007.01.008
Source: https://minerva.usc.es/bitstreams/a2d1fbd8-7b82-40c0-a377-d28dbeb2c57c/download
VISUAL TARGET PROCESSING IN HIGH- AND LOW PERFORMING
OLDER SUBJECTS INDEXED BY P3 COMPONENT
LE P3 EN TANT QU’INDEX DU NIVEAU DE PERFORMANCE DE
SUJETS ÂGÉS IMPLIQUÉS DANS UNE TÂCHE VISUELLE
Au ho s: L. Lo enzo-López∗, E. Amenedo, P. Pazo-Ál a ez, F. Cada ei a
This is he pee e iewed e sion o he ollowing a icle: Lo enzo-López, L., Amenedo, E., Pazo-
Ál a ez, P., Cada ei a, F. (2007). Visual a ge p ocessing in high- and low-pe o ming olde
subjec s indexed by P3 componen . Neu ophysiologie Clinique / Clinical Neu ophysiology, 37,
53-61. doi: 10.1016/j.neucli.2007.01.008
This a icle may be used o non-comme cial pu poses in acco dance wi h Else ie , In e na ional
Fede a ion o Clinical Neu ophysiology, I alian Clinical Neu ophysiology Socie y, Japanese
Socie y o Clinical Neu ophysiology, B azilian Socie y o Clinical Neu ophysiology e ms and
condi ions o use o sel -a chi ed e sions.
Pos -p in ( inal d a pos - e e eeing)
2
Visual a ge p ocessing in high- and low-pe o ming
olde subjec s indexed by P3 componen
Le P3 en an qu’index du ni eau de pe o mance de
suje s âgés impliqués dans une âche isuelle
Au ho s:L. Lo enzo-López∗, E. Amenedo, P. Pazo-Ál a ez, F. Cada ei a
Depa men o Clinical Psychology and Psychobiology, Facul y o Psychology, Uni e si y o
San iago de Compos ela, Galicia, Spain
*Co esponding au ho : lau a[email p o ec ed] (L. Lo enzo-López).
Pos -p in ( inal d a pos - e e eeing)
3
Abs ac
Aim. — To explo e he possible changes in he pa ame e s o he P3 e en - ela ed po en ial (ERP)
componen among g oups o young and olde heal hy subjec s cha ac e ized as ei he high- o
low-pe o me s in a isual a en ion ask.
Me hods. — Bo h con en ional and single- ial analyses o he isual P3 componen we e
pe o med on each g oup o subjec s.
Resul s. — P3 componen signi ican ly inc eased in la ency as a unc ion o age. The high
pe o ming olde subjec s showed he pos e io p edominance o P3, as in young subjec s.
Howe e , he low-pe o ming olde subjec s showed a signi ican P3 ampli ude educ ion a
pos e io loca ions and opog aphically mo e widesp ead ac i i y. Fu he mo e, single- ial
analysis showed ha low-pe o ming olde subjec s p esen ed highe in e ial a iabili y in P3
la ency, ew ials wi h P3 gene a ion, and a educed P3 ampli ude in hese ials in whom P3 was
gene a ed.
Conclusion. — These da a sugges a speci ic decline in isual a ge p ocessing in he low
pe o ming olde subjec s, which would imply a educ ion in hese a en ional b ain esou ces ha
a e alloca ed o co ec ly selec he ele an s imuli. The implica ions o his inding o he ac ual
compensa ion e sus dedi e en ia ion deba e in no mal aging a e discussed.
Résumé
Bu . — Compa e les pa amà es du composan P3 des po en iels é oqués dans un g oupe de suje s
jeunes en bonne san é e dans un g oupe de suje s âgés classi iés en onc ion de leu ni eau
d’exécu ion d’une âche d’a en ion isuelle (meilleu s e moins bons exécu eu s).
Mé hodes. — Des analyses con en ionnelles e des analyses « en sweep unique » du composan
P3 on é é éalisées dans chaque g oupe de suje s.
Résul a s. — Le emps de la ence du composan P3 augmen e de ac¸on signi ica i e a ec l’âge.
Chez les suje s âgés meilleu s exécu eu s le P3 p édominai au ni eau des égions pos é ieu es,
comme chez les suje s jeunes. Pa con e, chez les suje s âgés moins bons exécu eu s, le P3 é ai
signi ica i emen moins ample en pos é ieu e plus di usémen épa i su le scalp. Les analyses
« en sweep unique » on mon é que ces de nie s p ésen aien une plus g ande a iabili é in e essai
en ce qui conce ne le emps de la ence de P3, moins de es s où le P3 é ai p ésen , ainsi qu’une
éduc ion de l’ampli ude de P3 dans les es s où il é ai p ésen .
Conclusion. — Ces données suggè en l’exis ence d’un dé ici du ai emen isuel des s imuli
chez les suje s âgés moins bons exécu eu s qui pou ai consis e en une éduc ion des essou ces
Pos -p in ( inal d a pos - e e eeing)
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cé éb ales a en ionnelles mobilisées pou sélec ionne co ec emen le s imulus app op ié. Nous
discu ons les implica ions de ces ésul a s dans le d´eba conce nan la edis ibu ion des ai es
co icales ac i es chez les suje s âgés (hypo hèses de compensa ion e sus dédi é en ia ion).
Pos -p in ( inal d a pos - e e eeing)
5
In oduc ion
The P3 componen o e en - ela ed po en ials (ERPs) has demons a ed conside able u ili y in he
s udy o cogni i e li e-span changes, since i has been associa ed wi h basic in o ma ion-
p ocessing mechanisms including a en ion and memo y [33]. P3 is a la ge posi i e-going
wa e o m wi h a pos e io -pa ie al maximum ampli ude and a peak la ency o abou 300—400
ms in young subjec s, which has been ob ained in he audi o y, isual o soma ic modali y ( o a
ecen e iew, see [19]). The isual P3 was shown o be signi ican ly la ge in ampli ude and
longe in la ency han he audi o y P3 [22,32]. In he ERP li e a u e, P3 la ency has been
conside ed an indica o o he speed o cogni i e p ocessing associa ed wi h he selec ion o
ele an s imuli; i is gene ally un ela ed o esponse selec ion p ocesses and independen o
beha io al measu es [26,30]. P3 ampli ude has been conside ed as an index o he alloca ion o
a en ional b ain esou ces o he olun a y selec ion o ele an s imuli ( o a e iew, see [23]).
The esul s o se e al ERP aging s udies employing audi o y o isual pa adigms demons a ed
he exis ence o age- ela ed changes in he la ency, ampli ude, and scalp dis ibu ion o his
componen . Speci ically, he e is gene al consensus ha he peak la ency o P3 p og essi ely
inc eases wi h age [1,20,25,31,32,34,39,40]. Howe e , esul s on P3 ampli ude changes wi h age
a e less consis en , especially o isual s imuli, since ampli udes we e ound o be una ec ed by
age in some s udies [32], bu educed only a some elec ode loca ions in o he s [31,34]. O he
common inding in he li e a u e is an age- ela ed opog aphic al e a ion in he scalp dis ibu ion
o P3, which becomes mo e an e io ly dis ibu ed and, he eby, mo e di used o equipo en ial
ac oss he scalp wi h inc easing age [1,10—12,15,17,18,32,40]. These age- ela ed opog aphical
changes ha e been in e p e ed as e lec ing a en ional al e a ions in olde subjec s, who would
con inue o u ilize on al p ocesses o s imuli ha ha e al eady been well-ca ego ized [1,10],
(see [16] o a ecen e iew). In pa allel wi h hese age- ela ed changes in P3 scalp dis ibu ion,
unc ional neu oimaging s udies o aging ha e shown a pa adoxical inc ease in he b ain
ac i a ion o olde subjec s du ing he execu ion o memo y asks, pa icula ly in p e on al a eas
[6,28,35]. I has been sugges ed ha his age- ela ed ec ui men o a ypical b ain pa hways migh
e lec a possible compensa o y esponse ( o e iews, see [3—5]). In keeping wi h his iew, he
‘compensa ion’ hypo hesis sugges s ha , in o de o each an adequa e le el o beha io al
pe o mance in a speci ic ask, high pe o ming olde subjec s would ec ui di e en and wide
a eas o he b ain, which a e no ac i a ed by younge subjec s ( o e iews, see [5,16,36]).
Al e na i ely, i has been sugges ed ha his age- ela ed inc ease in on al ac i a ion could e lec
an ine icien neu al dis ibu ion o ask- ele an co ical ne wo ks in olde subjec s, which was
e e ed o as he ‘dedi e en ia ion’ hypo hesis (see [3—5,28,36] o e iews).

Pos -p in ( inal d a pos - e e eeing)
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In ou opinion, a ui ul way o shed new ligh on his deba e would be o di e en ia e be ween
pe o mance le els in aging s udies. The e o e, he aim o his s udy was o explo e whe he he
P3 la ency, ampli ude, and scalp dis ibu ion di e in young and olde subjec s cha ac e ized as
ei he high- o low-pe o me s in a isual a en ion ask. Since he ypical oddball ask is ela i ely
easy, and pe o mance in olde subjec s is usually almos pe ec , we used a mo e demanding ask.
We ied o de e mine whe he possible P3 di e ences be ween bo h subg oups o olde subjec s
should be conside ed compensa o y o ine icien . Indeed, i di e ences a e due o a
compensa o y mechanism, highpe o ming olde subjec s should be expec ed o p esen a mo e
widesp ead scalp dis ibu ion o P3 han young subjec s. Al e na i ely, i he di e ences a e due
o a de ici o an ine icien neu al ac i a ion, he scalp dis ibu ion changes should be obse ed
in low-pe o ming olde subjec s.
Because he p e iously desc ibed age- ela ed P3 ampli ude educ ions may ac ually be due o: (a)
he exis ence o mo e in e ial a iabili y in P3 la ency (i.e. la ency ji e e ec ), (b) educed P3
ampli udes in all ials, o (c) absence o P3 gene a ion in some ials [26], we used a single- ial
me hod o desc ibe P3 luc ua ions in addi ion o he con en ional ERP a e aging.
Finally, i should be no ed ha , whe eas in mos o p e ious s udies he cogni i e unc ioning o
olde subjec s was de ined by hei pe o mance on s anda dized neu opsychological es s [7], in
ou s udy he olde subjec s we e cha ac e ized as ei he high- o low-pe o me s acco ding o
hei ac ual beha io al pe o mance in he isual a en ion ask. This allows us compa ing hese
elec ophysiological esponses ha a e ela ed o di e en ac ual pe o mance le els among
g oups in he same ask.
Ma e ials and me hods
Subjec s
Ten young (7 emales, age ange: 22—38, mean: 29.4±6.3 yea s), and en olde subjec s (5
emales, age ange: 58—67, mean: 62.2±3.2 yea s) we e es ed. All we e heal hy well unc ioning
subjec s and had no his o y o neu ological o psychia ic diseases. All subjec s had no mal o
co ec ed o-no mal ision. Olde subjec s pe o med he Spanish e sion (MEC-35) [27] o he
Mini-Men al S a e Exam (MMSE) [13] and had no mal sco es (> 28). In o med consen was
ob ained om all subjec s.
The olde subjec s we e assigned o wo g oups on he basis o hei beha io al pe o mance in
he isual a en ion ask ha was ca ied ou du ing he eco ding o P3: a g oup o olde subjec s
who pe o med as well as he young subjec s (high-pe o ming, N = 5), and a g oup o olde
subjec s who pe o med a a signi ican ly lowe le el compa ed o he young subjec s (low-
Pos -p in ( inal d a pos - e e eeing)
7
pe o ming, N = 5). Reac ion imes (RTs) and pe o mance le els con i med ha he olde
subjec s assigned o he low-pe o ming g oup, pe o med signi ican ly wo se han young and
high-pe o ming olde subjec s (see esul sec ion). Age and gende dis ibu ions we e simila in
bo h olde g oups (see Table 1).
S imuli and p ocedu e
Subjec s sa in a com o able a mchai in an elec ically shielded and sound-a enua ed oom a
61 cm iewing dis ance om a compu e moni o . All s imuli we e c ea ed, p esen ed, and
con olled using he P esen a ion so wa e applica ion (Neu obeha io al Sys ems, Inc., e sion
0.76). A ixa ion c oss was p esen ed con inuously a he cen e o he moni o . The s imuli
consis ed o nine possible digi s (1, 2, 3, 4, 5, 6, 7, 8 o 9) in h ee di e en colo s ( ed, g een o
blue) sub ending 1.04◦ ×0.66◦ o isual angle, which we e equip obably p esen ed o 40 ms o e
he cen al ixa ion c oss. Subjec s we e equi ed o p ess a mouse bu on as quickly as possible
in esponse o digi s lowe han i e o any colo . Thus, digi s 1, 2, 3 and 4 o any colo we e he
a ge s imuli.
Ho izon al sinusoidal g a ings di e ing in mo ion di ec ion (4.13◦ isual angle, 20% con as ,
speed 1.95 deg/s, spa ial equency 0.7 cycles/deg) we e also p esen ed bila e ally a 10.7◦ o he
le and o he igh om he ixa ion c oss o 133 ms. These g a ings we e p esen ed in sequences
o epe i i e upwa d-d i ing g a ings (s anda d mo ion, p = 0.8), which we e occasionally
eplaced by downwa d d i ing g a ings (de ian mo ion, p = 0.2) and we e ollowed by a blank-
sc een ISI o 665 ms. Subjec s we e p esen ed wi h a block o 770 ials, om which 500
co esponded o una ended g a ings and 270 o a ended digi s. All s imuli we e p esen ed wi h a
s imulus onse asynch ony (SOA) o 798 ms. Subjec s we e equi ed o ix hei gaze on he
cen al c oss and o pay a en ion o he digi s, while igno ing he pe iphe al g a ings. In a ecen
s udy, we epo ed he e ec s o no mal aging on he p ea en i e p ocessing o hese una ended
pe iphe al g a ings [29] and he e we only epo he esul s on he cen al ask.
ERP eco dings
Con inuous elec oencephalog am (EEG) was eco ded (bandpass 0.05—100 Hz, 500
Hz/channel) wi h a Neu oScan sys em om 20 ac i e elec odes (Fp1, Fp2, F3, Fz, F4, F7, F8,
C3, Cz, C4, P3, Pz, P4, T3, T4, T5, T6, O1, O2, Oz), e e ed o he nose ip and g ounded wi h
an elec ode a nasion. Ve ical and ho izon al eye mo emen s we e eco ded bipola ly wi h
addi ional elec odes placed abo e and below he le eye and a he ou e can hi o bo h eyes,
espec i ely. Elec ode impedance was kep below 10 K_.
Pos -p in ( inal d a pos - e e eeing)
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Da a analysis
Beha io al da a analysis RTs we e au oma ically on-line eco ded o all subjec s, and he
pe o mance le el was calcula ed as he pe cen age o co ec esponses o a ge digi s in he
cen al isual ask. Only RT alues associa ed wi h co ec esponses we e conside ed o da a
analysis. Mean RTs and pe cen ages o co ec esponses we e compa ed ac oss g oups using
one-way analysis o a iance (ANOVA) wi h G oup (young, high-pe o ming olde , low-
pe o ming olde ) as he be ween subjec s ac o .
ERP da a analysis
Two ypes o analysis we e pe o med on ERP da a: con en ional analysis o ampli ude, la ency
and scalp dis ibu ion, and single- ial analysis.
Con en ional a e aging
The EEG was digi ally il e ed o -line wi h a 0.1—30 Hz bandpass il e , and epoched in o
pe iods o 1000 ms (100 ms p e a ge and 900 ms pos - a ge ). Epochs exceeding± 100µV and
hose con aining ho izon al o e ical eye mo emen s, o inco ec esponses we e excluded om
analysis. The EEG was a e aged o he a ge digi s in each g oup o subjec s, sepa a ely. The
P3 componen was hen measu ed as he maximum posi i e ol age peak be ween 300 and 600
ms pos s imulus ela i e o he 100 ms baseline in each g oup o subjec s. These ampli ude alues
we e subjec ed o mixed ANOVA wi h G oup (young, high-pe o ming olde , low-pe o ming
olde ) as he be ween-subjec s ac o , and Localiza ion (an e io , pos e io ), and Elec ode
(an e io : Cz, Fz, F3, F4, Fp1, Fp2; pos e io : Pz, Oz, P3, P4, O1, O2) as he wi hin-subjec
ac o s. The P3 la ency alues we e de e mined wi h espec o he la ges posi i e ol age a Pz
elec ode and compa ed ac oss g oups using one-way ANOVA wi h G oup (young, high-
pe o ming olde , low-pe o ming olde ) as he be ween-subjec s ac o . No e ha , in his s udy,
we explo ed he age- ela ed di e ences in P3 pa ame e s along an an e io -pos e io axis, so da a
on speci ic elec odes a e no p esen ed. An alpha le el o 0.05 was used o all s a is ical es s.
Deg ees o eedom we e co ec ed by he conse a i e G eenhouse—Geisse es ima e when
app op ia e. Pos hoc compa isons we e pe o med using he Bon e oni adjus men o mul iple
compa isons.
Finally, in o de o examine he scalp dis ibu ion o P3 and o explo e in mo e de ail he possible
changes in he scalp dis ibu ion o P3 ampli ude among g oups, ol age maps we e compu ed
wi h he EEGLAB p og am [8], which plo s opog aphic maps o EEG ields as a 2D ci cula
iew using coin e pola ion on a ine Ca esian g id.
Single- ial analysis
Pos -p in ( inal d a pos - e e eeing)
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In o de o isualize and desc ibe mo e accu a ely he ial- o- ial a iabili y in he ampli ude and
la ency o P3 componen du ing he ask, EEG epochs o a ge digi s associa ed wi h co ec
esponses we e subjec ed o single- ial analysis using he EEGLAB so wa e [8] a Fz and Pz
elec odes in each subjec . In a i s s ep, EEG Neu oscan da a epoch iles including only co ec
esponses we e impo ed ia he EEGLAB oolbox unde MATLAB en i onmen . The speci ic
channels o in e es (Fz and Pz) we e hen selec ed. The ea e , he EEGLAB menu allowed us o
so da a ials acco ding o hei occu ence in he expe imen and, inally, o c ea e ERP-image
plo s. The compu ed ERP-images consis ed o wo-dimensional colo ed ec angula
ep esen a ions o ial da a, in which each ho izon al line ep esen s ac i i y occu ing in each
single expe imen al ial. In hese images he ac i i y alues a e colo -coded in le - o- igh
s aigh lines, wi h he changing colo alue indica ing po en ial a ia ions a each ime poin in
he ial. Inspec ing he adjacen single ials allowed us o explo e he ial-by- ial P3
consis ency, making possible o de e mine whe he a P3 esponse was p esen in each indi idual
ial, and o explo e i s momen - o-momen luc ua ions in each g oup o subjec s. Resul s o his
single- ial analysis we e compa ed wi h hose o he con en ional a e aging.
Resul s
Beha io al da a
RTs and pe cen ages o co ec esponses a e summa ized in Table 1. The e was a signi ican
main e ec o G oup on mean RT (F2,17 = 5.67, P < 0.013). Pai wise compa isons (Bon e oni)
e ealed ha he mean RT o low-pe o ming olde subjec s was signi ican ly longe han ha o
young subjec s (P < 0.011), wi h no signi ican di e ences be ween he mean RT o high-
pe o ming olde and young subjec s (P = 1), and be ween bo h low- and high-pe o ming olde
subjec s (P = 0.138). The e was a signi ican main e ec o G oup on pe cen age o co ec
esponses (F2,17 = 7.74, P < 0.004). Pai wise compa isons e ealed ha pe o mance accu acy
was signi ican ly lowe o he low-pe o ming olde subjec s han o he o he wo g oups
(young: P < 0.005; high-pe o ming olde : P < 0.017), wi h no signi ican di e ences be ween
he pe o mance le els o he la e wo g oups (P = 1) (see Table 1).
ERP da a
Figu e 1 shows ERPs o a ge s o young, high-, and lowpe o ming olde subjec s a an e io
and pos e io scalp loca ions. As can be seen, all h ee g oups showed a clea ly iden i iable P3
componen .
P3 la ency
Pos -p in ( inal d a pos - e e eeing)
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