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Neu obiology o Lea ning and Memo y
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Spa io empo al pa e n o b ain elec ical ac i i y ela ed o immedia e and
delayed episodic memo y e ie al
Miguel Ángel Ri as-Fe nández
⁎
, San iago Galdo-Ál a ez, Mon se a Zu ón, Fe nando Díaz,
Mónica Lindín
Labo a o io de Neu ociencia Cogni i a, Depa amen o de Psicoloxía Clínica e Psicobioloxía, Uni e sidade de San iago de Compos ela, Galicia, Spain
ARTICLE INFO
Keywo ds:
Episodic memo y
Recogni ion memo y
E en - ela ed b ain po en ials (ERPs)
Old/new ERP e ec s
eLORETA
ABSTRACT
In he p esen s udy we used he e en - ela ed b ain po en ials (ERP) echnique and eLORETA (exac low-
esolu ion elec omagne ic omog aphy) me hod in o de o cha ac e ize and compa e he pe o mance and he
spa io empo al pa e n o he b ain elec ical ac i i y ela ed o he immedia e episodic e ie al o in o ma ion
(wo ds) ha is being lea ned ela i e o delayed episodic e ie al wen y-minu es la e . Fo his pu pose, 16
young pa icipan s ca ied ou an old/new wo d ecogni ion ask wi h sou ce memo y (wo d colou ). The ask
included an immedia e memo y phase (wi h h ee s udy- es blocks) ollowed (20 min la e ) by a delayed memo y
phase wi h one es block. The beha iou al da a showed p og essi e lea ning and consolida ion o he in-
o ma ion (old wo ds) du ing he immedia e memo y phase. The ERP da a o co ec ly iden i ied old wo ds o
which he colou was subsequen ly ecollec ed (H/H) compa ed o he co ec ly ejec ed new wo ds (CR)
showed: (1) a signi ican mo e posi i e-going po en ial in he 500–675 ms pos -s imulus in e al (pa ie al old/
new e ec , ela ed o ecollec ion), and (2) a mo e nega i e-going po en ial in he 950–1850 ms in e al (LPN
e ec , ela ed o e ie al and pos - e ie al p ocesses). The eLORETA da a also e ealed ha he success ul
ecogni ion o old wo ds (and p obably e ie al o hei colou ) was accompanied by ac i a ion o (1) le
medial empo al (pa ahippocampal gy us) and pa ie al egions in ol ed in he ecollec ion in bo h memo y
phases, and (2) p e on al egions and he supe io empo al gy us (in he immedia e and delayed memo y phases
espec i ely) in ol ed in moni o ing, e alua ing and main aining he e ie al p oduc s. These indings indica e
ha episodic memo y e ie al depends on a ne wo k in ol ing medial empo al lobe and on al, pa ie al and
empo al neoco ical s uc u es. Tha ne wo k was in ol ed in immedia e and delayed memo y e ie al and
du ing he cou se o memo y consolida ion, wi h g ea e ac i a ion o some nodes (mobiliza ion o mo e p o-
cessing esou ces) o he delayed espec o he immedia e e ie al condi ion.
1. In oduc ion
Episodic memo y (EM), de ined as a neu ocogni i e sys em ha
enables us o consciously ecall pas expe iences (Tul ing, 2002), has
ecei ed inc easing a en ion in cogni i e, neu opsychological, psy-
chophysiological and neu oimaging s udies in he pas decade (Rugg &
Vilbe g, 2013; Rugg & Yonelinas, 2003; Yonelinas, 2002). EM s udies
ha e p o ided insigh s in o how in o ma ion is acqui ed, o ganized and
e ie ed in long- e m memo y, by e alua ing (1) encoding p ocesses
(o s o age o new in o ma ion in ol ing changes in he s eng h and/o
numbe o synap ic connec ions wi hin he ne ous sys em, known as
memo y aces), (2) consolida ion (s abiliza ion o memo y aces
ollowing he ini ial encoding), and (3) e ie al (i.e. ecall o p e-
iously s o ed in o ma ion) (Squi e, Wix ed, & Cla k, 2007).
The S anda d Consolida ion Theo y (SCT) (Squi e & Al a ez, 1995)
p oposed ha he encoding, consolida ion and e ie al o memo ies
a e always dependen on di ec connec ions be ween he hippocampal
o ma ion and neoco ical egions; howe e , once consolida ion s abi-
lizes he memo y aces, he e ie al o episodic memo ies is suppo ed
by ac i a ion o neoco ical egions ha a e mo e independen o hip-
pocampal o ma ion, i.e. connec ions be ween hippocampal o ma ion
and neoco ical egions become less c i ical o e ie ing he s o ed
in o ma ion. Howe e , his iew was la e ques ioned, and i is be-
coming mo e widely accep ed ha mos memo ies ne e become
h ps://doi.o g/10.1016/j.nlm.2020.107309
Recei ed 6 May 2020; Recei ed in e ised o m 30 July 2020; Accep ed 26 Augus 2020
⁎
Co esponding au ho a : Labo a o io de Neu ociencia Cogni i a, Depa amen o de Psicoloxía Clínica e Psicobioloxía, Uni e sidade de San iago de Compos ela,
Campus Vida, Calle Xosé Ma ía Suá ez Núñez, s/n, 15782 San iago de Compos ela, Galicia, Spain.
E-mail add esses: [email p o ec ed] (M.Á. Ri as-Fe nández), [email p o ec ed] (S. Galdo-Ál a ez), [email p o ec ed] (M. Zu ón),
[email p o ec ed] (F. Díaz), [email p o ec ed] (M. Lindín).
Neu obiology o Lea ning and Memo y 175 (2020) 107309
A ailable online 02 Sep embe 2020
1074-7427/ © 2020 The Au ho s. Published by Else ie Inc. This is an open access a icle unde he CC BY-NC-ND license
(h p://c ea i ecommons.o g/licenses/by-nc-nd/4.0/).
T
independen o hippocampal o ma ion (see Skelin, Kilianski, &
McNaugh on, 2019). The Mul iple T ace Theo y (MTT) (Nadel &
Mosco i ch, 1997) and he la e T ace T ans o ma ion Theo y (TTT)
(Seke es, Winocu , & Mosco i ch, 2018) pos ula e ha he epea ed
ac i a ion o memo ies c ea es new memo y aces and ha he e-
ie al o episodic memo ies ( ecen o emo e) will always depend on
ac i a ion o hippocampal o ma ion.
The h ee a o emen ioned heo ies we e p oposed in ela ion o he
sys ems consolida ion. Two essen ial componen s o he consolida ion
p ocess we e p oposed (Dudai, 2004; Dudai, Ka ni, & Bo n, 2015;
Seke es e al., 2018; Winocu & Mosco i ch, 2011): (1) a cellula /sy-
nap ic componen (synap ic consolida ion, which is achie ed wi hin
minu es o hou s), ela ed o ea ly and apid changes a local synap ic
connec ions and cellula nodes in local neu onal assemblies. I is
media ed by in acellula molecula mechanisms, and e e s o he pos -
encoding ans o ma ion o in o ma ion in o a long- e m o m; and (2) a
sys ems componen (sys ems consolida ion, wi h a ia ion in i s du a ion,
om minu es o decades), which is associa ed wi h he pos -encoding
ime-dependen eo ganiza ion o long- e m memo y ep esen a ions
o e dis ibu ed (medial empo al-neoco ical) ne wo ks. Bo h we e
conside ed as a pa o a con inuous and dynamic p ocess, so ha sy-
nap ic consolida ion could be deemed as sub ou ines in o sys ems con-
solida ion p ocess (Dudai e al., 2015).
Neu oimaging and beha iou al s udies in humans ha e demon-
s a ed he impo ance o he medial empo al lobe (MTL) in episodic
memo y (Eichenbaum, Yonelinas, & Rangana h, 2007; Nadel &
Mosco i ch, 1997; Squi e e al., 2007; Tul ing, 2002). EM p ocesses
imply he con inuous exchange o in o ma ion in a ne wo k o b ain
a eas cen e ed on he medial empo al lobe (MTL) and neoco ical e-
gions (Ba aglia, Benchenane, Si o a, Penna z, & Wiene , 2011; Ison,
Quian Qui oga, & F ied, 2015). Howe e , as a as we a e awa e, no
p e ious s udies ha e used a b ain ac i i y eco ding echnique wi h
high empo al esolu ion o disen angle he ole o he MTL and neo-
co ical egions in he success ul episodic e ie al a di e en imes
ac oss memo y consolida ion.
Wi h he aim o add essing his lack o in o ma ion, in he p esen
s udy we applied exac low esolu ion omog aphy (eLORETA) so wa e
o e en - ela ed b ain po en ial (ERP) da a, ob ained du ing wo di -
e en condi ions o success ul EM e ie al: immedia e and delayed
( wen y minu es la e ).
The ERP echnique, which has a high empo al esolu ion, has been
widely used in psychophysiological s udies o e alua e he ime cou se
o b ain elec ical ac i i y du ing di e en EM p ocesses. Recogni ion
memo y is commonly e alua ed using old/new ecogni ion asks, in
which pa icipan s mus classi y i ems as p e iously p esen ed (old
s imuli) o no p esen ed (new s imuli, co ec ejec ion). The di e ence
be ween he ERPs elici ed by co ec ly ejec ed new i ems (CR) and he
ERPs elici ed by co ec ly ecognized old i ems (Hi ) e lec s EM e-
ie al phenomena (F iedman, 2013). Speci ically, be ween 300 and
500 ms pos -s imulus, a nega i e ERP componen is obse ed a on al
and cen al scalp si es, wi h a smalle nega i e ol age in esponse o
old s imuli han in esponse o new s imuli: his di e ence is commonly
known as he mid- on al old/new e ec o on al N400 e ec -FN400-
(Cu an, 2000). Mos e idence sugges s ha his e ec is a co ela e o
amilia i y, as a ia ions in ampli ude a e obse ed depending on he
amilia i y con idence (Wood u , Hayama, & Rugg, 2006; Yu & Rugg,
2010). Familia i y-based ecogni ion is conside ed a as -ac ing, ela-
i ely au oma ic p ocess ha does no p o ide quali a i e in o ma ion
abou he s udy episode (Rugg & Cu an, 2007).
A pa ie al posi i e componen is iden i ied be ween 500 and 800 ms
pos -s imulus and wi h la ge ol age in esponse o old s imuli han in
esponse o new s imuli: his di e ence, which is commonly known as
he pa ie al old/new e ec (Wilding, F ase , & He on, 2005), is e-
quen ly la ge a le scalp si es when he s imuli a e wo ds. This
componen has been associa ed wi h ecollec ion, which is conside ed a
slowe and mo e e o ul p ocess han amilia i y-based ecogni ion
and which p o ides in o ma ion abou quali a i e aspec s o a p io
e en , including i s con ex (Rugg & Vilbe g, 2013). The pa ie al old/
new e ec shows ampli ude modula ions in ecogni ion memo y asks
ha demand conscious ecall o p e iously s udied con ex ual de ails
(sou ce o con ex memo y ask). In pa icula , his e ec has been
ound o ha e a la ge ampli ude in episodic ela i e o seman ic
(knowing ac s) judgmen s (Macleod & Donaldson, 2017), in co ec
ela i e o inco ec sou ce memo y judgmen s (Macleod & Donaldson,
2017; Wilding & Rugg, 1996), and also when e ie al o a la ge amoun
o in o ma ion is equi ed (Vilbe g, Moosa i, & Rugg, 2006). Howe e ,
some e idence sugges s ha a ia ions in he magni ude o he pa ie al
old/new e ec migh no always p edic a ia ions in episodic e-
collec ion be ween pa icipan s (Macleod & Donaldson, 2017).
Ano he wo la e onse old/new ERP e ec s ha e been iden i ied
om 600 ms onwa ds: (1) he igh on al old/new e ec (RFE), whe eby
old s imuli elici a la ge posi i e ol age han new s imulus o e igh
on al scalp si es. E idence sugges s ha he RFE indica es moni o ing
and e alua ion p ocesses ha ac on he e ie al p oduc s (C use &
Wilding, 2009); and (2) he la e pos e io nega i i y (LPN) e ec , which
shows he opposi e pa e n o e pa ie o-occipi al scalp si es, i.e. old
s imuli elici a mo e nega i e-going ol age han new s imuli. E idence
sugges s ha LPN may e lec mnemonic p ocesses in ol ed in he e-
cons uc ion o a p e ious s udy episode when some i em a ibu e is
no eadily e ie ed o when he in o ma ion e ie ed needs addi-
ional e alua ion, and/o non-mnemonic p ocesses o moni o ing ha
ac in highly demanding asks (Somme , Vi a, & De Pascalis, 2018; o a
e iew see Mecklinge , Rosbu g, & Johansson, 2016).
In he p esen ERP s udy, we e alua ed he old/new ERP e ec s in
an old/new wo d ecogni ion ask wi h sou ce memo y (i.e. he colou
o he old wo d) o cha ac e ize he spa io empo al pa e n o he b ain
elec ical ac i i y du ing he immedia e and he delayed EM e ie al.
Some p e ious s udies ha e e alua ed he old/new ERP e ec s in young
adul s, also using an old/new ecogni ion ask wi h wo ds, wi h di -
e en empo al in e als om he s udy ask o he ecogni ion es :
immedia ely (Wang, de Chas elaine, Min on, & Rugg, 2012), one
minu e (see expe imen one o Macleod & Donaldson, 2017), 39 min
(Wolk e al., 2006), one week (see expe imen wo o Macleod &
Donaldson, 2017) and one day (Wolk e al., 2006). Howe e , as a as
we a e awa e, only one s udy (Wolk e al., 2006) ha e e alua ed wi hin
he same expe imen he old/new ERP e ec s using di e en s udy- es
delay in e als: 39 min e sus one day. In he a o emen ioned s udy, he
esea che s did no obse e any di e ences in he ERP pa ame e s
(ob ained in esponse o co ec ly ecognized old o new wo ds) be-
ween bo h delay condi ions; mo eo e , al hough hey iden i ied he
mid- on al and pa ie al old/new e ec s in each delay condi ion, hey did
no e alua e he b ain a eas in ol ed in hese e ec s.
Al hough he spa ial esolu ion o ERPs is lowe han in he unc-
ional magne ic esonance imaging ( MRI) echnique, wo s udies ha e
p e iously e alua ed he spa io empo al pa e n o he b ain ac i i y
ela ed o he old/new e ec s (Alhaj, Massey, & McAllis e -Williams,
2006; Kim e al., 2009), by applying he LORETA b ain sou ce es i-
ma ion algo i hm (Pascual-Ma qui, Michel, & Lehmann, 1994, 2011) o
ERP da a. In bo h s udies, pa icipan s pe o med an old/new e-
cogni ion ask wi h sou ce memo y, in which wo ds we e used as s i-
muli and he gende o he oice ha spoke he wo ds as he sou ce o
emembe . These s udies demons a ed he in ol emen o mul iple
b ain a eas in he success ul immedia e e ie al, a a ound 600–700 ms
pos -s imulus, speci ically in he hippocampus, he igh in e io pa -
ie al lobe, and also some egions o he supe io empo al and on al
co ex. EM s udies using MRI, a echnique wi h a much lowe empo al
esolu ion han ERP, showed high consis ency in he same ac i a ed
b ain a eas iden i ied in he a o emen ioned s udies in which LORETA
was applied o ERP da a (Be gs öm e al., 2013; Eichenbaum e al.,
2007; Henson, Rugg, Shallice, Josephs, & Dolan, 1999; Rugg e al.,
2002; Scalici, Cal agi one, & Ca lesimo, 2017; Vilbe g & Rugg, 2008).
In summa y, e alua ion o old/new ERP e ec s allows us o assess
M.Á. Ri as-Fe nández, e al. Neu obiology o Lea ning and Memo y 175 (2020) 107309
2
changes in he b ain elec ical ac i i y ela ed o immedia e and de-
layed EM e ie al, as well as o delimi , wi h a good empo al e-
solu ion, he empo al anges (conside ing he la ency o hese e ec s)
wi hin which we can es ima e he ne wo k o di e en b ain a eas in-
ol ed. Mo eo e , we conside ed ha he neu al da a ob ained (wi h
good empo al esolu ion) migh shed some ligh on he ole o MTL and
neoco ical egions in di e en imes o memo y consolida ion and e-
ie al p ocesses.
In he p esen s udy, we used an old/new wo d ecogni ion ask
wi h sou ce memo y (wo d colou ) o compa e he pe o mance and he
spa io empo al pa e ns o b ain elec ical ac i i y du ing success ul EM
e ie al in an immedia e memo y phase (wi h h ee s udy- es blocks)
and in a delayed memo y phase (wi h a es p esen ed wen y minu es
la e ). P e ious s udies showed ha he p esen a ion o mul iple s udy-
es blocks (as in he immedia e memo y phase o he p esen s udy)
imp o ed he old/new disc imina ion abili y o young adul s when hey
had o ecognize symbols (De Chas elaine, F iedman, Cycowicz, &
Ho on, 2009) and wo ds (Jacoby, Jones, & Dolan, 1998). This im-
p o emen was e lec ed no only by an inc ease o he old/new dis-
c imina ion accu acy ac oss es epe i ions (De Chas elaine e al.,
2009; Jacoby e al., 1998) bu also by a educ ion in he eac ion imes
du ing he ecogni ion o old and new i ems (De Chas elaine e al.,
2009).
The speci ic aims o he s udy we e as ollows:
(1) To compa e pe o mance be ween he immedia e memo y phase and
he delayed memo y phase.
(2) To iden i y and e alua e he old/new ERP e ec s in each memo y
phase (immedia e and delayed) and o compa e hese be ween bo h
phases.
(3) To apply eLORETA o he in e als o he old/new ERP e ec
iden i ied in o de o de e mine:
a. Which b ain a eas a e mo e ac i a ed du ing he success ul EM
e ie al o old wo ds ela i e o he co ec iden i ica ion o new
wo ds, in each memo y phase (immedia e and delayed).
b. Which b ain a eas a e ac i a ed di e en ly be ween bo h
memo y phases, du ing he success ul e ie al o old wo ds and
du ing he co ec iden i ica ion o new wo ds.
c. The in ol emen o MTL and neoco ical egions (e.g. p e on al
co ex and pos e io pa ie al co ex) du ing he success ul e-
ie al o old wo ds, in each memo y phase.
In line wi h p e ious s udies ha e ealed an inc ease in he old/
new disc imina ion abili y in young adul s du ing he p esen a ion o
mul iple s udy- es blocks (De Chas elaine e al., 2009; Jacoby e al.,
1998), we expec ed o obse e a lea ning p ocess o he old wo ds
ac oss he h ee s udy/ es blocks o he immedia e memo y phase, de-
mons a ed beha iou ally by (1) a g adual imp o emen in he pe -
o mance ac oss he blocks, and (2) no di e ences be ween he hi d
block o he immedia e memo y phase and he es o he delayed memo y
phase, which would indica e ha ea ly consolida ion is main ained
du ing he 20-minu e delay in e al (du ing which pa icipan s had o
pe o m a isuospa ial wo king memo y ask: see Task in Me hod sec-
ion). On he o he hand, we expec ed o ind he ollowing in bo h
memo y phases: (1) old/new ERP e ec s, especially in he empo al
anges o he mid- on al old/new e ec ela ed o he amilia i y and he
pa ie al old/new e ec ela ed o he ecollec ion; and (2) g ea e ac i-
a ion o he MTL and neoco ical egions du ing he e ie al o old
wo ds ela i e o he co ec iden i ica ion o new wo ds.
2. Ma e ials and me hod
2.1. Pa icipan s
Six een uni e si y s uden s (8 women, 8 men) be ween 18 and
25 yea s old (mean age: 21 yea s old, SD: 2.1) pa icipa ed olun a ily
in he s udy. All pa icipan s had no mal audi ion and no mal o co -
ec ed o no mal ision, and none had any his o y o neu ological o
psychia ic diso de s. All pa icipan s we e igh -handed, as e alua ed
by he Edinbu gh Handedness In en o y (Old ield, 1971), and all o
hem ga e hei w i en in o med consen p io o pa icipa ion in he
s udy. The esea ch p ojec was app o ed by he Galician Clinical Re-
sea ch E hics Commi ee (Xun a de Galicia, Spain) and was pe o med
in acco dance wi h he e hical s anda ds es ablished in he 1964 De-
cla a ion o Helsinki (Lynöe, Sandlund, Dahlq is , & Jacobsson, 1991).
2.2. Task and s imuli
2.2.1. Task
Du ing he elec oencephalog aphic (EEG) eco ding, pa icipan s
pe o med an old/new wo d ecogni ion ask wi h sou ce memo y
(wo d colou ) and o med by an immedia e memo y phase and a delayed
memo y phase (see Fig. 1). A p ac ice block wi h i e wo ds was p e-
sen ed be o e he ask, o ensu e ha pa icipan s had unde s ood and
Fig. 1. Task scheme.
M.Á. Ri as-Fe nández, e al. Neu obiology o Lea ning and Memo y 175 (2020) 107309
3
pe o med he ask co ec ly.
The immedia e memo y phase consis ed o h ee s udy- es blocks,
wi h an in e -block es in e al o 2–3 min. In he s udy ask, he same
lis o 40 wo ds (names o li ing beings and common objec s), p in ed
in ed o blue, we e andomly p esen ed ac oss blocks. Pa icipan s
we e ins uc ed o memo ize he wo d and he colou in which i was
p in ed and o simul aneously make a judgmen abou whe he he
wo ds ep esen ed li ing/non-li ing hings and o espond by p essing
as quickly and accu a ely as possible one o wo di e en bu ons on a
CEDRUS Model RB-834 de ice (le bu on: index inge ; igh bu on:
middle inge ). The es began immedia ely a e he s udy ask. Du ing
each es , 26 o 27 wo ds ha had been p esen ed in he s udy ask (old
wo ds) we e andomly in e spe sed wi h 26 o 27 new wo ds, bo h
p in ed in black (Block 1: 26 old/26 new; Block 2: 26 old/26 new; Block
3: 27 old/27 new. Thus, a o al o 79 new wo ds and 79 old wo ds ( he
40 old wo ds p esen ed in he s udy ask we e epea ed wice, excep
o one wo d) we e p esen ed in all h ee es s. Pa icipan s we e in-
s uc ed o decide whe he he wo d was old o new and o espond by
p essing (as quickly and accu a ely as possible) one o wo bu ons (le
bu on: index inge ; igh bu on: middle inge ), depending on he
ca ego y o he wo d: “old” i i had been p esen ed in he s udy ask o
“new” i i had no . I he wo d was co ec ly ecognized as old, pa i-
cipan s we e equi ed o espond 500 ms la e o he ques ion “was i
p in ed in blue?” o “was i p in ed in ed?”, by p essing he same
bu ons as be o e (yes/no).
A e inishing he hi d block o he immedia e memo y phase, pa -
icipan s pe o med a di e en ask ( isuospa ial wo king memo y ask,
las ing 20 min, wi h non- e bal isual s imuli). A e a sho es in-
e al, an unexpec ed delayed memo y es (delayed memo y phase) was
p esen ed. In his phase, he 40 old wo ds (memo ized du ing he s udy
ask o he h ee blocks o he immedia e memo y phase) we e andomly
in e spe sed wi h 40 new wo ds. All wo ds we e p in ed in black and
pa icipan s we e again ins uc ed o p ess one o wo di e en esponse
bu ons co esponding o old/new and, o co ec ly ecognized old
wo ds, o answe he ques ion abou he colou in which wo ds we e
p in ed in he s udy asks ( ed o blue). Response bu ons (yes/no)
du ing he immedia e and delayed memo y phases we e coun e balanced
among pa icipan s.
2.2.2. S imuli
A o al o 159 wo ds we e selec ed om wo Spanish wo d da a-
bases: APO –“Animal-Pe sona-Obje o”- (Fe é, Guasch, Moldo an, &
Sánchez-Casas, 2012) and EsPal (Duchon, Pe ea, Sebas ián-Gallés,
Ma í, & Ca ei as, 2013). The wo ds we e p esen ed in lowe case and
Chicago on (size 80: ed o blue o he s udy ask and black o he
es ) on a ligh g ey backg ound and we e displayed in he cen e o a
17-inch la moni o loca ed a a dis ance o one me e om he pa -
icipan . In he s udy ask, he du a ion o each s imuli was 2500 ms,
and a andom in e -s imulus in e al o be ween 800 and 1200 ms was
used. In he es , each s imulus las ed up o 2000 ms ( he wo d dis-
appea ed om he moni o sc een when he pa icipan pushed he
esponse bu on), and he du a ion o he in e -s imulus in e al was
be ween 800 and 1200 ms. In he s udy ask and he es , a black c oss
was p esen ed in he cen e o he moni o on a ligh g ey backg ound
du ing he in e -s imulus in e al, and he pa icipan s we e ins uc ed
o keep hei gaze ixed on he c oss.
The 159 wo ds (o which 80 e e ed o li ing beings and 79 o non-
li ing i ems) we e selec ed acco ding o he ollowing c i e ia: alence,
a ousal and amilia i y o he wo d in he con ex o Spanish speech,
deg ee o conc e ion, equency o use and leng h.
2.3. EEG eco ding
Pa icipan s we e sea ed on a com o able chai in an elec ically
shielded oom, wi h a enua ed le els o ligh and noise, and we e in-
s uc ed o mo e as li le as possible du ing he eco ding. EEG ac i i y
was eco ded wi h a B ain Vision Reco de de ice, ia 60 ac i e elec-
odes placed in an elas ic cap (Easycap, GmbH), acco ding o he
In e na ional 10–10 sys em. All elec odes we e e e enced o an elec-
ode a ached o he ip o he nose and an elec ode posi ioned a Fpz
se ed as a g ound. The ho izon al elec o-oculog am (HEOG) was e-
co ded ia wo elec odes placed a he ou e can hi o bo h eyes,
whe eas he e ical EOG (VEOG) was eco ded ia wo elec odes
placed sup a and in ao bi ally o he igh eye. The EEG was con-
inuously digi ized a a a e o 500 Hz (bandpass il e 0.01–100 Hz)
and elec ode impedances we e main ained below 10 kΩ.
Once he signal was s o ed, he EEG da a we e expo ed o Ma lab
(R2017a e sion) and p ocessed using EEGLAB (Delo me & Makeig,
2004) and ERPLAB (Lopez-Calde on & Luck, 2014). The signal was
passed h ough a digi al 0.1–30 Hz (12 dB/oc a e slope) bandpass
il e , and ocula a e ac s we e co ec ed o -line by Independen
Componen Analysis (ICA). In o de o s udy he b ain ac i i y ela ed
o es blocks o he immedia e and delayed memo y phases, he EEG was
hen segmen ed by ex ac ion o epochs om −200 o 2000 ms pos
s imuli, only o co ec ly ecognized old wo ds and wi h co ec colou
ecollec ion (Hi /Hi , H/H), and o co ec ly ejec ed new wo ds (CR).
All epochs we e co ec ed o he mean ol age o 200 ms p e-s imulus
eco ding pe iod, and EEG segmen s exceeding ± 100 µV we e au o-
ma ically ejec ed. EEG co esponding o old wo ds ha we e co ec ly
ecognized wi hou pos e io colou ecollec ion (Hi /Miss, H/M) we e
no analyzed in he p esen s udy because he numbe o epochs o he
a e ages in each phase (immedia e and delayed) was insu icien (< 20
epochs). The mean numbe o a e aged epochs (SD: s anda d de ia ion)
o each phase was as ollows: Immedia e memo y phase: 46.9 ( ± 9.4)
o H/H and 65.6 ( ± 11.2) o CR; Delayed memo y phase: 27.8 ( ± 5.2)
o H/H and 34.6 ( ± 4.2) o CR. EEG ela ed o each s udy block we e
no analyzed.
2.4. P ocedu e
2.4.1. Da a analysis
2.4.1.1. Beha iou al da a. Reac ion imes (RT, be ween he onse o he
wo d and p essing he key) and he pe cen age o esponses we e
eco ded in he ollowing expe imen al condi ions: H/H, H/M, CR,
e o s in he ecogni ion o old wo ds (as hey we e conside ed new
wo ds), alse ala ms (new wo ds we e conside ed old wo ds) and misses
( esponse omissions). In he p esen s udy we only e alua ed he
esponses: H/H, H/M and CR.
2.4.1.2. ERPs da a. The same ERP componen s we e iden i ied in he
g and-a e age ERP wa e o ms o he immedia e and delayed memo y
phases. All ERP wa e o ms included a posi i e ollowed by a nega i e
peak a abou 100 and 200 ms (P100 and N170 componen s)
espec i ely, bu only he ERP componen s iden i ied om 200 ms
onwa ds we e analyzed. The associa ed pa ame e s (ampli ude and
la ency) we e e alua ed in di e en empo al anges de e mined om
he g and-a e age ERP wa e o ms.
The ollowing ERP componen s we e e alua ed: a nega i e compo-
nen , wi h maximal ampli ude a on al scalp si es, in he 200–500 ms
pos -s imulus in e al (coinciding wi h he empo al ange desc ibed in
he li e a u e o he mid- on al old/new e ec o FN400 e ec ), and a
posi i e componen wi h maximal ampli ude a pa ie al scalp si es, in
he 400–900 ms pos -s imulus in e al (coinciding wi h he empo al
ange desc ibed in he li e a u e o he pa ie al old/new e ec ). Mean
ampli udes we e measu ed o bo h componen s conside ing an in e al
a ound he peak, which was es ima ed a he elec ode si es whe e he
ampli ude o each componen was la ges : a Fz o he on al nega i e
componen , and a Pz o he pa ie al posi i e componen . In he im-
media e memo y phase, he mean ampli ude o he on al nega i e
componen was measu ed in he 250–350 ms in e al (conside ing ±
50 ms a ound he peak), and he mean ampli ude o he pa ie al po-
si i e componen in he 500–650 ms in e al (conside ing ± 75 ms
M.Á. Ri as-Fe nández, e al. Neu obiology o Lea ning and Memo y 175 (2020) 107309
4
a ound he peak in he ERP wa e o ms o he old wo ds). Simila
measu emen s we e made in he delayed memo y phase, al hough wi h
sligh ly di e en empo al in e als compa ed o he immedia e memo y
phase due o sligh di e ences in he la ency o he peak ampli ude:
270–370 ms ( ± 50 ms a ound he peak) o he on al nega i e
componen and 525–675 ms ( ± 75 ms a ound he peak) o he pa ie al
posi i e componen . Mean ampli udes o bo h componen s we e e al-
ua ed a he ollowing elec ode clus e s (scalp egions o in e es -ROI-
o s a is ical analyses), p e iously employed in he li e a u e (Voss &
Fede meie , 2011): Mid on al (F1, Fz, F2, FC1, FCz, FC2, C1, Cz, C2),
mid pos e io (CP1, CPz, CP2, P1, Pz, P2, POz), le pos e io (TP7, CP5,
CP3, P7, P5, P3, PO7, PO3) and igh pos e io (TP8, CP6, CP4, P8, P6,
P4, PO8, PO4).
In addi ion, he 50% ac ional a ea la ency was also es ima ed o
bo h componen s. This in ol ed compu ing he a ea unde he ERP
wa e o m o e a gi en la ency ange and hen inding he ime poin
ha di ides he a ea in o a 50% ac ion (Luck, 2014). The la ency
ange o calcula ion o he a ea o each componen was es ablished
obse ing he g and-a e age ERP wa e o ms comp ising he comple e
du a ion o he componen (onse o end). F ac ional a ea la ency was
e alua ed o he on al nega i e componen and he pa ie al posi i e
componen a hose elec odes whe e hese componen s showed max-
imal ampli ude, ha is, Fz o he on al nega i e componen and Pz
o he posi i e pa ie al componen . In bo h memo y phases o he ask
(immedia e and delayed memo y phases), he la ency o he on al ne-
ga i e componen o bo h condi ions (H/H and CR) was es ima ed in
he 200–500 ms in e al. In addi ion, he la ency o he pa ie al posi i e
componen was es ima ed: (1) in he immedia e memo y phase, using
di e en empo al in e als o he H/H (400–850 ms) and CR
(400–900 ms) condi ions, and (2) in he delayed memo y phase, using
he 350–900 ms in e al o bo h condi ions (H/H and CR).
The LPN was iden i ied a pa ie o-occipi al loca ions, i.e. om
800 ms onwa ds in he immedia e memo y phase, and om 950 ms on-
wa ds in he delayed memo y phase. In o de o e alua e his componen
in bo h condi ions (H/H and CR), mean ampli udes we e also measu ed
a he ou ROIs a o emen ioned (mid on al, mid pos e io , le pos-
e io and igh pos e io ), in se en empo al windows (each o 150 ms)
be ween 950 and 2000 ms pos -s imuli, in he immedia e and delayed
memo y phases.
Vol age maps we e also ob ained o opog aphic analysis o he
on al nega i e componen , he pa ie al posi i e componen and he
LPN, in each phase (immedia e and delayed) and condi ion (H/H and
CR). The ol age maps we e calcula ed in he empo al anges whe e
he mean ampli udes o hese componen s we e iden i ied.
2.4.1.3. B ain sou ce localiza ion analysis. Exac low- esolu ion
elec omagne ic omog aphy (eLORETA) so wa e (publicly a ailable,
ee academic so wa e, a h p://www.uzh.ch/keyins /lo e a.h m) was
used o es ima e co ical sou ces o EEG ac i i y ( eco ded a 60 scalp
elec odes) in he in e als whe e he on al nega i e componen , he
pa ie al posi i e componen , and he LPN we e iden i ied o he H/H
and CR condi ions du ing bo h phases o he ask.
This so wa e is a h ee-dimensional, disc e e, linea , weigh ed
minimum no m in e se solu ion me hod ha es ima es he sou ces o
EEG eco ded on he scalp. A 3 shell-sphe ical head model is used as a
e e ence (using he Talai ach human b ain a las) and is di ided in
6239 oxels a a spa ial esolu ion o 5 mm. eLORETA ep esen s he
elec ical ac i i y a each oxel in neu oana omical Mon eal
Neu ological Ins i u e (MNI) space, al hough Talai ach coo dina es,
ana omical s uc u es and B odmann a eas a e also p o ided. Fo a
mo e de ailed desc ip ion o he me hod and he exac ze o-e o lo-
caliza ion p ope y, see Pascual-Ma qui e al. (2011).
2.5. S a is ical analysis
2.5.1. Beha iou al da a
Rega ding he immedia e memo y phase, epea ed measu es analysis
o a iance (ANOVA) wi h wo wi hin-subjec ac o s, Condi ion ( h ee
le els: H/H, H/M, CR) and Tes Block ( h ee le els: i s , second and
hi d), was conduc ed o compa e he pe cen age o esponses and he
RTs among H/H, H/M, CR condi ions and ac oss he h ee es blocks.
Rega ding he delayed memo y phase, a epea ed measu es ANOVA wi h
one wi hin-subjec ac o , Condi ion ( h ee le els: H/H, H/M, CR), was
used o compa e he pe cen age o esponses and he RTs among he
h ee condi ions. In addi ion, pai ed-sample - es s we e used o com-
pa e he RTs and he pe cen age o H/H esponses, be ween he hi d
es block o he immedia e memo y phase and he es o he delayed
memo y phase.
2.5.2. ERPs da a
Repea ed measu es ANOVAs wi h h ee wi hin-subjec ac o s,
Phase ( wo le els: Immedia e, Delayed), Condi ion ( wo le els: H/H, CR)
and ROI ( ou le els: mid on al, mid pos e io , le pos e io , igh
pos e io ), we e conduc ed in o de o compa e, be ween phases and
condi ions and among ROIs, he mean ampli udes o he on al nega-
i e componen and he pa ie al posi i e componen .
In he case o he LPN, a epea ed measu es ANOVA wi h ou
wi hin-subjec ac o s Phase ( wo le els: Immedia e, Delayed), Condi ion
( wo le els: H/H, CR), ROI ( ou le els: mid on al, mid pos e io , le
pos e io , igh pos e io ) and In e al (se en le els: 950–1100 ms,
1100–1250 ms, 1250–1400 ms, 1400–1550 ms, 1550–1700 ms,
1700–1850 ms and 1850–2000 ms) was pe o med in o de o compa e
he mean ampli ude be ween phases and condi ions, and among ROIs
and empo al in e als.
In addi ion, ac ional a ea la ency was e alua ed ia a epea ed
measu es ANOVA wi h wo wi hin-subjec ac o s, Phase ( wo le els:
Immedia e, Delayed) and Condi ion ( wo le els: H/H, CR) in o de o
compa e, be ween phases and condi ions, he la encies o he on al
nega i e componen (a Fz) and he pa ie al posi i e componen (a Pz).
G eenhouse-Geisse co ec ions o he deg ees o eedom we e
applied in all cases in which he condi ion o sphe ici y was no me . In
hese cases, he o iginal deg ees o eedom a e p esen ed oge he wi h
he co ec ed p and ε alues. When he ANOVAs showed signi ican
e ec s o he ac o s and/o hei in e ac ions o he beha iou al o
ERP da a, pos -hoc es ing o he mean alues was ca ied ou by pai ed
mul iple compa isons (wi h Bon e oni co ec ions). In addi ion, pa ial
e a squa ed (η2p) was calcula ed o each signi ican compa ison, wi h
he aim o de e mining he size o he e ec s. S a is ical signi icance
was conside ed o be p ≤ 0.05. The s a is ical analyses we e pe o med
wi h IBM SPSS S a is ics package .21 o Windows.
2.5.3. B ain sou ce localiza ion analysis
The eLORETA so wa e package was used o pe o m ( oxel-by-
oxel) wi hin-subjec compa isons. This non-pa ame ic me hod is
based on es ima ion, ia andomiza ion, o he empi ical p obabili y
dis ibu ion o he max-s a is ic unde he null hypo hesis, and i co -
ec s o mul iple es ing (Nichols & Holmes, 2002). The ollowing
s a is ical compa isons we e made: (1) H/H ela i e o CR condi ions, in
each memo y phase (immedia e and delayed), in o de o compa e he
ac i a ion o neu al sou ces be ween bo h condi ions, and (2) immedia e
ela i e o delayed memo y phases o each condi ion (H/H and CR), in
o de o compa e ac i a ion o neu al sou ces be ween bo h memo y
phases, o he co ec ly ecognized old wo ds (which we e pos e io ly
accompanied by co ec colou ecollec ion, H/H) and o he co ec ly
ejec ed new wo ds (CR). These compa isons we e pe o med (1) in
bo h empo al anges in which he on al nega i e and he pa ie al
posi i e componen s we e iden i ied: he 200–500 ms in e al and
400–900 ms in e al, espec i ely, and (2) in he 1200–1600 ms in-
e al, a ound which he maximum ampli ude di e ences be ween
M.Á. Ri as-Fe nández, e al. Neu obiology o Lea ning and Memo y 175 (2020) 107309
5
condi ions (H/H and CR) we e obse ed o LPN, in based on he g and-
a e age ERP wa e o ms o he immedia e memo y phase (in which a
signi ican LPN was ob ained, see Resul s sec ion). S a is ical compa -
isons be ween condi ions o phases, o he cu en densi y dis ibu ion,
we e es ima ed using pai ed sample - es . S a is ical signi icance was
conside ed o be p ≤ 0.05.
3. Resul s
3.1. Pe o mance
The mean alues o RTs and he pe cen age o esponses in each
condi ion (H/H, H/M, CR, e o s o old wo ds, alse ala ms and misses)
a e shown in Table 1. Mean alues o RTs and he pe cen age o e-
sponses in H/H, H/M and CR a e ep esen ed in Fig. 2.
3.1.1. Reac ion imes
Rega ding he immedia e memo y phase, he epea ed-measu es
ANOVA (Tes Block × Condi ion) showed a signi ican e ec o he Tes
Block ac o (F(2,30) = 26.4, p < 0.001, ε = 0.71; η
2
p = 0.63). Pos
hoc compa isons showed ha he mean RT in he h ee condi ions was
signi ican ly longe in he i s han in he second (p = 0.002) and he
hi d (p < 0.001) es blocks, and signi ican ly longe in he second
han in he hi d (p = 0.001) es block. No signi ican di e ences we e
obse ed o he RTs be ween he H/H, H/M and CR condi ions in each
phase, no be ween he hi d es block o he immedia e memo y phase
and he es o he delayed memo y phase in he H/H condi ion.
3.1.2. Pe cen age o esponses
Rega ding he immedia e memo y phase, he epea ed measu es
ANOVA (Tes Block × Condi ion) showed a signi ican e ec o he Tes
Block ac o (F(2,30) = 37.7, p < 0.001, ε = 0.72, η
2
p = 0.71),
Condi ion ac o (F(2,30) = 189.7, p < 0.001, ε = 0.61, η
2
p = 0.93)
and o he Tes Block × Condi ion in e ac ion (F(4,60) = 11.3,
p < 0.001, ε = 0.51, η
2
p = 0.43). Pos hoc compa isons e ealed ha
he pe cen age o CR and H/H esponses was signi ican ly lowe in he
i s han in he second and hi d es blocks [CR i s s second:
p = 0.03, i s s hi d: p < 0.001] [H/H i s s second: p = 0.003,
i s s hi d: p = 0.001], and he pe cen age o CR esponses was also
signi ican ly lowe in he second han in he hi d es block
(p = 0.008). In addi ion, he pe cen age o H/M esponses was sig-
ni ican ly highe in he i s han in he hi d es block (p = 0.03).
In he h ee blocks, he pe cen age o CR esponses was signi ican ly
highe han he pe cen age o H/H and H/M esponses [CR e sus H/H
in i s block: p < 0.001, second block: p < 0.001, hi d block:
p < 0.001] [CR e sus H/M in he i s block: p < 0.001, second
block: p < 0.001, hi d block: p < 0.001], and he pe cen age o H/H
esponses was signi ican ly highe han he pe cen age o H/M
Table 1
Mean alues and s anda d de ia ions (be ween pa en heses) o he pe cen age o esponses (%) and he eac ion imes (RTs, ms), in each condi ion: Hi /Hi (H/H),
Hi /Miss (H/M) and Co ec Rejec ion (CR), e o s o old wo ds, alse ala ms and misses.
Immedia e Phase Delayed Phase
Tes -Block 1 Tes -Block 2 Tes -Block 3 Mean Tes Blocks Delayed es
% RT % RT % RT % RT % RT
H/H 54.8 (11.5) 872 (129) 68.7 (9.5) 792 (140) 75.0 (13.7) 722 (136) 66.2 (8.4) 796 (124) 75.8 (11.0) 698 (110)
H/M 31.7 (14.6) 896 (215) 23.3 (11.3) 795 (156) 19.4 (12.3) 716 (167) 24.8 (10) 802 (145) 18.7 (9.8) 718 (142)
CR 86.5 (9.6) 921 (141) 92.8 (8.3) 789 (121) 98.2 (3.8) 705 (98) 92.5 (6.2) 805 (102) 97.0 (3.1) 686 (101)
ERRORS TO OLD WORDS 6.7 (8.4) 857 (219) 3.9 (5.3) 1084 (412) 2.8 (4.6) 769 (200) 4.5 (5.6) 873 (256.4) 2.8 (4.7) 783 (164)
FALSE ALARMS 7.2 (7.1) 1067 (287) 2.9 (3.6) 766 (202) 0.2 (0.9) –
a
3.4 (3.2) –
b
1.9 (2.5) 775 (210)
MISSES TO OLD WORDS 6.7 (9.1) 4.1 (4.3) 2.8 (4.2) 4.5 (4.6) 2.7 (4.5)
MISSES TO NEW WORDS 6.3 (10) 4.3 (8.5) 1.6 (3.8) 4.1 (7.0) 1.1 (2.7)
a
Mean and s anda d de ia ion o he mean eac ion ime o alse ala ms in he hi d es block we e no calcula ed because he e was only one pa icipan wi h one
alse ala m in ha block o he ask.
b
Mean and s anda d de ia ion o he mean eac ion imes o alse ala ms was no calcula ed because mos o pa icipan s did no ha e alse ala ms in one o mo e
es blocks.
Fig. 2. Mean alues o he pe cen age o esponses
(le ) and eac ion imes (RTs, igh ) in each condi-
ion: co ec ecogni ion o old wo ds wi h e ie al
o hei colou (Hi /Hi ), co ec ejec ion o new
wo ds (CR) and co ec ecogni ion o old wo ds
wi hou e ie al o hei colou (Hi /Miss). IMP-1:
Immedia e memo y phase-Tes 1; IMP-2: Immedia e
memo y phase-Tes 2; IMP-3: Immedia e memo y
phase-Tes 3; DMP: Delayed memo y phase es .
**p < 0.01, ***p < 0.001.
M.Á. Ri as-Fe nández, e al. Neu obiology o Lea ning and Memo y 175 (2020) 107309
6
esponses ( i s block: p = 0.006, second block: p < 0.001, hi d
block: p < 0.001).
Rega ding he delayed memo y phase, he epea ed measu es ANOVA
(Condi ion) e ealed a signi ican e ec o he ac o (F(2,30) = 248.7,
p < 0.001, η
2
p = 0.9), as he pe cen age o CR esponses was sig-
ni ican ly highe han he pe cen age o H/H (p < 0.001) and H/M
(p < 0.001) esponses, and he pe cen age o H/H was signi ican ly
highe han he pe cen age o H/M esponses (p < 0.001).
The pe cen age o H/H esponses was no signi ican ly di e en
be ween he hi d es block o he immedia e memo y phase and he es
o he delayed memo y phase.
3.2. E en - ela ed po en ials (ERPs)
G and-a e age ERP wa e o ms o he H/H and CR condi ions a
mid on al, mid pos e io , le pos e io and igh pos e io ROIs in he
immedia e and delayed memo y phases, a e shown in Fig. 3, and he
ol age maps a e shown in Fig. 4. Mean ampli ude and ac ional la-
ency esul s o he on al nega i e componen and he posi i e pa -
ie al componen a e summa ized in Table 2. Mean ampli ude esul s o
he LPN a e summa ized in Table 3.
Fo he ampli ude o he on al nega i e componen , he epea ed
measu es ANOVA (Phase × Condi ion × ROI) showed a signi ican
Fig. 3. G and-a e age ERP wa e o ms a he mid on al, mid pos e io , le pos e io and igh pos e io elec ode clus e s in he H/H and CR condi ions, du ing he
immedia e memo y phase and delayed memo y phase. The ed and blue do ed lines ep esen he mean RT o he H/H and CR condi ions, espec i ely. The black dashed
line ep esen s he mean ime o he p esen a ion o he colou ques ion. The g ey shaded a ea ep esen s in e als wi h signi ican esul s.
M.Á. Ri as-Fe nández, e al. Neu obiology o Lea ning and Memo y 175 (2020) 107309
7
e ec o he ROI ac o and he Phase × ROI in e ac ion. Pos hoc
compa isons e ealed ha , du ing he immedia e memo y phase, he
ampli ude was signi ican ly mo e nega i e a he mid on al han a he
mid pos e io (p = 0.007) and he igh pos e io (p = 0.047) ROIs. In
addi ion, du ing he delayed memo y phase, i was signi ican ly mo e
nega i e a he mid on al han a he mid pos e io (p = 0.003), he
le pos e io (p = 0.044) and he igh pos e io (p = 0.008) ROIs.
The epea ed measu es ANOVA (Phase × Condi ion) did no show
any signi ican e ec o he ac o s o hei in e ac ion o he la ency o
he on al nega i e (FN400) componen .
Fo he ampli ude o he pa ie al posi i e componen , he epea ed
measu es ANOVA (Phase × Condi ion × ROI) showed a signi ican
e ec o he Phase, Condi ion and ROI ac o s as well as he
Phase × Condi ion and he Phase × ROI in e ac ions. Pos hoc
compa isons e ealed ha he mean ampli ude was signi ican ly la ge :
(1) in he H/H han in he CR condi ion in bo h memo y phases (im-
media e: p = 0.005, delayed: p < 0.001), indica ing a signi ican pa -
ie al old/new e ec ; (2) a he mid pos e io han a he mid on al ROI
(p = 0.005) du ing he immedia e memo y phase, (3), a he mid pos-
e io han a he mid on al (p < 0.001) and he igh pos e io
(p = 0.01) ROI, and a he le pos e io han a he mid on al ROI
(p = 0.02), du ing he delayed memo y phase; (4) in he delayed han in
he immedia e memo y phase (p = 0.02), in he H/H condi ion; and (5)
in he delayed han in he immedia e memo y phase in he mid pos e io
(p = 0.03) and le pos e io (p = 0.03) ROIs.
Fo he pa ie al posi i e componen la ency, he epea ed measu es
ANOVA (Phase × Condi ion) showed a signi ican e ec o he
Fig. 4. Vol age maps o he mean ampli ude o he on al nega i i y componen ( op), he pa ie al posi i e componen (middle) and he la e pos e io nega i i y
(LPN, bo om), in he H/H and CR condi ions, du ing he immedia e and delayed memo y phases.
Table 2
F alues in epea ed measu es ANOVA (Phase × Condi ion × ROI) o he
mean ampli udes and 50% ac ional a ea la encies o he on al nega i e
componen and he pa ie al posi i e componen .
F on al nega i e
componen
Pa ie al posi i e
componen
Mean Ampli ude
ANOVA (P × C × R)
P 1.4, η
2
p = 0.09 4.6*, η
2
p = 0.24
C 4.4, η
2
p = 0.23 24.2***, η
2
p = 0.62
R 7.3***, η
2
p = 0.33 11.2***, η
2
p = 0.43
P X C 1.4, η
2
p = 0.08 6.5*, η
2
p = 0.30
P X R 5.1*, ε = 0.56;
η
2
p = 0.25
10.8***, η
2
p = 0.42
C X R 0.8, ε = 0.52; η
2
p = 0.05 2.8, ε = 0.71; η
2
p = 0.16
P X C X R 0.1, ε = 0.51;
η
2
p = 0.006
2.4, ε = 0.56; η
2
p = 0.14
F ac ional A ea La ency
ANOVA (P × C)
P 2.2, η
2
p = 0.13 0.003, η
2
p < 0.001
C 0.7, η
2
p = 0.04 11.2**, η
2
p = 0.43
P × C 3.6, η
2
p = 0.2 0.95, η
2
p = 0.06
P: Phase ac o ; C: Condi ion ac o ; R: ROI ac o ; ε = epsilon, η
2
p = pa ial e a
squa ed alue. Deg ees o eedom o : P: 1,15; C: 1,15; R: 3,45 and he in e -
ac ions P × C: 1,15; P × R: 3,45; C × R: 3,45; P × C × R: 3,45.
*p < 0.05; **p < 0.01; ***p < 0.001
Table 3
F alues in epea ed measu es ANOVA (Phase × Condi ion × ROI × In e al)
o he mean ampli udes o he LPN in se en empo al windows o 150 ms.
La e Pos e io Nega i i y (LPN)
Mean Ampli ude
ANOVA (P × C × R × I)
P 9.4**, η
2
p = 0.39
C 12.1**, η
2
p = 0.45
R 2.6, η
2
p = 0.15
I 2.4, η
2
p = 0.14
P × C 10.6**, η
2
p = 0.41
P × R 1.7, η
2
p = 0.10
P × I 0.8, η
2
p = 0.47
C × R 3.7*, ε = 0.55, η
2
p = 0.20
C × I 8.8***, ε = 0.42, η
2
p = 0.37
R × I 2.1**, η
2
p = 0.12
P × C × R 2.9, η
2
p = 0.16
P × C × I 0.5, η
2
p = 0.03
P × R × I 1.5, η
2
p = 0.09
C × R × I 6.5***, η
2
p = 0.30
P × C × R × I 1.1, η
2
p = 0.07
P: Phase ac o ; C: Condi ion ac o ; R: ROI ac o ; I: In e al; ε = epsilon,
η
2
p = pa ial e a squa ed alue. Deg ees o eedom o : P: 1,15; C: 1,15; R:
3,45; I: 6,90 and he in e ac ions P × C: 1,15; P × R: 3,45; C × R: 3,45;
P × C × R: 3,45; P × I: 6,90, C × I: 6,90, P × C × I: 6,90, R × I: 18,270,
P × R × I: 18,270, C × R × I: 18,270, P × C × R × I: 18,270.
*p < 0.05; **p < 0.01; ***p < 0.001.
M.Á. Ri as-Fe nández, e al. Neu obiology o Lea ning and Memo y 175 (2020) 107309
8
Condi ion ac o . Pos hoc compa isons e ealed ha he la ency was
signi ican ly sho e in he H/H han in he CR condi ion (p = 0.004).
Fo he LPN mean ampli ude, he epea ed measu es ANOVA
(Phase × Condi ion × ROI × In e al) showed a signi ican e ec o
he Phase and Condi ion ac o s, as well as he ollowing in e ac ions:
Phase × Condi ion, Condi ion × ROI, Condi ion × In e al,
ROI × In e al, and Condi ion × ROI × In e al.
Pos hoc compa isons e ealed ha he mean ampli ude o LPN was
signi ican ly mo e nega i e in he H/H condi ion han in he CR con-
di ion (p = 0.001) in he immedia e memo y phase; and no signi ican
di e ences we e ob ained be ween bo h condi ions (p = 0.07) in he
delayed memo y phase, al hough he di e ences we e in he same di-
ec ion (H/H mo e nega i e han CR). In addi ion, he mean ampli ude
o he H/H condi ion was signi ican ly mo e nega i e in he immedia e
han in delayed memo y phase (p = 0.002).
On he o he hand, pos hoc compa isons also e ealed ha he
mean ampli ude in he H/H condi ion was signi ican ly mo e nega i e
han he CR condi ion, a he ollowing ROIs and in e als: (1) Mid
on al loca ions, in he 950–1100 ms (p = 0.004), 1100–1250 ms
(p = 0.001), 1250–1400 ms (p = 0.001), 1400–1550 ms (p < 0.001),
1550–1700 ms (p = 0.002), 1700–1850 (p = 0.017) in e als; (2) Mid
pos e io loca ions, in he 950–1100 ms (p = 0.001), 1100–1250 ms
(p < 0.001), 1250–1400 ms (p < 0.001), 1400–1550 ms (p = 0.001),
1550–1700 ms (p = 0.002), 1700–1850 (p = 0.049) in e als; (3) Le
pos e io loca ions, in he 950–1100 ms (p = 0.017), 1100–1250 ms
(p = 0.002), 1250–1400 ms (p = 0.002), 1400–1550 ms (p = 0.003),
1550–1700 ms (p = 0.007) in e als and (4) Righ pos e io loca ions,
in he 950–1100 ms (p = 0.001), 1100–1250 ms (p = 0.001),
1250–1400 ms (p = 0.001), 1400–1550 ms (p = 0.005) and
1550–1700 ms (p = 0.018) in e als.
In addi ion, pos hoc compa isons e ealed ha he mean ampli ude
o LPN in he H/H condi ion was signi ican ly mo e nega i e: (1) a he
le pos e io han a he igh pos e io loca ions in he 1250–1400 ms
in e al (p = 0.031) and he 1850–2000 ms in e al (p = 0.041), and
(2) a he mid pos e io and he le pos e io han he igh pos e io
loca ions in he 1550–1700 ms in e al (p = 0.002 and p = 0.016,
espec i ely) and in he 1700–1850 ms in e al (p = 0.037 and
p = 0.012, espec i ely).
The mean ampli ude o LPN in he CR condi ion was signi ican ly
mo e nega i e: (1) a he le pos e io han a he mid pos e io loca-
ions du ing he 950–1100 ms (p = 0.018) and he 1100–1250 ms
(p = 0.005) in e als, (2) a he mid on al (p = 0.049) and a he le
pos e io (p = 0.003) han a he mid pos e io loca ions, as well as a
he le pos e io han a he igh pos e io loca ions (p = 0.05), du ing
he 1250–1400 ms, and (3) a he le pos e io han a he mid pos-
e io loca ions in he 1400–1550 ms (p = 0.006) and he
1550–1700 ms in e als (p = 0.039).
Finally, pos hoc compa isons also e ealed ha he mean ampli-
ude o LPN in he H/H condi ion was signi ican ly mo e nega i e: (1)
in he 1550–1700 ms (p = 0.018) and 1700–1850 ms (p = 0.016)
in e als han in he 1850–2000 ms in e al, a he mid pos e io lo-
ca ions, (2) in he 1100–1250 ms (p = 0.02), 1550–1700 ms
(p = 0.014) and 1700–1850 ms (p = 0.013) in e als han in he
1850–2000 ms in e al, a he le pos e io loca ions, and (3) in he
950–1100 ms (p = 0.002), 1100–1250 ms (p = 0.008), 1400–1550 ms
(p = 0.037), 1550–1700 ms (p = 0.004) and he 1700–1850 ms
(p = 0.007) in e als han in he 1850–2000 ms in e al, as well as in
he 1550–1700 ms han in he 1700–1850 ms in e al (p = 0.034), a
he igh pos e io loca ions.
3.3. B ain sou ce localiza ion analysis
Table 4 shows he MNI coo dina es and B odmann a eas o hose
b ain egions in which signi ican di e ence in ac i a ion was obse ed
in he ollowing: (1) he H/H > CR con as , du ing he immedia e and
delayed memo y phases; and (2) he delayed memo y phase > immedia e
memo y phase con as , in he H/H and CR condi ions.
Du ing he immedia e memo y phase, he pai ed sample - es did no
e eal any signi ican di e ences in b ain ac i a ion be ween he H/H
and CR condi ions in he empo al in e al o he on al nega i e
componen (200–500 ms); howe e , hey showed signi ican ly g ea e
neu al ac i i y in he H/H han he CR condi ion in he pa ie al posi i e
componen in e al (400–900 ms) [ (15) = 4.1, p < 0.05], speci ically
in he in e io pa ie al lobule (BA: 40), pa ahippocampal gy us (BA: 28,
34), uncus (BA: 28, 34), p ecuneus (BA: 7) and lingual gy us (BA: 18) o
he le hemisphe e, and in he igh pos e io cingula e (BA: 30). In he
empo al in e al o LPN (1200–1600 ms), he pai ed sample - es
showed signi ican ly g ea e neu al ac i i y in he H/H han he CR
condi ion [ (15) = 3.8, p < 0.05] in he pa ahippocampal gy us (BA:
28), an e io cingula e gy us (BA: 32), insula (BA: 13), supe io , medial
and middle on al gy i (BA: 10, 32, 46), uncus (BA: 28) and ans e se
empo al gy us (BA: 41) o he le hemisphe e, as well as in he ec al
gy us (BA: 11), in e io on al gy us (BA: 46), subcallosal gy us (BA:
25) and pos e io cingula e gy us (BA: 30) o he igh hemisphe e (see
Table 4 and Fig. 5).
Rega ding he delayed memo y phase, he pai ed sample - es did no
e eal any signi ican di e ences in b ain ac i a ion be ween he H/H
and CR condi ions in he on al nega i e componen in e al
(200–500 ms). In he pa ie al posi i e componen in e al
(400–900 ms), he pai ed sample - es showed signi ican ly g ea e
neu al ac i i y o he H/H han he CR condi ion [ (15) = 4.0,
p < 0.05] in he insula (BA: 13), pos e io cingula e gy us (BA: 31),
uncus (BA: 28), p ecuneus (BA: 7) and pa ahippocampal gy us (BA: 34)
o he le hemisphe e, he bila e al supe io empo al gy us (BA: 22,
42) and also he pos e io cingula e gy us (BA: 23) o he igh hemi-
sphe e. In he LPN empo al in e al (1200–1600 ms), he pai ed
sample - es showed signi ican ly g ea e neu al ac i i y o he H/H
han he CR condi ion ( (15) = 3.9, p < 0.05) in he supe io em-
po al gy us (BA: 41) and insula (BA: 13) o he le hemisphe e, and also
in he igh pa ahippocampal gy us (BA: 28) (see Table 4 and Fig. 5).
Finally, wi hin he H/H condi ion, he pai ed sample - es s e ealed
signi ican ly g ea e ac i a ion [ (15) = − 3.9, p < 0.05)] o he le
insula (BA: 13) and he igh medial on al gy us (BA: 10) in he de-
layed compa ed o he immedia e memo y phase du ing he LPN empo al
in e al (1200–1600 ms) (see Table 4 and Fig. 6). In addi ion, o he
CR condi ion, signi ican ly g ea e ac i a ion [ (15) = − 4.4,
p < 0.01)] o he igh pa ahippocampal gy us (BA: 19) was obse ed
in he delayed memo y phase han in he immedia e memo y phase, du ing
he empo al in e al o LPN (1200–1600 ms) (see Table 4 and Fig. 6);
howe e , no di e ences be ween bo h memo y phases we e obse ed in
he 400–900 ms in e al.
4. Discussion
In he p esen ERP s udy using he exac low elec omagne ic e-
solu ion omog aphy (eLORETA), we cha ac e ized and compa ed he
pe o mance and he spa io empo al pa e n o he b ain elec ical ac-
i i y ela ed o he success ul immedia e episodic e ie al o in-
o ma ion which is being lea ned ela i e o delayed episodic e ie al
( wen y minu es la e ) o he same in o ma ion.
Fo his pu pose, young pa icipan s ca ied ou an old/new wo d
ecogni ion ask wi h sou ce memo y, which included an immedia e
memo y phase (wi h h ee s udy- es blocks) ollowed (a e 20 min) by a
delayed memo y phase wi h one es block. Beha iou al da a showed
g adual lea ning and consolida ion o he in o ma ion (old wo ds)
du ing he immedia e memo y phase. The ERP da a showed ha , ela i e
o co ec ly iden i ied new wo ds (CR esponses), co ec ly judged old
wo ds (H/H esponses) elici ed he ollowing in bo h memo y phases:
(1) a mo e posi i e-going po en ial, demons a ing a pa ie al old/new
e ec (a ound 500–675 ms pos -s imulus in e al) ela ed o ecollec-
ion, and (2) a mo e nega i e-going po en ial, demons a ing an LPN
e ec (in he 950–1850 ms pos -s imulus in e al a he mid on al and
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