Brief learning induces a memory bias for arousing-negative words

15 Pages·2015·1.19 MB·English

ORIGINALRESEARCH
published:21August2015
doi:10.3389/fpsyg.2015.01226
Brief learning induces a memory bias
for arousing-negative words: an fMRI
study in high and low trait anxious
persons
Editedby:
AnnuschkaS.Eden1,2*,VeraDehmelt1,2,MatthiasBischoff3,PienieZwitserlood4,
CorneliaHerbert,
UniversityClinicforPsychiatry HaraldKugel5,KatiKeuper6,PeterZwanzger7andChristianDobel1,8,9*
andPsychotherapy,Tübingen,
1InstituteofBiomagnetismandBiosignalanalysis,UniversityHospitalofMünster,Münster,Germany,2Instituteof
Germany
Psychology,UniversityofMünster,Münster,Germany,3InstituteofSportandExerciseSciences,UniversityofMünster,
Reviewedby:
Münster,Germany,4DepartmentofPsycholinguisticsandCognitiveNeurosciences,InstituteofPsychology,Universityof
ChristophScheepers, Münster,Münster,Germany,5DepartmentofClinicalRadiology,UniversityofMünster,Münster,Germany,6Universityof
UniversityofGlasgow,UK HongKong,HongKong,HongKong,7kbo-Inn-SalzachClinic,AcademicHospitalofPsychiatry,Psychotherayand
Hsu-WenHuang, Neurology,WasserburgamInn,Germany,8DepartmentofPsychology,UniversityofBielefeld,Bielefeld,Germany,
NationalTaiwanNormalUniversity, 9DepartmentofOtolaryngology,JenaUniversityHospital,Jena,Germany
Taiwan
*Correspondence:
Persons suffering from anxiety disorders display facilitated processing of arousing and
AnnuschkaS.Eden,
InstituteofBiomagnetism negative stimuli, such as negative words. This memory bias is reflected in better
andBiosignalanalysis,University recall and increased amygdala activity in response to such stimuli. However, individual
HospitalofMünster,Malmedyweg15,
learning histories were not considered in most studies, a concern that we meet here.
48143Münster,NRW,Germany
[email protected]; Thirty-four female persons (half with high-, half with low trait anxiety) participated in
ChristianDobel,
a criterion-based associative word-learning paradigm, in which neutral pseudowords
DepartmentofPsychology,
UniversityofBielefeld, were paired with aversive or neutral pictures, which should lead to a valence change
P.O.Box100131,D-33501Bielefeld, for the negatively paired pseudowords. After learning, pseudowords were tested with
Germany
fMRI to investigate differential brain activation of the amygdala evoked by the newly
[email protected]
acquiredvalence.Explicitandimplicitmemorywasassesseddirectlyaftertrainingandin
Specialtysection:
threefollow-ups at 4-day intervals.The behavioral results demonstrate that associative
Thisarticlewassubmittedto
word-learning leads to an explicit (but no implicit) memory bias for negatively linked
LanguageSciences,
asectionofthejournal pseudowords,relativetoneutralones,whichconfirmsearlierstudies.Bilateralamygdala
FrontiersinPsychology
activationunderlinesthebehavioraleffect:Highertraitanxietyiscorrelatedwithstronger
Received:13February2015
amygdala activation for negatively linked pseudowords than for neutrally linked ones.
Accepted:03August2015
Published:21August2015 Most interestingly, this effect is also present for negatively paired pseudowords that
Citation: participantscould not remember well. Moreover, neutrally paired pseudowords evoked
EdenAS,DehmeltV,BischoffM, higheramygdalareactivitythancompletely novelonesinhighlyanxiouspersons,which
ZwitserloodP,KugelH,KeuperK,
canbetakenasevidenceforgeneralization.Thesefindingsdemonstratethatfewword-
ZwanzgerPandDobelC(2015)Brief
learninginducesamemorybias learning trials generate a memory bias for emotional stimuli, indexed both behaviorally
forarousing-negativewords:anfMRI
andneurophysiologically. Importantly,thetypicalmemory biasforemotional stimuliand
studyinhighandlowtraitanxious
persons. thegeneralization toneutralonesislargerinhighanxiouspersons.
Front.Psychol.6:1226.
doi:10.3389/fpsyg.2015.01226 Keywords:traitanxiety,fMRI,emotions,memorybias,consolidation,statisticalword-learning,amygdala
FrontiersinPsychology|www.frontiersin.org 1 August2015|Volume6|Article1226
Edenetal. Memorybiasforarousing-negativewords
Introduction for emotional information is still under debate. While some
providesupportforitsexistence(e.g.,Williamsetal.,1988,1996,
Emotionally arousing situations and stimuli are processed 1997;EysenckandByrne,1994),otherscouldnotreplicatetheir
preferentially. This has been shown by a vast body of studies, findings (McCabe, 1999; Russo et al., 1999). Our results might
withmethodsrangingfromsimplebehavioralmeasurestostate- contributetothiscontroversy.
of-the-artimagingtechniques(e.g.,Junghöferetal.,2001;Koster The memory bias can be detected with neuroimaging
et al., 2006; Laeger etal., 2012; Edenet al., 2014; Weierich and measuressuchasfunctionalmagneticresonanceimaging(fMRI),
Treat, 2015; for a meta-analysis, see Bar-Haim et al., 2007; for whichissensitiveenoughtoevenrevealemotionalresponsesto
a review, see Cisler and Koster, 2010). Preferential processing itemsthatcannotberecalledexplicitly(Dannlowskietal.,2007b).
leads to a memory bias, apparent in enhanced memory for As neural correlates of emotion processing many fMRI studies
emotionalascomparedtoneutralstimuli.Thishasbeenshown have focused on limbic structures, particularly the amygdalae
for many stimulus types, such as pictures (Bradley et al., 1992; (e.g.,DavisandWhalen,2001;PhelpsandLeDoux,2005).Ithas
Schuppetal.,2004a;Touryanetal.,2007;YegiyanandYonelinas, been repeatedly demonstrated that the amygdala is hyperactive
2011),faces(Schuppetal.,2004b),scenes(HeuerandReisberg, inresponse tothreatening andnegativeemotionalstimuli.This
1990), gestures (Flaisch et al., 2011), and words (Kissler et al., hyperactivity is evident for faces (e.g., Birbaumer et al., 1998;
2007, 2009;Herbert etal., 2008;Scott et al.,2009;Laegeret al., Shelineetal.,2001;Phanetal.,2006;Dannlowskietal.,2007a,b;
2012;Keuperetal.,2013,2014;Edenetal.,2014).Thememory Evansetal.,2008;Halletal.,2014),scenes(e.g.,Kryklywyetal.,
bias,especiallyforstimulithatarenegativeandarousing,seems 2013;FrankandSabatinelli,2014;Raduaetal.,2014),andwords
more prominent in persons suffering from an anxiety disorder (e.g.,Isenbergetal.,1999;Strangeetal.,2000;Tabertetal.,2001;
(Calvo et al., 1994; Friedman et al., 2000; Dalgleish et al., HamannandMao,2002;Cunninghametal.,2004;Herbertetal.,
2003; Eysenck et al., 2007) or from a subclinically anxious 2011;Kanske and Kotz, 2011;Straubeetal.,2011;Laegeretal.,
personality (Norton et al., 1988; McCabe, 1999; Russo et al., 2012;Hoffmannetal.,2015),and isassumedtoexplain partof
2006; Mühlberger et al., 2009; Eden et al., 2014). The latter thepathogenesisandthemaintenanceofanxiety(disorders;e.g.,
group exhibits high levels of trait anxiety, does not meet the Etkin and Wager, 2007; Etkin et al., 2010; Shin and Liberzon,
criteria for an anxiety disorder, but is prone to develop one 2010; Xu et al., 2013; Binelli et al., 2014; but see Dresler et al.,
(e.g.,McCabe,1999;Russoetal.,2006;Mitte,2008;Waldhauser 2013foranalternativeview).Giventheongoingdebateaboutthe
etal.,2011).Increasedpreferentialprocessingofnegativestimuli, neurobiologicalbasisof(trait)anxiety,itiscrucialtoincorporate
difficultdisengagementfromsuchstimuli,attentionalavoidance, imaging measurements into the study design, especially when
and their underlying mechanisms explain part of the anxiety stimuli are presented below threshold, or trained in a shallow
disorders’etiology(e.g.,Edenetal.,2015;forareview,seeCisler learningparadigmthatdoesnotguaranteerobustexplicitaccess.
andKoster,2010).Thus,forabetterunderstandingofthislarge The latter is the case in our study, in which persons with high
group of disorders, and for the improvement of therapeutic or low levels of anxiety should learn to associate meaning to
treatments, it is crucial to understand the mechanisms that pseudowords with only few learning instances. Pseudowords
underlie the acquisition and processing of arousing-negative were either paired with neutral or with emotionally negative
stimuli. To this aim, we compare persons with high and low content, and tested with explicit as well as implicit memory
(subclinical) anxiety in an associative learning paradigm, using measures.Weinvestigatedthememorybiasfornovelemotional
behavioralandneuroimagingmeasures. (and neutral) words in persons with subclinically high and
Learningandmemoryhaveexplicitandimplicitcomponents low trait anxiety. A criterion-based approach during learning
that are indexed by different measures and methods. Explicit allowedfordistinguishingbetweennovelwordswhosemeaning
memory involves conscious recollection of previous experience could be accessed explicitly, and words that were learned less
and information (semantic, episodic, and autobiographic). well.
Memoryistypicallymeasuredbyexplicitrecallorrecognitionof Despite the many studies on emotion, our approach allows
learned material. In contrast, memory access remains unaware to addresssome important issues.First, we investigate memory
in implicit memory, as is the case for procedural information bias for neutral stimuli that gain their emotional connotation
used in tie-knotting or bike-riding. Implicit memory reveals via associative learning (similarly as in Eden et al., 2014).
itselfthroughpriming,measuredintaskssuchasword-fragment These stimuli possess no specific innate or learned valence
completion(e.g.,EysenckandByrne,1994),orvalencejudgment (in contrast to a picture of an attacking tiger, or of a
of recently acquired words – when explicit knowledge about weapon). With meaningless and association-free pseudowords,
their meaning is absent. Implicit and explicit memories differ, we aim at better control of the individual learning histories
and have different neurobiological correlates (e.g., Starr and and the depth of encoding. Second, we use explicit and
Phillips, 1970; Cohen and Squire, 1980; Nissen and Bullemer, implicitmemorymeasurestorepresentthesedifferingaspectsof
1987; Gabrieli et al., 1995; Rugg et al., 1998). The memory memory.Third,weappliedacriterion-basedlearningapproach,
bias for emotional stimuli is more reliable in explicit than in ensuring that participants learned the same amount of word-
implicit measures(Eysenck andByrne,1994;Russoetal.,2006; picture pairs, and were presented with equal sets of explicitly
for a review, see Mitte, 2008). Mitte (2008) showed that (trait) learned and less well-learned items in the fMRI measurement,
anxiety has an impact on explicit measures such as recall, but independent of their learning history. Fourth, we included an
not on recognition. The existence of an implicit memory bias fMRI measurement into our design to analyze the amygdala’s
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Edenetal. Memorybiasforarousing-negativewords
response to the newly acquired and to completely novel increased emotional valence for neutrally paired pseudowords
pseudowords. after training. We included completely novel pseudowords for
Inthefollowing,wedescribetherationaleandthebackground particularfMRIcontrasts(seebelow).
ofourlearningdesigninmoredetail.Withastatisticallearning Insum,weinstantiatedshallowlearningviathecombination
paradigm(e.g.,Saffranetal.,1996;BreitensteinandKnecht,2002; of pseudowords with arousing-negative or neutral picture
Saffran, 2002; Breitenstein et al., 2007; Cunillera et al., 2010; content, which should nevertheless lead to a memory bias.
Eden et al., 2014; Laeger et al., 2014a), neutral pseudowords Next to behavioral effects we focused on neurophysiological
were paired with either arousing-negative or neutral pictures. consequencesoflearning,asindexedbyamygdalaractivity.For
This paradigm implements an increased conjoint probability this,wecontrastedthefollowingconditions:
of two events (“correct pairings”) throughout the training,
comparedtotwoeventswitharandomcontingency(“incorrect (a) Explicitly learned pseudowords vs. novel pseudowords
pairings”). Participants extract relevant information without (contrast 1); less well-learned pseudowords vs. novel
receivingfeedbackandwithoutknowingtheunderlyinglearning pseudowords(contrast2).Thesecomparisonsinformabout
principle –ashallowtype of learning.Byrepeated presentation generallearningeffectsfornewwordforms,eveniftheywere
of stimulus combinations, highly robust long-term learning is notlearnedwellexplicitly.
possible. The more repetitions, the stronger the associations (b) Arousingpseudowordsvs.neutralpseudowords(contrast3).
between the stimuli, which results in a typical learning curve. Thiscontrastdisplaysword-affecteffects.
Hebbian cell assemblies probably provide the neural bases of (c) Explicitly learned arousing pseudowords vs. less well-
these processes (Pulvermüller, 1999). The paradigm has some learnedarousingpseudowords(contrast4).Thiscomparison
ecological validity and can be taken as a model for language informs about similarities or differences between explicitly
acquisitioninchildrenandadults(Dobeletal.,2009,2010).Italso learned vs. less well-learned emotionally arousing-negative
allowstheinvestigationofexplicitandimpliciteffectsofshallow stimuli.
learning(asinvestigatedsimilarlyinourpriorstudy,Edenetal., (d) Less well-learned arousing-negative pseudowords vs.
2014). less well-learned neutral pseudowords (contrast 5); less
Two groups of participants, one high and one low in trait well-learned neutral pseudowords vs. novel pseudowords
anxiety,weretested.Variousmeasurementswereusedtoevaluate (contrast 6). Less well-learned arousing-negative vs. novel
and analyze potentially biased memories: a valence rating, a pseudowords(contrast7).Thesecontrastsinvestigateeffects
cued-recall test and an fMRI assessment. The behavioral tests ofword-affectwhenwordsarenotlearnedandremembered
werepresenteddirectlyafter,4,8,and12daysafterlearning,to well.
assesseffectsofconsolidationandforgetting.Thevalencerating (e) Neutral pseudowords vs. novel pseudowords (contrast
entailedaspontaneous evaluationofthepseudowords’(gained) 8), to assess generalization effects reported earlier (Eden
valence.Valenceratingsdonotrequireexplicitmemoryandcan et al., 2014). This contrast tested additionally whether
thustapintoimplicitmemory,indexingthevalencetransferred pseudowords paired with neutral meaning evoke higher
from pictures to formerly neutral pseudowords. We chose the activitythancompletelynovelpseudowords.
valence rating because it has been effectively applied after only
a few learning instances, when explicit measures are not yet In a second step, we tested whether effects are mediated by
sensitive to learning (e.g., Steinberg et al., 2012; Eden et al., traitanxiety.Thiswasdonebyenteringtraitanxietyascovariate.
2014). The cued-recall test measured explicit knowledge about
theacquiredmeaningofthepseudowords.Itiscomparabletoa
vocabularytest. Materials and Methods
In Eden et al. (2014), we used a very similar design to
investigate learning of emotional words in persons with high EthicsStatement
anxiety. We obtained very little evidence for a memory bias All procedures were cleared by the ethical review board of
during learning, but explicit and implicit measures revealed a the Ärztekammer Westfalen-Lippe and subjects gave informed
bias after learning. High-anxious persons displayed a stronger consent to participate. All clinical investigation was conducted
memory bias than low-anxious individuals. In fact, they even accordingtotheprinciplesoftheDeclarationofHelsinki.
judged neutrally paired words as negative when their meaning
could not explicitly be recalled. We took this effect asevidence Participants
for generalization (Eden et al., 2014). Given these findings and TheSpielbergerStateTraitAnxietyInventory(Spielbergeretal.,
thecurrentliterature,weexpectedforthecurrentstudyenhanced 1983) was completed via online survey by 310 non-clinical
memoryeffects(i.e.,memorybias)foraversivestimulusmaterial participants. On the basis of individual scores, 17 participants
immediately after learning and a stabilization of this effect scoring thirty or below in the trait-anxiety inventory (range:
after a time delay allowing consolidation. In line with Mitte 20–80) were assigned to the low-anxiety group (mean trait
(2008), we predicted a stronger bias in explicit cued-recall score = 27.76, SD = 4.15; mean age 26.53, SD = 6.21).
and fMRI measurements than in (implicit) valence ratings. Another 17 subjects scoring fifty or above were assigned to
We also expected a more pronounced bias in high-anxious the high-anxiety group (mean trait score = 57.18, SD = 4.33;
individuals, who should also show a generalization effect, with mean age 26.12, SD = 5.60). Both groups consisted of only
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Edenetal. Memorybiasforarousing-negativewords
females that were matched for age and years of schooling. upcoming recall and valence tests and received no feedback
All participants were native speakers of German, right-handed on their responses during training. The training consisted
(as assessed by the Edinburgh HandednessInventory, Oldfield, of at least six learning passes. During each learning pass,
1971) and exhibited no current axis I disorders, as diagnosed participants were confronted with one matching “correct” and
bytheMini-InternationalNeuropsychiatric Interview(M.I.N.I., onemismatching“incorrect”pseudoword-picturepair,separated
Sheehanetal.,1998).Nonetookpartinourearlierstudy(Eden by at least one other pair. Hence, after learning pass eight,
etal.,2014). for instance, participants had heard each pseudoword sixteen
times, eight times paired correctly (the same pseudoword-
Materials object combination) and eight times paired incorrectly (the
Forty-fourpseudowords(e.g.,“muxo,”“alep”)servedaslearning pseudowordpairedwitheightdifferentotherobjects).Notethat
materials, presented visually during learning and testing. all pseudowords used in “incorrect” pairings were “correctly”
(Stimulus material and result files are available from the paired with other pictures. Thus, all presented pseudowords
corresponding author). All pseudowords were disyllabic and could be associated with meaning, and all pseudowords and
phonotactically legal (in German). They were taken from pictures appeared equally often. There were 88 pseudoword-
Breitenstein and Knecht (2002; Breitenstein et al., 2007), who picture pairs per learning pass (22 correct arousing-negative,
tested the stimuli for emotional neutrality and low similarity 22 correct neutral, 22 incorrect arousing-negative, 22 incorrect
to existing German words. The selected 44 pseudowords were neutral).
randomlyassignedto44picturesdepictingconcreteobjects.Half The training aborted when 11 arousing-negative and 11
displayed neutral objects such as a bucket or a chair, and the neutralpseudoword-picture pairswereaccuratelyidentified(hit
other half showed arousing-negative objects such as a gun or or correct rejection) for eight times. Training continued until
a shark. Pictures were color photos taken from Hemera Photo thiscriterionwasreached.Thecriterionapproachensuredequal
Objects, Wikipedia Commons1 and the International Affective learning for all participants. Participants were confronted with
Picture System (Langetal.,1999). Somepictures were cropped 8.26(range:7–12)learningpassesonaverage.Thechoicefor11
toensurethatonly oneobject wasvisibleandpositioned inthe pairs per valence condition and eight correct answers ensured
center.(SeeAppendixinSupplementaryMaterialforalistofall thatenoughpairingswerelearnedwellenoughtobedetectablein
pseudowordsandmatchedconcepts.Thepicturematerialcanbe explicit/implicitbehavioralandimagingmeasures.Ontheother
requestedfromtheauthor). hand,wewantedtoavoidaceilingeffect,tobeabletoinvestigate
A pre-test assessed neutral or arousing-negative appraisal of pseudowordswhosemeaningwasnotlearnedtocriterion.Thus,
the pictures. Thirty participants (psychology students from the the total number of trials was not fixed and depended on the
University of Münster) were presented with 100 pictures (50 learners’ pace of learning. Left/right assignment of “correct”
subjectively judged to be negative and arousing, 50 subjectively and“incorrect”answerstoreponsebuttonswascounterbalanced
judged neutral, non-arousing). Subjects rated valence and across participants. All participants finished within an hour
(cid:2)
arousalofallpicturesviaSelf-AssessmentManikin(SAM)-scales (44 min on average). Presentation font size was 48, on a 15
(Bradley and Lang, 1994), ranging from one (very pleasant monitor.Allstimuliwerepresentedcentered,inwhiteagainsta
or low arousal) to nine (very unpleasant or high arousal). blackbackground.Alltrialsbeganwithafixationcross(500ms),
The 22 most negatively rated pictures (valence: Mean = 7.85, followed by a pseudoword (1000 ms). Another fixation cross
SD=0.30;arousal:Mean=5.77,SD=0.38)differedsignificantly (300ms)andapicture (1000ms)followed.Afer3000ms,ared
from the 22 most neutrally rated (valence: Mean = 4.76, exclamation mark ended the trial, providing sufficient time for
SD=0.21;arousal:Mean=1.90,SD=0.21)pictures[valence: the subjects to decide whether pseudoword and pictured object
t(42) = 38.908, p < 0.001; arousal: t(42) = 42.149, p < 0.001]. matched.If no answerwas given,the next trial wasinitiated. If
These 44 pictures served as materials in the experiment. abutton waspressedwithin the3000 msinterval,the nexttrial
According to the German version of CELEX-Database (Baayen beganimmediately.ThetrainingandthefMRI-paradigmforthis
et al., 1995), the frequency of object names did not differ study (described below) were programmed with Presentation(cid:3)R
betweenarousing-negativeandneutralconcepts,t(42)=–0.032, Software2 (Version12.1,NeurobehavioralSystems,Inc.,Albany,
p=0.975.Participantswhoperformedthepre-testratingdidnot CA,USA).
takepartinthemainexperiment. Explicit knowledge of all picture-pseudoword pairings was
assessed via cued-recall. Subjects were presented with the
Design andProcedure, Analysis pseudowords in written format (cues) and were asked to
During training, the subject’s task was to decide intuitively write down the corresponding Germanword (comparable with
by button-press whether a visually presented pseudoword and a translation or vocabulary test). The cued-recall test was
object (color picture) matched. Training stopped as soon as administered four times: directly after, 4 days after, 8 days
the participant reached criterion, that is, a predefined level after, and 12 days after learning. A pseudoword-valence rating
of knowledge concerning the pseudoword-picture associations assessed the transfer of valence from objects to pseudowords.
(this allowed for a balanced block-procedure in the fMRI- Subjects were asked to spontaneously and intuitively rate the
task; see below). Participants were not informed about the pseudowords in terms of valence, on a scale ranging from
1http://commons.wikimedia.org 2www.neurobs.com
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Edenetal. Memorybiasforarousing-negativewords
minus five (very negative) to five (very positive), with zero using a single-shot echo planar (EPI) sequence (whole brain
marked as neutral. The valence rating was administered five coverage, TE = 30 ms, TR = 2.5 s, FA = 90◦, slice thickness
times: directly before, directly after, 4 days after, 8 days after, 3.6 mm, interleaved acquisition order, no gap, matrix 64 × 64,
and 12 days after learning. Note that the last three cued-recall FOV 230 mm, in-plane resolution 3.6 mm × 3.6 mm). The
◦
testsandthelastthreevalenceratingswerecarried outonline3, 40 transversal slices were tilted 25 from the AC/PC line in
while allassessmentson thefirst daytookplace inthe Institute order to minimize drop out artifacts in the orbitofrontal and
for Biomagnetism and Biosignalanalysis (Faculty of Medicine, mediotemporalregion.
UniversityofMünster).Participantsreceivedwritteninstructions
but were not informed that their memory for the pseudowords Cued-RecallAnalyses
wouldbetested. Answers in the cued-recall test (translation of pseudowords
The fMRI measurement took place in the Department of into German) were treated as correct if they described the
ClinicalRadiology(FacultyofMedicine,UniversityofMünster) intended object (e.g., sofa), were synonyms (e.g., couch), or
2 days after the training, allowing for memory consolidation subordinate-category responses that were correct descriptions
through sleep (Payne and Kensinger, 2010, 2011; Bennion of the depicted object (e.g., chesterfield). Responses were
et al., 2013). The fMRI measurement used a block design, regarded incorrect if they described the superordinate category
with six blocks, crossing valence (arousing-negative, neutral) (e.g., furniture), semantically related objects (e.g., armchair),
with learning achievement(explicitly learned,lesswell-learned) or unrelated objects (e.g., scissors). Incorrect answers and
and two additional blocks with completely novel pseudowords. misses (no answer given) were excluded from further analyses.
Since learning outcome varied betweenparticipants (i.e.,which Means of correctly translated pseudowords were subjected
picture-word pairs a participant had learned), the respective to an ANOVA with the additional factor session, with four
blockswereindividuallyarrangedforeveryparticipant.Forthis levels (immediately after, 4, 8, and 12 days after). This
purpose, the pseudowords were divided into the eleven best, resulted in a 2 (pseudoword affect: arousing-negative versus
i.e., “explicitly learned” and the eleven remaining “less well- neutral)×4(session)×2(traitanxiety:highversuslow)mixed
learned” pseudowords, individually for each valence condition. within/betweendesign.
Thiswasdoneonthebasisofeachparticipant’sresultsfromthe
cued-recall test directly after training. The novel pseudowords, Valence-RatingAnalyses
taken from the corpus of Breitenstein and Knecht (2002), The factor sessionhad five levelsin the analysis of pseudoword
had not been used during training. Each block constisted of valence ratings: before, immediately after, 4, 8, and 12 days
11 pseudowords. The presentation format was the same as after training. Mean valence ratings were calculated for
during training. Each pseudoword was presented for 950 ms, arousing-negatively and neutrally linked pseudowords. With a
with a fixed interstimulus interval of 150 ms. The six blocks 2 (pseudoword affect) × 5 (session) × 2 (trait anxiety) mixed
(explicitly learned arousing-negative pseudowords, explicitly within/between design, the development of valence ratings was
learnedneutralpseudowords,lesswell-learnedarousing-negative investigatedovertime.
pseudowords, less well-learned neutral pseudowords, and two
blocks of novel pseudowords) were presented in a pseudo- ImageAnalysis
randomized order, to control for sequence effects. A 12500 ms The imaging data were analyzed with the Statistical Parametric
resting phase (white fixation cross centered on a black Mapping software4 (SPM8, Wellcome Department of
screen) followed each block. Each block was presented twice, Cognitive Neurology, London, UK) implemented in Matlab
resulting in 26 instances in each learning condition, and 52 (Mathworks Inc., Natick, MA, USA). Preprocessing included
instances of novel pseudowords. In all, the paradigm took unwarping, realignment and normalization to the standard
approximately 9 min. The stimuli were projected onto a MNI space (Montreal Neurological Institute). Smoothing
screen at the rear end of the MR tunnel, using a beamer was conducted with an isotropic three-dimensional Gaussian
shielded against RF interference. Participants were instructed filter with a Gaussian kernel of 6 mm full width at half
to read the words attentively. No further instruction was maximum (FWHM). Afterward, on the first level, we
given. applied a general linear model to the data (modeled with
thecanonicalhemodynamicresponsefunction).Theconditions
Image Acquisition were: explicitly learned arousing-negative, explicitly learned
Magnetic resonance imaging scanning was performed on neutral, less well-learned arousing-negative, less well-learned
a 3 T whole-body scanner (Gyroscan Intera T3.0, Philips neutral, and novel. The eight contrasts of interest were:
MedicalSystems,Best,Netherlands)equippedwithQuasarDual (1) Explicitly learned pseudowords vs. novel pseudowords,
gradients (nominal gradient strength in the setting used for (2) Less well-learned pseudowords vs. novel pseudowords, (3)
fMRI 40 mT/m, maximal slew rate 200 mT/m/ms). For spin Arousing-negative pseudowords vs. neutral pseudowords, (4)
excitationandresonancesignalacquisition,acircularlypolarized Explicitly learned arousing-negative pseudowords vs. less well-
transmit/receivebirdcageheadcoilwithanHFreflectingscreen learned arousing-negative pseudowords, (5) Less well-learned
∗
at the cranial end was used. T2 functional data were acquired arousing-negative pseudowords vs. less well-learned neutral
3http://www.limesurvey.org/ 4www.fil.ion.ucl.ac.uk/spm
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Edenetal. Memorybiasforarousing-negativewords
pseudowords, (6) Less well-learned neutral pseudowords vs. traitanxietyinthecontrastsdefinedabove.Voxelwisetestsinside
novel pseudowords, (7) Less well-learned arousing-negative theROI wereperformed andactivitywithin theamygdalaewas
pseudowords vs. novel pseudowords. (8). Neutral pseudowords correlatedwithSTAI-T(traitanxiety)scoresseparatelyforeach
vs. novelpseudowords. These contrasts were also analyzed in a subject.
second analysis,taking into account the individualtrait anxiety
scoreasacovariate(regressionanalysis).Pleasenotethatdueto
the criterion-based designandthe differentiation into explicitly Results
learnedandlesswell-learnedwords,therearetothebestofour
knowledge no (fMRI) studies with a comparable orientation. Cued-Recall
Thus,the contrastsinvestigatingsuchdifferences(i.e.,contrasts Figure 1 displays the recall rates (correct translation)
2,5,and6)aremoreexploratoryinnature. immediately after, 4, 8, and 12 days after training, for
To control for multiple testing on the second level (group) both participant groups and pseudoword affects. Note that
random-effects analysis, all group results were calculated using performance isdisplayed in percentage correct, while statistical
acombinedheightandextentthresholdbasedonMonte–Carlo analyses were done on absolute values (maximum = 44). As
simulations,asimplementedintheAlphaSimprogram(Forman expected,the briefandshallowtraining yieldedmoderaterecall
etal.,1995).Basedonthistechnique,wemaintainedacorrected results. These were highest in the first session immediately
false-positive detection rate for the amygdala, our region of after training (about 25% correct translations), decreased to
interest (ROI) analysis, at p < 0.05, with a cluster extent (k) around 15% correct translations by the second session 4 days
empiricallydeterminedbycomputing1000simulations(yielding later, but remained stable in session three and four (8 and
k=45forthebilateralamygdala). 12daysafterlearning).Themaineffectofsessionwassignificant:
According to our hypotheses, ROI analyses of the bilateral F(3,96) = 50.655; p < 0.001, and is best explained by a linear
amygdalawereperformedforallcontrastsbyone-samplet-tests, effect:F(1,32)=56.493;p<0.001.Overall,pseudowordslinked
including allindividualcontrast mapsofthe first level.Forthis witharousing-negativepictureswererecalledsignificantlybetter
purpose,amaskforthebilateralamygdalawascreatedwiththe thanneutrallylinkedones,whichisreflectedinamaineffectfor
aid of the WFU PickAtlas (Maldjian et al., 2003) implemented pseudoword affect, F(1,32) = 4.347; p = 0.045. The three-way
in the SPM-software. The defined mask was dilated (according interaction betweenpseudoword affect,session,andtraitanxiety
to the AAL Atlas (Tzourio-Mazoyer et al., 2002) by 1 mm in alsoreachedsignificanceF(3,96)=6.523;p=0.013.
radius. The regression analysis tested our a priori hypothesis Additional ANOVAS (word affect × session), separately
concerningtherelationbetweenamygdalaactivityanddegreeof for each group, further investigated this interaction. The
FIGURE1|Percentageofcorrectresponsesinthecued-recalltest,forfoursessions(1=immediately,2=4days,3=8days,and4=12daysafter
training),forhigh-anxiety(Upper)andlow-anxiety(Lower)participants.Pseudowordspairedwitharousing-negativecontentarepresentedingraybars;
neutrallylinkedpseudowordsindashedbars.Errorbarsrepresents1SE.
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Edenetal. Memorybiasforarousing-negativewords
data of the low-anxious group showed a main effect of fMRI Results
session F(3,48) = 22.690; p < 0.001, and the interaction RegionofInterestAnalysisRegardingAmygdala
pseudoword affect × session, F(3,48) = 8.843; p = 0.005. The ResponsivenesstoPseudowords
main effect of pseudoword affect did not reach significance
With contrasts one and two, we investigated a general learning
F(1,16) = 1.652; p = 0.217. Post hoc t-tests calculated to assess
effect. As expected, in contrast 1, explicit pseudowords elicited
theinteractionyieldedasignificantdifferencebetweenarousing-
more amygdala activity than novel pseudowords, bilaterally
negative(Mean=11.06,SD=5.910)andneutralpseudowords x = 31, y = −10, z = −14, t(33) = 2.26, k = 56 voxels,
(Mean = 9.29, SD = 5.565) at session one [t(16) = 2.624; p = 0.015 corrected. Contrast 2 was not significant, showing
p = 0.018]. No other session showed such a difference (all
similaramygdalaactivityforlesswell-learnedpseudowordsand
p > 1.444). The data for the high-anxious group also yielded
novelpseudowords.Contrast3testedforeffectsofpseudoword
a main effect of session: F(3,48) = 28.448, p < 0.001. No
affect, independent of learning success. As expected, arousing-
other main effects or interactions reached significance [word
negative pseudowords elicited more amygdala activity than
affect: F(1,16) = 2.698; p = 0.120 and word affect × session: neutrally linked pseudowords x = −22, y = −8, z = −9,
F(3,48)=0.255;p=0.857]. t(33) = 3.19, k = 108, p = 0.002 corrected. Contrast 4
tested for effects of explicit learning. There was no difference
Pseudoword ValenceRating
in amygdala activity between explicitly learned and less well-
Figure 2 displays the mean valence ratings separately for
learned arousing-negative pseudowords. With contrasts five
participant groups and pseudoword affect, in all five sessions.
to seven, effects of acquired affect were investigated for
The ANOVA with session, pseudoword affect, and trait anxiety
yielded no main effect of pseudoword affect, F(1,32) = 1.872; pseudowords that are not well learned or remembered. As
expected (and in line with contrast 3), contrast 5 showed
p = 0.506. The rating behavior toward a more negative rating
that arousing-negative pseudowords elicited more bilateral
changed significantly over time, indicated by a main effect of
amygdala reactivity than neutral pseudowords x = −30,
session F(4,128) = 10.335; p < 0.001, best described as a linear
trend, F(1,32)= 7,823;p = 0.009. Although the meanssuggest y = 4, z = −14, t(33) = 2.45, k = 71, p = 0.010.
However, contrast 6 (less well-learned neutral pseudowords vs.
a difference between negative and neutral pseudowords for the
novel words), contrast 7 (less well-learned arousing-negative
high-anxietygroup,noothermaineffectsorinteractionsreached
pseudowords vs. novel pseudowords) and contrast 8 (neutral
significance.(Note:AnANOVAonthesamevalencedatawhere
pseudowords vs. novel pseudowords) did not yield significant
ratings of the first session were subtracted from ratings given
results. (See Table 1 for a clear arrangement of all results
at the second and third session (baseline correction), yielded
above).
qualitativelythesameresults.)
FIGURE2|Meanvalenceratingsforfivesessions(0=beforetraining,1=immediately,2=4days,3=8days,and4=12daysaftertraining),and
forhigh-anxiety(Upper)andlow-anxiety(Lower)participants.Pseudowordspairedwitharousing-negativecontentarepresentedingraybars;neutrallylinked
pseudowordsindashedbars.Errorbarsrepresents1SE.
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Edenetal. Memorybiasforarousing-negativewords
TABLE1|Regionofinterestanalysisregardingamygdalaresponsivenesstopseudowords.
Contrast T MNI-coordinates Cluster(k) p
x y z
1 Explicitlylearnedpseudowordsvs. 2.26 31 −10 −14 56 0.015
novelpseudowords
2 Lesswell-learnedpseudowordsvs. − − − − Nosignificantclusters –
novelpseudowords
3 Arousing-negativepseudowordsvs. 3.19 −22 −8 −9 108 0.002
neutralpseudowords
4 Explicitlylearnedarousing-negative − − − − Nosignificantclusters –
pseudowordsvs.lesswell-learned
arousing-negativepseudowords
5 Lesswell-learnedarousing-negative 2.45 −30 4 −14 71 0.010
pseudowordsvs.lesswell-learned
neutralpseudowords
6 Lesswell-learnedneutralwordsvs. − − − − Nosignificantclusters −
novelwords
7 Lesswell-learnedarousing-negativevs. − − − − Nosignificantclusters −
novelwords
8 Neutralwordsvs.novelwords 2.43 38 4 −23 8(clusterbelowAlphaSim 0.010
correctionlevel)
Conductedatp<0.05,uncorrected(correctedatp<0.05ontheclusterlevelusingtheAlphaSimprocedure,whichresultedinanempiricallydeterminedcluster-extent
thresholdofk=45voxels).CoordinatesaregiveninMNIspace.
Trait AnxietyasCovariate than neutral pseudowords, and this was positively related to
The ROI-analysis of the bilateral amygdala with trait anxiety trait anxiety. As in the analysis without covariate, contrast
as covariate revealed a significant contrast 1 (explicitly learned 4 (explicitly learned arousing pseudowords vs. less well-
pseudowords vs. novel pseudowords, see Figure 3). Explicitly learned arousing pseudowords) was not significant. Contrast 5,
learned pseudowords elicited more amygdala activity than comparingarousing-negativeandneutralpseudowordsthatwere
novel pseudowords in the bilateral amygdala, and this effect not learned well, was significant x = 32, y = −7, z = −9,
was positively related to measures of trait anxiety x = 32, t(32) = 2.16, k = 47 voxels, p = 0.019. The arousing-negative
y = 5, z = −21, t(32) = 2.62, k = 111 voxels, p = 0.007. pseudowordselicitedmoreamygdalareactivitythantheneutral
Importantly, and contrary to the analysis without covariate, pseudowords, again, positively related to measures of trait
contrast2(lesswell-learnedpseudowordsvs.novelpseudowords) anxiety. Contrast 6 (less well-learned neutral pseudowords vs.
also yielded significant results x = 31, y = 2, z = −19, novel pseudowords), however, was not significant. But contrast
t(32) = 2.42, k = 77 voxels, p = 0.011, positively related to 7 (less well-learned arousing-negative pseudowords vs. novel
trait anxiety. Contrast 3 (arousing-negative pseudowords vs. pseudowords) and contrast 8 (neutral pseudowords vs. novel
neutral pseudowords) was also significant x = 34, y = −7, pseudowords),werehighlysignificant(contrast7:x=31,y=0,
z = −11, t(32) = 2.74, k = 55 voxels, p = 0.005. Hence, z = −23, t(33) = 3.25, k = 207 voxels, p < 0.001; contrast 8:
arousing-negative pseudowords elicited more amygdala activity x=31,y=4,z=−19,t(32)=3.39,k=116voxels,p<0.001.
FIGURE3|Coronal,sagittalandaxialviewdepictingactivationextensionofoneexamplecontrast;supra-thresholdvoxelsareshowninred.Region
ofinterest(ROI)-analysiswithtraitanxietyasacovariateforthebilateralamygdala;contrast1:Explicitlylearnedpseudowords>novelpseudowords(x=32,y=5,
z=−21).
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Edenetal. Memorybiasforarousing-negativewords
Hence, pseudowords that were less well learned elicited more Most interestingly, this hyperactivation was more pronounced
amygdalareactivitythannovelpseudowords,independentofthe in high-anxious persons, replicating previous behavioralresults
linked affect. This was positively related to measures of trait (Edenetal.,2014).Theeffectwasnotrestrictedtopseudowords
anxiety. See Table 2 for an overview of all regression analysis thatparticipantscouldexplicitlyremember.Infact,itseemsthat
results and Figure 3 for a visualization of the spatial extension the amygdala of high trait-anxious persons reacted sensitively
ofamygdalaactivationofcontrast1. to all stimulus material, an indication for generalization.
Note thatthe significant contrasts showed clusterwithin the Note, however, that the behavioral data showed no general
amygdala’sVOIsaftercorrectionformultipletesting(seeTables1 enhancement for negative-arousing over neutral pseudowords
and2).Subnucleioftheamygdalacouldnotbedistinguishedby forhigh-anxious individulas,noteveninsessionone,wherewe
ourmethods. saw an effect for low-anxious persons. Moreover, and against
our expectation, there were no significant changes in memory
bias from session two onward. The latter two findings stand in
Discussion contrasttoourearlierstudy(Edenetal.,2014).Wewilldiscuss
eachoftheseaspectsinturn.
We analyzed the development of a memory bias for novel Asexpected,veryfew(i.e.,sixtonine)correct andincorrect
and neutral stimuli before and after a learning phase, during pairings in an associative learning paradigm resulted in a
whichthepseudowordswerepairedwithpictureswitharousing- memory bias for pseudowords that were paired with negative-
negativeorneutralcontent.Highandlowtraitanxiouspersons arousing pictures. This, once again, shows the effectiveness of
participated. Our results demonstrate that a brief training in thisparadigmforword learning(Dobeletal.,2009,2010;Eden
an associative learning paradigm suffices to elicit a memory etal.,2014).Afterlearningparticipantsshowedamemorybiasin
bias for those pseudowords that were combined with arousing, the cued-recall test. Thus, all participants, independent of their
negativepictures,comparedtothosethatwerelinkedtoneutral level of trait anxiety, were better able to translate pseudowords
pictures. This bias became evident in behavioral as well as that had been combined with arousing-negative content than
in fMRI measures. A cued-recall translation test, administered pseudowordslinkedwithneutralcontent.Thisreplicatesearlier
directly after and at four 4-day-intervals following training, findings,whereparticipantswerebetterabletomemorizestimuli
showed better recall for pseudowords that had been combined with aversive emotional content (e.g., Mitte, 2008). Here, as in
with arousing-negative content. However, the valence ratings our earlier work (Eden et al., 2014), we observe this advantage
showed no differences between arousing-negative and neutral even after a very brief associative training. However, the same
pseudowords.ThefMRImeasurementthattookplace2daysafter effectwasnotfoundinthe(implicit)valencerating.Participants
learningshowedahyperactivationoftheamygdalainresponseto ratedarousing-negativepseudowordsmorenegativethanneutral
thearousing-negativepseudowords,indicatingthatthesestimuli ones,butthisdifferencedidnotreachsignificance(seeFigure2).
were processed differently from neutrally linked pseudowords. Thus, participants showed an explicit but no implicit memory
TABLE2|Regressionanalysiswithtraitanxietyascovariate.
Contrast T MNI-coordinates Cluster(k) p
x y z
1 Explicitlylearnedpseudowordsvs. 2.62 32 5 −21 111 0.007
novelpseudowords
2 Lesswell-learnedpseudowordsvs. 2.42 31 2 −19 77 0.011
novelpseudowords
3 Arousing-negativepseudowordsvs. 2.74 34 −7 −11 55 0.005
neutralpseudowords
4 Explicitlylearned − − − − Nosignificantclusters −
arousing-negativepseudowordsvs.less
well-learned
arousing-negativepseudowords
5 Lesswell-learnedarousing-negative 2.16 32 −7 −9 47 0.019
pseudowordsvs.lesswell-learned
neutralpseudowords
6 Lesswell-learnedneutralwordsvs. − − − − − −
novelwords
7 Lesswell-learnedarousing-negativevs. 3.25 31 0 −23 207 <0.001
novelwords
8 Neutralwordsvs.novelwords 3.39 31 4 −19 116 <0.001
Conductedatp<0.05,uncorrected(correctedatp<0.05ontheclusterlevelusingtheAlphaSimprocedure,whichresultedinanempiricallydeterminedcluster-extent
thresholdofk=45voxels).CoordinatesaregiveninMNIspace.
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Edenetal. Memorybiasforarousing-negativewords
bias. This isin line with the resultsof a meta-analysis by Mitte cued-recall data of the current study. Of interest is whether
(2008), who indeed showed that implicit memory effects are this neural correlate for a memory bias is driven solely by
seldom found. Some authors even question the existence of an the explicitly recalled items. This, as contrast 4 showed, was
implicit memory bias (e.g., McCabe, 1999; Russo et al., 1999). not the case: Explicitly learned and less well-learned arousing-
An explanation why explicit tests yield the memory bias but negative pseudowords elicited equal amygdala reactivity. This
the implicit ones do not, could be as follows. According to clearlygoesagainstthesuggestionthatnothingislearnedwhen
Scott et al. (2009), valence features are part of the semantic stimuli cannot be recalled explicitly. Clearly, aversive stimuli
representation of words. Hence it can be assumed that the have similar amygdalar effects, independent of their level of
activation of such features is required in explicit tasks such as explicit recall. To explore this further, we contrasted less well-
cued-recall. In this task, participants had to perform a one-to- learnedarousing-negativeandneutralpseudowords(contrast5),
one mapping of a pseudoword to an existing German word. andobservedmoreamygdalareactivityforthearousing-negative
In contrast, an implicit task such as the valence rating applied stimuli.Thiscorroboratestheabovefindingthataffectisindeed
heredoesnotrequiretheactivationofGermanwords,withtheir acquiredforthesepseudowords,eventhoughparticipantscould
semantic and valence features. This may explain why implicit not explicitly translate these words very well. These findings
memory bias effects for words are so much harder to detect corroborate the observed amygdala sensitivity for emotionally
than explicit ones. Note that we did obtain implict bias effects arousingstimuli–evenintheabsenceofexplicitmemory(e.g.,
in our earlier study (Eden et al., 2014), which had more power Dannlowski et al., 2007a,b; Pichon et al., 2012; Suslow et al.,
in terms of items and partipants. The missing effect in the 2013). Note, however, that the overall amygdala activation of
valence rating might at first glance invite to speculate about these less well-learned pseudowords did not differ from the
the processing depth of learned words and seems to suggest a activationforcompletelynovelpseudowords.Thiscontrastwas
shallow encoding. However, results of former studies from our thus only significant for explicitly learned stimuli. There is
groupthatusedverysimilarassociativeword-learningparadigms ample evidence that completely novel stimuli are processed
(e.g., Breitenstein et al., 2007; Dobel et al., 2009, 2010; Liuzzi differently from items that have been seen before. Repetition
et al., 2010) strongly suggest that meaning is indeed acquired decreases amygdala activity, and only explicitly learned and
for the pseudowords. Breitenstein et al. (2007) showed with recalledstimuliovercomethisrepetitionsuppression(e.g.,Ishai
crossmodal priming that learned pseudowords primed existing et al., 2004; Wendt et al., 2011). Finally, contrast 8 was
wordsrelatedtotheiracquiredmeaningaseffectivelyasnative- implemented to investigate effects of generalization, comparing
language words. This was corroborated by Dobel et al. (2010), all neutrally linked pseudowords (explicitly and less well-
whoappliedmagnetencephalography(MEG).Theyshowedthat learned) with all novel pseudowords. Both conditions elicited
the N400 component [an indicator for semantic (mis)matches about equal amygdala activity. This provides no evidence for
betweenwordandpicture]topictureswasstronglyreducedwhen generalization.Neutralwordswerenotassociatedorconfounded
they were preceded by pseudowords whose acquired meaning withnegativeaffect,andthatthehyperactivationoftheamygdala
correspondedtothepicturedconcept.Basedontheseandother for arousing-negative pseudowords was indeed due to this
findings,wefeelconfidentthatthelearningeffectsfound inthe negativeaffect.
presentstudytrulyreflectsemantic/emotionallearning,andthat The second fMRI-analysis, with the factor trait anxiety as
the pseudowords do not simply present superficial mnemonic a covariate, revealed the following. As expected and as in the
cuestoexistingwordsand/orcorrespondingpictures. firstfMRI-analysis,explicitlylearnedpseudowordselicitedmore
We now turn to the fMRI data, for which we carried amygdala reactivity than novel pseudowords in the bilateral
out two analyses: the first analysis served to investigate the amygdala, and this effect was positively related to measures
general effect of memory bias, and the second to additionally of trait anxiety. The effect increases with increasing levels
assess the influence of trait anxiety. With respect to the first of trait anxiety, showing that persons with higher levels of
analysis, we observed general effects of learning. Explicitly trait anxiety process stimuli, gathered in emotionally arousing
learnedpseudowordselicitedmoreamygdalaactivitythannovel situations, differently from persons with low levels of anxiety
pseudowords,showingthatonlyfewrepetitionsofpseudoword- (e.g., Tolkunov et al., 2010; Asakawa et al., 2014; Burgess
picture pairssufficedtoactivatetheamygdala,even2daysafter et al., 2014). Different from analysis one, the contrast was
learning.Thisamygdalarhyperactivationwasseenforexplicitly also significant for less well-learned pseudowords vs. novel
learnedpseudowordsonly,notforthesetof “notsowelllearned” pseudowords. This lends support to the amygdala’s sensitivity
pseudowords (the worst 11 for each participant). This suggests (i.e.,hyperreactivity)inpersonswithhighlevelsoftraitanxiety.
that they either were not learned at all, or that their superficial Contrast 3 investigated the occurrence of a memory bias. As
learning history leads to different processing or storage – expected and as in analysis one, the arousing-negatively linked
evident in explicit recall and amygdala reactivity. The third pseudowordselicited more amygdalaactivitythantheneutrally
contrastinvestigatedpseudowordaffect,morepreciselywhether linked pseudowords, supporting similar prior studies (Laeger
arousing-negativepseudowordsgenerallyelicitedmoreamygdala etal.,2012,2014a,b).Contrast4,comparingtheexplicitlyandless
activity than neutralones. Importantly, this was the case,when well-learned arousing-negative pseudowords, was–again–not
lookingforexplicitlyandlesswelllearnedpseudowordstogether. significant.Thus,evenwhentakingintoaccountthetraitanxiety
Thiseffectcorroborates thememorybiasfoundinpriorstudies levels, the amygdalae of our participants did not differentiate
(for a review, see Mitte, 2008) and the main effect in the betweenexplicitlyandlesswell-learnedpseudowordswhenboth
FrontiersinPsychology|www.frontiersin.org 10 August2015|Volume6|Article1226