ORIGINAL RESEARCH ARTICLEpublished: 01 February 2013

doi: 10.3389/fnbeh.2013.00002

Aging-related episodic memory decline: are emotionsthe key?Kiyoka Kinugawa1,2,3†, Sophie Schumm3†, Monica Pollina1,2,3, Marion Depre1,2,3, Carolin Jungbluth4,

Mohamed Doulazmi1,2, Claude Sebban1,2,3, Armin Zlomuzica5, Reinhard Pietrowsky 4, Bettina Pause4,Jean Mariani1,2,3 and Ekrem Dere1,2,3*

1 Neurobiologie des Processus Adaptatifs, UMR 7102, Université Pierre et Marie Curie, Paris 6, Paris, France2 CNRS, UMR 7102, Paris, France3 Institut de la longévité, AP-HP Hôpital Charles Foix, Ivry-sur-Seine, Paris, France4 Institute of Experimental Psychology, University of Düsseldorf, Düsseldorf, Germany5 Center for the Study and Treatment of Mental Health, Ruhr-Universität Bochum, Bochum, Germany

Edited by:

Hans J. Markowitsch, University ofBielefeld, Germany

Reviewed by:

Armelle Viard, Inserm-EPHE-UCBNU1077, FranceAlexander Easton, DurhamUniversity, UK

*Correspondence:

Ekrem Dere, Neurobiologie desProcessus Adaptatifs, UMR7102, Université Pierre et MarieCurie, Paris 6, 9 quai St. Bernard,Paris F-75005, France.e-mail: ekrem.dere@snv.jussieu.fr†These authors equally contributedto this work.

Episodic memory refers to the recollection of personal experiences that containinformation on what has happened and also where and when these events took place.Episodic memory function is extremely sensitive to cerebral aging and neurodegerativediseases. We examined episodic memory performance with a novel test in young (N = 17,age: 21–45), middle-aged (N = 16, age: 48–62) and aged but otherwise healthy participants(N = 8, age: 71–83) along with measurements of trait and state anxiety. As expected wefound significantly impaired episodic memory performance in the aged group as comparedto the young group. The aged group also showed impaired working memory performanceas well as significantly decreased levels of trait anxiety. No significant correlation betweenthe total episodic memory and trait or state anxiety scores was found. The present resultsshow an age-dependent episodic memory decline along with lower trait anxiety in theaged group. Yet, it still remains to be determined whether this difference in anxiety isrelated to the impaired episodic memory performance in the aged group.

Keywords: aging, anxiety, episodic memory, depression, working memory

INTRODUCTIONEpisodic memory refers to the conscious recollection of apersonal experience that contains information on what has hap-pened and also where and when it happened (Tulving, 1983).Remembering a personal experience might also be accompa-nied by the remembrance of specific perceptions, emotions, andthoughts one had during a particular experience (Tulving, 2002).Episodic memory deficits are observed after medial temporal lobeinjury (Nyberg et al., 1996) which includes important memorystructures such as the hippocampus (Burgess et al., 2002) andamygdala (Markowitsch and Staniloiu, 2011) but also after lesionsto the frontal cortex (Kirchhoff et al., 2000) and diencephalicstructures, such as the mediodorsal thalamus and the mammillarybodies (Tsivilis et al., 2008; Wolff et al., 2008).

Episodic memory function is also extremely sensitive to cere-bral aging (Shing et al., 2010; Nyberg et al., 2012), neurode-generative (Williams-Gray et al., 2006; Dubois et al., 2007), andpsychiatric diseases (Dere et al., 2010). Cross-sectional studieshave indicated that the age-dependent decline in episodic mem-ory function starts as early as at the age of 30 (Park et al., 2002),while longitudinal studies propose a later onset between ages 65and 70 years (Rönnlund et al., 2005). Age-dependent memorydecline seems to be paralleled by volume reductions in brainstructures important for memory performance, including themedial temporal lobe (Persson et al., 2006), the hippocampus(Rajah et al., 2010), and the prefrontal cortex (Van Petten et al.,

2004). Although, it is well known that the amygdala, besides itsprominent role in the generation of emotions, is also involvedin memory consolidation after fear conditioning (LeDoux, 2007)and emotional events (McIntyre et al., 2003; McGaugh, 2004), itsrole during age-dependent memory decline has attracted surpris-ingly fewer research activity.

The role of emotions in the decline of episodic memory func-tion that is seen in the course of physiological aging is still poorlyunderstood. Although emotions are not necessarily an integralcomponent of episodic memory, emotional arousal, or psychoso-cial stress induced in the laboratory during the encoding ofepisodic information can facilitate episodic memory consolida-tion into long-term memory (Wolf, 2012).

It has been also proposed that emotions might be a triggerfor episodic memory formation (Libkuman et al., 2004; Dereet al., 2010; Kensinger et al., 2011), play a role in the bind-ing of different features of an event into an integrated episodicmemory (Nashiro and Mather, 2011), mediate the self-relevantaspect of an episodic memory (Wheeler et al., 1997) and mightalso determine their durability in a way that strong emotionalactivation leads to long-durable episodic memories, while weakemotional activation leads only to short-durable episodic mem-ories (Dere et al., 2010). In line with this proposition it hasbeen found that emotions improve the ability of aged individ-uals to retrieve more details of an event as well as its context(Kensinger, 2009). There is also evidence suggesting that the

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Kinugawa et al. Episodic memory, aging, and emotion

processing of emotional stimuli and the physiological arousalmediated by the autonomic system in response to emotionallynegative stimuli is compromised in aged individuals (Kaszniakand Menchola, 2012). In this study, we investigated the possibil-ity that aging-induced episodic memory decline might be due tochanges in emotionality e.g., in terms of the response to stimulithat have been associated with an emotionally arousing contextstory.

In order to test the emotionality hypothesis of aging-inducedepisodic memory impairments, we measured episodic memory inyoung, middle-aged, and aged participants with a novel paradigmwhich measures memory for different stimuli, the temporal orderof their presentation as well as the spatial locations where theyhave been presented. This test also measures the ability to estab-lish new episodic memories. We further assessed trait and stateanxiety in the 3 groups in order to determine if impairmentsin episodic memory performance are indeed correlated withdecreased levels of trait and/or state anxiety.

Given that depressive symptoms are common in the aged pop-ulation and are associated with cognitive impairments includingworking memory deficits (Bornstein et al., 1991; Nebes et al.,2000) we additionally probed whether aging-induced episodicmemory decline would be associated with impairments in work-ing memory or depressive symptoms.

MATERIALS AND METHODSPARTICIPANTSForty-one healthy adult volunteers (♀ = 22, ♂ = 19) partic-ipated in this study. The participants were recruited fromUniversity Pierre and Marie Curie Paris 6 students and employ-ees and among healthy relatives of patients attending the geriatrichospital Charles Foix in Ivry-Sur-Seine, France. The participantswere aged between 21 and 83 years. They were divided into threegroups of young (N = 17, mean: 26.76 ± 1.69, age range: 21–45),middle-aged (N = 16, mean: 55.31 ± 1.06, age range: 48–62)and aged participants (N = 8, mean: 79.13 ± 1.33, age range:71–83).

None of the participants reported a psychiatric record, his-tory of vascular, psychiatric, neurological, motor or oncologicdisease, psychopharmacologic or hormonal therapy or any otherhealth issue that would prohibit their testing. All participants hada corrected to normal vision and audition.

The groups were comparable regarding their socio-demographic and educational background. The study wasconducted in accordance with the declaration of Helsinki.Written informed consent was obtained from all participants.All experimental procedures have been approved by the localethical committee of the University Pierre and Marie CurieParis 6.

EXPERIMENTAL DESIGNIn a reverse translational approach by Pause et al. (2010) the ratio-nale and principles of the episodic-like memory test for rodents(Dere et al., 2005a,b; Kart-Teke et al., 2006) have been adaptedto humans. We developed a paradigm that measures the spatio-temporal memory for emotional and neutral pictures presentedon an eight-quadrant computer-screen task (Pause et al., 2010).

This test has been further developed to be applicable to agedindividuals and patient populations.

General procedureThe total experiment including the presentation of general infor-mation about the experiment, the completion of the participantquestionnaire, the neuropsychological testing as well as theepisodic memory test had a total duration of approximately 2.5 h.However, the net time of testing was approximately 65 min. Theparticipants received 3 pauses of 2 × 20 min and 1 × 45 min inthe course of the 2.5 h total duration in order to minimize pos-sible effects of tiredness and fatigue on test performance in theolder individuals. Figure 1 gives overview of the different phasesof the experiment, their sequence, and the approximate durationof each test.

First the participant was informed about the general proce-dure of the experiment without providing an explicit statementthat he or she is participating in a memory experiment orhad to retain the information presented during the course ofthe experiment. It is important to note that no explicit infor-mation about the purpose of the test was given. Instead theparticipants were informed that “The aim of this study is toinvestigate the effects of imagination on visual perception andattention.” Thereafter, the participants were asked to completea standard participant questionnaire including questions aboutthe current and past health status, current and past medica-tion, history of mental diseases, etc. After that the participantsworking memory for series of numbers was tested using asubtest of the WAIS-R. Immediately thereafter the participantsperformed the episodic memory test consisting of 3 slide pre-sentations followed by an episodic memory test as described indetail below. Immediately after the third slide presentation, theparticipants were asked to complete the state anxiety subtestof the STAI (Spielberger et al., 1970). Finally, after the partic-ipants had completed the episodic memory test, the Goldbergtrait anxiety, and depression scale was performed (Goldberg et al.,1988).

THE EPISODIC MEMORY TESTThis test is based on the “what, where, and when” paradigm(Clayton and Dickinson, 1999; Dere et al., 2005a) that allows tomeasure the core elements (content, temporal, and spatial con-text of an unique event) of episodic memory. The present testis designed to measure integrated memories for “what, where,and when” operationalized as “stimulus-position-trial” associa-tions. The test does not allow the assessment of the individualcomponents of episodic memory in terms of content, spatial, andtemporal order memory.

Each participant received 3 presentation trials using thePresentation® software Version 12 (Neurobehavioral Systems,CA, USA) and an episodic memory test (recall of 27 differentstimulus-position-trial associations). The 3 trials were embed-ded into a context story (see below) with emotional content.This context story was divided into 3 parts according to the 3trials. Each part of the context story was narrated by the exper-imenter to the participant immediately before the presentationof the corresponding presentation trial. Each presentation trial

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FIGURE 1 | Experimental design. Overview of the experimental design, the order of tests applied, presentation times of the slides, and the approximateduration of each experimental phase.

consisted of 12 slides. Each slide was presented for 8 s and wasfollowed by the presentation of a fixation cross for 2 s. Thefirst slide showed a background scene with an empty place sur-rounded by shops (Figure 2A). This place was virtually dividedinto a 3 × 3 matrix with 9 different positions for the presenta-tion of stimuli (Figure 3C). The center position was not usedfor the presentation of stimuli. The second slide consisted ofthe same background scene including 4 context story-relevantand 4 context story non-relevant stimuli presented within the3 × 3 matrix (Figure 2B). Context story-relevant stimuli weredrawings of 4 men wearing suits and having slightly differ-ent postures (Figure 2B). Stimuli not relevant to the contextstory consisted of drawings of 4 pigeons (Figure 2B). Duringthe slides 3–10 each stimuli position was presented individuallyfor 8 s while the reminder of the background scene includingthe other stimuli were darkened (Figures 2C,D). Each slide wasfollowed by the presentation of a gray slide for 2 s showing aplus-shaped fixation cross at the center. This slide ensured thesaccadic resetting of the participants view back to the centerof the slide before the next individual position was presented.Slide 11 again presented the complete scene including context

story-relevant and non-relevant stimuli. This slide was followedby the presentation of the background scene without stimuli.After a delay of 20 min the second presentation trial was per-formed. This was identical to the first trial, except that draw-ings of women were presented instead of men (Figures 2E,F).Two of the context story-relevant stimuli (women) were pre-sented at positions already used during the first trial for theplacement of context story-relevant stimuli (men), while theremaining 2 context story relevant stimuli were placed atpositions which contained context story non-relevant stimuli(pigeons).

After another delay of 20 min the participants viewed the thirdpresentation trial (Figure 3A). The third trial was identical to thefirst 2 presentation trials except that the 4 context story-relevantstimuli consisted of 2 men (in the following referred to as “old”stimuli with respect to the temporal order of the 2 previous tri-als) and 2 women “recent” stimuli. Additionally one “old” andone “recent” stimuli were presented at a position which was notused for the placement of context story-relevant stimuli dur-ing their initial presentation. Thus one “old” and one “recent”stimuli had been displaced to a “novel” position. These stimuli

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FIGURE 2 | The episodic memory test: presentation trials 1 and 2. Eachpresentation trial is composed of a series of 12 slides. Each slide is presentedfor 8 s and is followed by the presentation of a fixation cross for 2 s.Schematic drawings of men (presentation trial 1) or woman (presentationtrial 2) are used as context story-relevant stimuli while pigeons are used ascontext story-non relevant stimuli. (A) The first slide of each presentation trialshows the background scene without context story-relevant and non-relevantstimuli. (B) Presentation of the 8 positions with 4 men as context

story-relevant stimuli on the second slide of trial 1. (C) Example for thepresentation of a single man-position stimulus during the presentation of theslides 3–10 on trial 1. (D) Example for the presentation of a singlepigeon-position stimulus during the presentation of the slides 3–10 on trials1 or 2. (E) Presentation of the 8 positions with 4 women as contextstory-relevant stimuli on the second slide of trial 1. (F) Example for thepresentation of a single women-position stimulus during the presentation ofthe slides 3–10 on trial 2.

were referred to as “old displaced” and “recent displaced” stimuli(Figure 3B).

Sixty minutes after the third trial the episodic memory testwas performed. Here, the participants were asked to recall each ofthe 27 stimulus-position-trial associations that have been formedduring the 3 presentation trials. The sequence of memory tests forthe 3 presentation trials was 3-1-2. First the 9 stimulus-position-trial associations of trial 3 were tested, followed by the tests fortrials 1 and finally 2. During the test the participant was pre-sented with the background scene without context story-relevantor non-relevant stimuli. The place was divided into a matrix of9 positions.

Each episodic memory test for individual trials (1, 2, or 3)consisted of 18 slides. Each individual position, marked withred color, was presented for 2 s (Figure 3C). Thereafter, a slideappeared asking whether the participant remembered to have

seen an empty place, a pigeon, a woman, or a man at this posi-tion during that particular trial. On the bottom of this slide the4 choice options were presented as images. The participant couldselect the right answer by clicking on the corresponding stimuli(Figure 3D). The slide was presented until the participant madea decision. The responses of the participant were automaticallyrecorded and transferred to an Excel® output file. Please note thatthis procedure allowed the measurement of a memory for what,where, and when in terms of stimulus-position-trial associationswith a minimum of verbal requirements allowing the testing ofpatients with impairments in speech production.

CONTEXT STORYThe context story was divided into 3 parts which were narrated bythe experimenter before each presentation trial and had an emo-tionally arousing content. Before the experimenter narrated each

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FIGURE 3 | The episodic memory test: presentation trial 3 and test trial.

(A) Presentation trial 3 where human stimuli from trial 1 and 2 are presentedtogether. Depicted are the 4 positions with human stimuli as contextstory-relevant stimuli and the 4 position with context story non-relevantstimuli. (B) One “old” man and one “recent” woman stimuli were displacedto an unfamiliar position not used during the corresponding presentation trials1 or 2. Additionally, one “old” men and one “recent” woman stimuli werepresented at familiar positions already used during the correspondingpresentation trials 1 or 2. The red and green coloring of the quadrants withhuman stimuli was made for representational purposes and has not beenpresented to the participants. (C) Episodic memory test where participants

have to remember the stimulus-position-trial associations formed during the3 presentation trials. First the positions for the test trial were probed;thereafter the ones for the first trial and finally the ones for the second trialwere tested. There were 27 questions in total. On the test trial only thebackground scene was presented without stimuli. The scene was dividedinto 9 quadrants. Each of the 9 quadrants was colored and presentedindividually. (D) Thereafter, a slide with the question “What have you seen onthis position” and the corresponding response alternatives was presented.The participant was asked to select via mouse click the stimulus which he orshe was remembering to be presented on that particular position during aparticular presentation trial.

part of the context story the participant was asked to “Please tryto imagine the situation.”

Part 1“Please try to imagine the following situation. You are in a for-eign town for 3 days. On the first day you take a walk and reacha small place with little shops and pigeons. You see 4 men inblack suits. You recognize these men. You remember to have seentheir faces before. They are members of a terrorist group, whohad recently attempted to commit a poison gas attack to pre-vent a political conference. You feel that your heart is beating

faster. This attack had been prevented at the very latest moment.If it had been successful, there would have been hundreds ofvictims. You are quite sure that these men belong to this ter-rorist group. You now feel cold. You now have goose bumps.You are wondering why these men are here and what they havein mind. You are scared and you think about the cruel andunscrupulous crimes that have been committed by these men inthe past.

Then the experimenter asked whether the participant had beenable to imagine the situation: “Can you imagine the situation?In the following I will show you the close-ups of the place with

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the 4 terrorists. When viewing the close-ups please try to imag-ine what other crimes these people might have committed in thepast.”

Part 2“Please try to imagine the following situation.” This is your sec-ond day in the foreign town. During a walk you revisit the placewith the small shops and the pigeons. This time you encounter4 women. Again you are sure that you have seen these womenbefore. There was a report on a group of women who haveplanned a bomb attack to the city hall in the local news thismorning. You begin to sweat. This assault could only be stoppedseconds before the detonation of the bomb. You are sure thatthese women are the terrorists who have planned and initiatedthis assault. Your heart beats faster and your palms are cold. Youwonder why these women are here right now. You are scared andyou think about the brutal and bloody crimes these women mighthave committed in the past.

“Can you imagine this situation? In the following I will showyou the close-ups of the place with the 4 terrorists. When viewingthe close-ups please try to imagine what other crimes these peoplehave committed in the past.”

Part 3“Please try to imagine the following situation”. This is your thirdday in the town. During a walk you revisit the place with thesmall shops and the pigeons. This time you see 2 men and 2woman. You are sure that you have seen these men and womanon the previous occasions. You are breathing faster. You remem-ber to have seen these people in the morning news. It was saidthat yesterday evening these people have committed an assaultto the central station. You remember the pictures of the destruc-tion and the injured victims you saw this morning in the news.While realizing that you are now very close to these dangerouspeople you are getting horrified. You are feeling sick and yourhands are shivering. You feel insecure and you think about thebrutal and bloody crimes these people might have committed inthe past.

“Can you imagine this situation? In the following I will showyou the close-ups of the place with the 4 terrorists. When viewingthe close-ups please try to imagine what terrible consequences theattack to the central station might have for the injured innocents.”

STATISTICAL PROCEDURESStatistical analysis was performed with the program SigmaStat3.1® (Sysstat Software Inc.). All variables have been initiallyanalyzed with the Kolmogorov–Smirnov test to know whetherthe data varies significantly from the pattern expected if thedata was drawn from a population with a normal distribu-tion. Furthermore, the Levene test was performed to probethe homogeneity of variances across groups. Variables thatfailed the Kolmogorov–Smirnov or the Levene test were ana-lyzed with nonparametric statistics using the Kruskal–Wallisone-way analysis of variance on ranks and Mann–Whitneyrank sum tests for pair-wise multiple comparisons. Variablesthat passed the normality test were analyzed by means ofOne-Way ANOVA’s and Holm–Sidak and Student t-tests for

pair-wise multiple comparisons. Correlations between the stateand trait anxiety measures and the different episodic mem-ory measures (total score, human stimuli score, pigeon stimuliscore, and the scores for the trials 1–3) were performed usingboth Pearson pair-wise and Spearman-rank correlation proce-dures in dependence of the distribution of the variables. AllP-values given are two-tailed, and are considered to be signif-icant when P < 0.05 or in the case of the Holm–Sidak testswhen the P-value obtained was lower than the adjusted P-levelof significance.

RESULTSEPISODIC MEMORY PERFORMANCETotal episodic memory scoreIn this experiment we investigated whether a novel test ofepisodic memory is suited to detect age-related decrements inepisodic memory performance by testing 3 different age groupsconsisting of young [21–45], middle-aged [48–62], and aged[71–83] healthy adult participants. In order to know whetherthe groups differ in terms of episodic memory performancewe calculated a total episodic memory score that could varybetween 0 and 27 correctly remembered stimulus-position-trialassociations.

As expected a One-Way ANOVA revealed that the perfor-mance of the 3 groups was indeed significantly different fromeach other (Kolmogorov–Smirnov test: P > 0.05, Levene testP > 0.05; ANOVA: F(2, 38) = 7.785, P = 0.001, Figure 4A). Inorder to know which groups performed significantly differentfrom each other, we computed post-hoc tests using the Holm–Sidak method. We found that the young group had significantlyhigher episodic memory scores as compared to both the middle(T = 2.675; P = 0.011, significant at the critical P-level of P =0.025) and aged groups (T = 3.72; P < 0.001, significant at thecritical P-level of P = 0.017). The latter two groups performednot significantly different from each other (P > 0.05).

This result suggest that episodic memory performance is sig-nificantly better in young individuals aged between 21 and 45years as compared to individuals aged between 48 and 62 or olderparticipants.

Episodic memory performance for individual presentation trialsWe also analyzed whether the groups would differ regardingtheir episodic memory scores for the three presentation tri-als. We expected that the episodic memory performance fortrial 1 would be significantly different between the groupsbecause the delay between episodic memory encoding and therecollection of the episodic memory formed was longest >2 hfor the first trial as compared to the second and third tri-als. As predicted, we found that the 3 age groups differedsignificantly regarding the number of correctly rememberedstimulus-position associations for trial 1 (Kolmogorov–Smirnovtest: P > 0.05, Levene test: P > 0.05; ANOVA: F(2, 38) = 7.056,P = 0.002; Figure 4B).

Pair-wise post-hoc Holm–Sidak tests revealed that the perfor-mance of the aged group during the retrieval of the informationfor trial 1 was significantly worse as compared to both theyoung (T = 3.756; P = 0.000578, significant at the critical P-level

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FIGURE 4 | Effects of aging on episodic memory performance, working

memory, and emotionality. (A) Total episodic memory score. Barsrepresent mean and SEM number of correctly rememberedstimulus-position-trial associations for indicated groups. ∗P ≤ 0.05,Holm–Sidak test. (B) Performance on individual presentation trials. Barsrepresent mean and SEM number of correctly rememberedstimulus-position associations for indicated trials. ∗P ≤ 0.05, Holm–Sidaktest. (C) Context story relevant stimulus-position-trial performance. Barsrepresent mean and SEM total number of correctly rememberedhuman-position-trial associations for indicated groups. ∗P ≤ 0.05,

#0.05 < P < 0.1, Mann–Whitney rank sum test. (D) Context storynon-relevant stimulus-position-trial performance. Bars represent mean andSEM total number of correctly remembered pigeon-position-trialassociations for indicated groups. ∗P ≤ 0.05, Holm–Sidak test. (E) Workingmemory performance. Bars represent mean and SEM working memoryscores for indicated groups. ∗P ≤ 0.05, Mann–Whitney rank sum test.(F) Trait anxiety. Bars represent mean and SEM Goldberg anxiety scalescores. ∗P ≤ 0.05, #0.05 < P < 0.1, Student t-tests. Graphical presentationof the data: all data obtained with the episodic memory test and theneuropsychological tests were graphically presented as means ± SEM.

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of P = 0.017) and middle-aged group (T = 2.489; P = 0.0173,significant at the critical P-level of P = 0.025). No significant dif-ference was obtained for the comparison between the young andmiddle-aged group (P > 0.05).

While no significant difference between the groups was evi-dent for the stimulus-position associations established on trial2 (Kolmogorov–Smirnov test: P > 0.05, Levene test P < 0.05;Kruskal–Wallis One-Way analysis of variance on ranks: P > 0.05;Figure 4B), the groups performed significantly different whenprobed for the stimulus-position associations generated on trial3 (Kolmogorov–Smirnov test: P > 0.05; Levene test: P > 0.05;ANOVA: F(2, 38) = 4.863, P = 0.013).

The pair-wise post-hoc Holm–Sidak tests indicated a sig-nificant difference between the young and middle-aged group(T = 2.933; P = 0.0057, significant at the critical P-level ofP = 0.017) but not for the remaining 2 comparisons (Ps > 0.05).

This result suggests that age-related changes in episodicmemory performance are reflected by trial 1 and 3 per-formance. The inability of the second trial to discriminatebetween the groups might be due to processes of pro-and retroactive interference where the sequential acquisitionof learning material has a detrimental effect on the subse-quent retrieval process (Brophy et al., 2009). The suscepti-bility to pro- and retroactive interference might be possiblyage-independent.

Episodic memory for context-story relevant vs. non-relevant stimuliNext we analyzed whether the groups might show significantdifferences in the ability to establish and remember human-position-trial or pigeon-position-trial associations. We expectedthat the groups would differ significantly for the human context-relevant stimuli but possibly not for the context non-relevantpigeon stimuli.

A One-Way ANOVA on ranks revealed a trend towarda significant difference between the 3 groups regarding thehuman-position-trial associations (Kolmogorov–Smirnov test:P > 0.05, Levene test: P < 0.05; Kruskal–Wallis One-Way anal-ysis of variance on ranks: H = 5.345, degrees of freedom: 2,P = 0.069, Figure 4C). Mann–Whitney rank sum tests for pair-wise comparisons revealed that the young group rememberedthe human-position-trial combinations significantly better ascompared to the middle (T = 216.5, P = 0.047) group, whilethere was only a trend for a difference between the young andthe aged group (T = 74.5, P = 0.091). The middle and agedgroups performed not significantly different from each other(P > 0.05).

Contrarily to our hypothesis, the groups also differed sig-nificantly regarding their ability to remember the context-storynon-relevant pigeon-position-trial combinations (Kolmogorov–Smirnov test: P > 0.05; Levene test P > 0.05, ANOVA: F(2, 38) =4.986, P = 0.012, Figure 4D). Pair-wise post-hoc Holm–Sidaktests for the pigeon-position-trial associations showed thatthe aged group remembered a significantly fewer number ofpigeon-position-trial associations relative to the young group(T = 3.075; P = 0.00389, significant at the critical P-level ofP = 0.017). There was no significant difference between theyoung and middle-aged group (P > 0.05) or the middle-aged

and aged group (P > 0.05). Although statistically not significant,the aged group showed slightly better memory performances inthe human-position-trial associations compared to the pigeon-position trial condition.

WITHIN-GROUP COMPARISONS OF THE EPISODIC MEMORY FORCONTEXT-STORY RELEVANT vs. NON-RELEVANT STIMULINext we analyzed whether the performance of single groupswas significantly different for human vs. pigeon-position-trialassociations. However, none of the 3 groups showed a signifi-cant difference between the episodic memory for context-storyrelevant stimuli in comparison to the non-relevant stimuli (allPs > 0.05).

NEUROPSYCHOLOGICAL AND PSYCHOLOGICAL ASSESSMENTWorking memoryIn order to know whether the expected aging-related dif-ferences in episodic memory performance are at least inpart due to changes in working memory performance wealso measured this capacity in the three groups. A One-Way ANOVA on ranks revealed that the working memoryperformance of the 3 groups was indeed significantly dif-ferent from each other (Kolmogorov–Smirnov test: P < 0.05;Levene test: P > 0.05; Kruskal–Wallis One-Way analysis of vari-ance on ranks: H = 13.997, degrees of freedom: 2, P < 0.001,Figure 4E). In order to know which groups performed sig-nificantly different from each other, we computed Mann–Whitney rank sum tests for pair-wise comparisons. We foundthat the young group had significantly higher working mem-ory scores as compared to both the middle (T = 197.5, P =0.008) and aged groups (T = 48, P = 0.001). The latter twogroups performed not significantly different from each other(P > 0.05).

Depressive symptomsIt is known that the incidence of major depression isincreased in aged individuals and that depressive episodesare associated with memory impairments. We therefore testedwhether possible differences in episodic memory performancebetween the 3 groups might be explained by differencesin depressive symptoms. There were no significant differ-ences between the groups on the Goldberg depression scale(P > 0.05).

AnxietyWe have hypothesized that age-related decline in episodicmemory performance might be related to hypo-emotionalityor changes in the processing of emotionally-valenced stimuli.Therefore, we also tested whether possible group-differencesin episodic memory performance might be explained bydifferences in trait or state (experimental context-induced)anxiety.

Trait anxietyA One-Way ANOVA indicated a trend for a difference betweenthe groups in the Goldberg scale subtest measuring trait anxi-ety (Kolmogorov–Smirnov test: P > 0.05, Levene test P > 0.05;

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ANOVA: F(2, 37) = 2.781, P = 0.075, Figure 4F). Pair-wise com-parisons by means of Student t-tests revealed that the agedgroup showed significantly lower trait anxiety scores as com-pared to the young group (Kolmogorov–Smirnov test: P >

0.05, Levene test P > 0.05; T = 2.236, degrees of freedom:22, P = 0.036), but only a trend for a difference as com-pared to the middle-aged group (Kolmogorov–Smirnov test:P > 0.05, Levene test P > 0.05; T = 2.016, degrees of free-dom: 22, P = 0.056). No significant difference was found forthe comparison between the young and middle-aged group(P > 0.05).

State anxietyThe comparison of the STAI state anxiety reference valuesreported for patients with phobia or anxiety disorders (F40/F41)mean: 42.7 ± 11.5 (Laux et al., 1981) with the mean scores of our3 age groups: young: 50.59 ± 0.68, middle aged: 52.25 ± and aged:51.0 ± 2.67 indicates that the context story in combination withthe slide presentations has induced an level of emotional arousalin the participants that is similar to the one that has been mea-sured in clinical populations. However, there was no significantdifference between groups in the state anxiety test (P > 0.05).This result suggest that the experimental context induced sim-ilar levels of emotional activation respectively anxiety in the3 groups.

CorrelationsWe also performed Pearson and Spearman rank correlationsincluding data from all participants between different measuresof episodic memory performance and state and trait anxi-ety scores. There was only one significant correlation betweenthe state anxiety scores and the episodic memory scores forthe pigeon-position-trial associations (R(38) = 0.322, P = 0.049)all other correlations obtained failed to reach the level ofstatistical significance. We also calculated single group cor-relations for the significant correlation found between stateanxiety and pigeon-position-trial associations, but did notfound significant correlations between the two variables inany group (all Ps > 0.05). The highest correlation found wasR(16) = 0.431 with a P-value of 0.095 in the middle agedgroup.

DISCUSSIONSUMMARYIn the present study, we hypothesized that episodic memorydeficits will be associated with changes in trait and/or state anx-iety in the aged but also in the middle-aged group. The resultspresented above suggest that our novel test of episodic mem-ory that measures the core components of an episodic mem-ory (event, spatial, and temporal information) and in additionprobes the ability to form new episodic memories is suitedto detect age-related impairments in episodic memory perfor-mance. The episodic memory deficits observed in the aged groupwere observed along with lower anxiety scores measured withthe Goldberg anxiety scale. However, no significant correlationbetween episodic memory and trait or state anxiety scores werefound.

EPISODIC MEMORY PERFORMANCE ON INDIVIDUAL PRESENTATIONTRIALSIt is well known that aging affects episodic memory function moreseverely than other types of memory including semantic memory(Levine et al., 2002). It has been proposed that this difference ispossibly mediated by changes in the processing of emotionally-competent stimuli (Allen et al., 2005; Kensinger, 2009). We foundthat the young group was able to remember a higher numberof stimulus-position-trial associations (out of 27 associations tobe remembered) as compared to both the middle-aged and agedgroups. Age-dependent effects were most prominent when therecall of the information for trial 1 was tested. Here, the agedgroup performed inferior to both the young and middle-agedgroups. These results suggest that the aged group failed to consol-idate the trial 1 information (that had been acquired more than2 h before the test) into long-term memory.

CONTEXT STORY RELEVANT AND NON-RELEVANTSTIMULUS-POSITION-TRIAL PERFORMANCEWe hypothesized that context story-relevant stimuli (men andwoman) might be generally better remembered as context storynon-relevant stimuli and therefore would be much better suitedto identify age-dependent impairments in episodic memory per-formance. However, the present results suggest that this was notthe case. In fact there was no significant difference between thememory of the context story-relevant vs. non-relevant stimulieven in the young group. We found that both types of stimuliwere suited to detect age-dependent changes in episodic memoryperformance. As expected the young group showed better per-formance for context story-relevant stimuli as compared to theother groups. Interestingly, the aged group showed impaired con-text story non-relevant recall of pigeon-position-trial associationsas compared to the young group. The aged group also showedslightly better (although statistically not significant) memoryperformance in the context-story relevant human-position-trialassociations condition as compared to the pigeon-position-trialassociations condition. These results suggest the presence of animpairment in the possibly incidental or non-intentional encod-ing of information that is not directly relevant to the context-storyin the aged group (Naveh-Benjamin et al., 2009). It seems thatthe limited attention and memory capacities of aged individualsdo not permit the allocation of additional processing resources toattend to and encode context-story non-relevant stimuli. Anotherpossible explanation of this deficit might be that the episodicmemories encoded by aged individuals generally contain lessevent details and context-specific information. In fact there isevidence for limited information processing capacities in agedindividuals as well as changes in the management and allocationof processing resources in learning situations (Craik and Byrd,1982).

Interestingly we found a significant correlation between thestate anxiety scores and the episodic memory scores for thepigeon-position-trial associations. Given that the old groupshowed lower trait anxiety scores and impaired episodic memoryfor pigeon-position-trial associations, it is tempting to specu-late that incidental or non-intentional encoding of context-storynon-relevant information depends on the level of trait anxiety.

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AGING-DEPENDENT EFFECTS OF WORKING MEMORY ON THEENCODING OF EPISODIC INFORMATIONIt is known that working memory mediated by the dorso-lateral prefrontal cortex plays a role in the encoding andretrieval of long-term memories including episodic memory (Leeet al., 2000; Cabeza et al., 2002; Blumenfeld and Ranganath,2006). Thus, we also investigated whether age-related differ-ences in episodic memory performance might be explainedby changes in working memory performance. We found thatworking memory performance is impaired in the middle-agedand aged groups as compared to the young group. It is pos-sible that these working memory deficits might be relatedto an impairment at the encoding stage of episodic mem-ory formation (Unsworth et al., 2011) in the middle-agedand aged groups in the course of the presentation of the3 trials.

DEPRESSIVE SYMPTOMS AND EPISODIC MEMORYIt is known that the incidence of depressive symptoms that alsoinclude episodic memory impairments are increased in the agedpopulation (Airaksinen et al., 2004, 2007; Potter and Steffens,2007). In geriatric settings cognitive symptoms that are associatedwith a depressive disorder are often misinterpreted as demen-tia (Ouldred and Bryant, 2008). Therefore, we tested whetherthe middle-aged and aged group might exhibit an increase indepressive symptoms. However, this was not the case so that thedifferences in episodic memory performance observed betweenthe young and the older groups are unlikely to be due to adepressive condition in the middle-aged and/or aged group.

AGING-RELATED IMPAIRMENTS IN EPISODIC MEMORY ANDCHANGES IN EMOTIONALITYIt is well known that emotionally arousing events are more likelyto be encoded into long-term memory as compared to neu-tral events (Cahill and McGaugh, 1998). Furthermore, it hasbeen hypothesized that emotional activation might be a prereq-uisite for episodic memory formation (Dere et al., 2010). In thepresent study, we asked whether aging-related episodic memorydecline might be associated with changes in state or trait anx-iety. Trait anxiety reflects a general personality trait to exhibitanxiety-related behavior at the cognitive (e.g., worrying) and/orbehavioral level (e.g., avoidance of anticipated fear-inducing situ-ations) that might be affected by aging. Trait anxiety is relativelystable across time while state anxiety shows large fluctuations anddepends on the current context.

We found lower anxiety scores in the aged group as com-pared to the young and middle-aged group. This change in thetrait anxiety levels in the aged group might be associated witha reduced emotional activation by the experimental situationor by the context story. Given that there were no significantcorrelations between total episodic memory and trait or stateanxiety scores, it still remains to be determined whether thisdifference in anxiety is indeed related to the impaired episodicmemory performance in the aged group. In future studies, wewill measure physiological correlates of emotional activationsuch as the blood pressure and the galvanic skin reaction inthe aged population to test the above proposed relationship

between decreased anxiety and impairments in episodic memoryin healthy aged individuals.

There is evidence that older individuals exhibit a decreasedfunctional connectivity between the amygdala and the hippocam-pus (St Jacques et al., 2009). Episodic memory impairments inthe elderly might be related to a diminished emotional mod-ulation of declarative memory formation implemented by theamygdala-hippocampus axis (McGaugh et al., 1996; Tulving andMarkowitsch, 1998; Dere et al., 2010). This hypothesis mightbe tested by combining our novel test of episodic memory withhippocampal-amygdala EEG coherence measurements and neu-roimaging methods such as functional MRI.

Novel tests of episodic memory and limitations of the present taskRecently novel episodic memory tasks have been designed that arebased on paradigms that have been originally developed to studyepisodic-like memory in animals (Clayton and Dickinson, 1999;Dere et al., 2005a). These tasks are either based on the “what,where, and when” (Pause et al., 2010; Holland and Smulders,2011) or “what, where, which” (Easton et al., 2012) principles.Pause et al. (2010) followed a reverse translational approachand adapted the episodic-like memory test for rodents (Dereet al., 2005a) to humans and devised a computer-based test.However, this test requiring the active exploration of the com-puter screen using a keyboard might be too complicated to berun with older individuals. Others have probed episodic mem-ory based on the “what, where, and when” paradigm by ask-ing participants to hide different coin types (what) in differentlocations (where) on two separate occasions (when) (Hollandand Smulders, 2011). These authors conclude that paradigmsbased on the “what, where, and when” paradigm might beindeed reliable tests of episodic memory function. Anotherapproach to translate findings from animal research into tests ofhuman episodic memory was based on the “what, where, andwhich” paradigm (Easton et al., 2012). Here, it has been pro-posed that tasks using contextual information to discriminateevents could only be accurately performed using recollection,not familiarity, while tasks using temporal information to dis-criminate events might be solved using either recollection orfamiliarity (Easton et al., 2012). It thus remains to be deter-mined whether tasks based on the “what, where, and when”paradigm rely more on recollection vs. familiarity-based memoryperformance.

In order to fully explore the strengths and limits of the novelepisodic memory test described here, follow-up studies shouldbe performed in which recollection vs. familiarity-based memoryperformance is assessed, sample sizes are increased and in whichdirect physiological measurements of emotional activation duringtask performance are correlated with the episodic memory scoresobtained.

ACKNOWLEDGMENTSThis study was supported by funds from the DeutscheForschungsgemeinschaft (grant no.: DFG-DE-1149/6-1) andthe Centre National de la Recherché Scientifique (ActionInterdisciplinaire CNRS: Vieillissement) to Ekrem Dere.

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REFERENCESAiraksinen, E., Larsson, M., Lundberg,

I., and Forsell, Y. (2004). Cognitivefunctions in depressive disorders:evidence from a population-basedstudy. Psychol. Med. 34, 83–91.

Airaksinen, E., Wahlin, A., Forsell,Y., and Larsson, M. (2007). Lowepisodic memory performance asa premorbid marker of depression:evidence from a 3-year follow-up.Acta Psychiatr. Scand. 115, 458–465.

Allen, P. A., Kaut, K. P., Lord, R. G.,Hall, R. J., Grabbe, J. W., and Bowie,T. (2005). An emotional mediationtheory of differential age effects inepisodic and semantic memories.Exp. Aging Res. 31, 355–391.

Blumenfeld, R. S., and Ranganath,C. (2006). Dorsolateral prefrontalcortex promotes long-term mem-ory formation through its rolein working memory organization.J. Neurosci. 26, 916–925.

Bornstein, R., Baker, G., and Douglass,A. (1991). Depression andmem-oryin major depression disorder.J. Neuropsychiatry Clin. Neurosci. 3,78–80.

Brophy, L. M., Jackson, M., andCrowe, S. F. (2009). Interferenceeffects on commonly used memorytasks. Arch. Clin. Neuropsychol. 24,105–112.

Burgess, N., Maguire, E. A., andO’Keefe, J. (2002). The human hip-pocampus and spatial and episodicmemory. Neuron 35, 625–641.

Cabeza, R., Dolcos, F., Graham, R., andNyberg, L. (2002). Similarities anddifferences in the neural correlatesof episodic memory retrieval andworking memory. Neuroimage 16,317–330.

Cahill, L., and McGaugh, J. L. (1998).Mechanisms of emotional arousaland lasting declarative memory.Trends Neurosci. 21, 294–299.

Clayton, N. S., and Dickinson, A.(1999). Episodic-like memory dur-ing cache recovery by scrub jays.Nature 395, 272–274.

Craik, F. I. M., and Byrd, M. (1982).Aging and Cognitive Deficits: TheRole of Attentional Processes. NewYork, NY: Plenum Press.

Dere, E., Huston, J. P., and De SouzaSilva, M. A. (2005a). Integratedmemory for objects, places and tem-poral order: evidence for episodic-like memory in mice. Neurobiol.Learn. Mem. 84, 214–221.

Dere, E., Huston, J. P., and De SouzaSilva, M. A. (2005b). Protocol:episodic-like memory in mice:simultaneous assessment of object,place and temporal order memory.Brain Res. Brain Res. Protoc. 16,10–19.

Dere, E., Pause, B., and Pietrowsky,R. (2010). Emotion and episodicmemory in neuropsychiatric disor-ders. Behav. Brain Res. 215, 162–171.

Dubois, B., Feldman, H. H., Jacova, C.,Dekosky, S. T., Barberger-Gateau,P., Cummings, J., et al. (2007).Research criteria for the diagnosisof Alzheimer’s disease: revising theNINCDS-ADRDA criteria. LancetNeurol. 6, 734–746.

Easton, A., Webster, L. A., and Eacott,M. J. (2012). The episodic natureof episodic-like memories. Learn.Mem. 19, 146–150.

Goldberg, D., Bridges, K., Duncan-Jones, P., and Grayson, D. (1988).Detecting anxiety and depression ingeneral medical settings. BMJ 297,897–899.

Holland, S. M., and Smulders, T. V.(2011). Do humans use episodicmemory to solve a What-Where-When memory task? Anim. Cogn.14, 95–102.

Kart-Teke, E., De Souza Silva, M.A., Huston, J. P., and Dere, E.(2006). Wistar rats show episodic-like memory for unique experi-ences. Neurobiol. Learn. Mem. 85,173–182.

Kaszniak, A. W., and Menchola, M.(2012). Behavioral neuroscience ofemotion in aging. Curr. Top. Behav.Neurosci. 10, 51–66.

Kensinger, E. A. (2009). How emotionaffects older adults’ memories forevent details. Memory 17, 208–219.

Kensinger, E. A., Addis, D. R., andAtapattu, R. K. (2011). Amygdalaactivity at encoding correspondswith memory vividness and withmemory for select episodic details.Neuropsychologia 49, 663–673.

Kirchhoff, B. A., Wagner, A. D.,Maril, A., and Stern, C. E. (2000).Prefrontal-temporal circuitry forepisodic encoding and subsequentmemory. J. Neurosci. 20, 6173–6180.

Laux, L., Glanzmann, P., Schaffner,P., and Spielberger, C. D. (1981).Das State-Trait-Angstinventar.Theoretische Grundlagen undHandanweisung. Weinheim: BeltzTest GmbH.

LeDoux, J. (2007). The amygdala. Curr.Biol. 17, R868–R874.

Lee, A. C., Robbins, T. W., and Owen, A.M. (2000). Episodic memory meetsworking memory in the frontal lobe:functional neuroimaging studies ofencoding and retrieval. Crit. Rev.Neurobiol. 14, 165–197.

Levine, B., Svoboda, E., Hay, J. F.,Winocur, G., and Moscovitch, M.(2002). Aging and autobiographicalmemory: dissociating episodic fromsemantic retrieval, Psychol. Aging17, 677–689.

Libkuman, T. M., Stabler, C. L., andOtani, H. (2004). Arousal, valence,and memory for detail. Memory 12,237–247.

Markowitsch, H. J., and Staniloiu,A. (2011). Amygdala in action:relaying biological and socialsignificance to autobiographicalmemory. Neuropsychologia 49,718–733.

McGaugh, J. L. (2004). The amyg-dala modulates the consolidation ofmemories of emotionally arousingexperiences. Annu. Rev. Neurosci.27, 1–28.

McGaugh, J. L., Cahill, L., andRoozendaal, B. (1996). Involvementof the amygdala in memory stor-age: interaction with other brainsystems. Proc. Natl. Acad. Sci. U.S.A.93, 13508–13514.

McIntyre, C. K., Power, A. E.,Roozendaal, B., and McGaugh,J. L. (2003). Role of the basolateralamygdala in memory consolida-tion. Ann. N.Y. Acad. Sci. 985,273–293.

Nashiro, K., and Mather, M. (2011).How arousal affects younger andolder adults’ memory binding. Exp.Aging Res. 37, 108–128.

Naveh-Benjamin, M., Shing, Y. L.,Kilb, A., Werkle-Bergner, M.,Lindenberger, U., and Li, S. C.(2009). Adult age differences inmemory for name-face associa-tions: the effects of intentional andincidental learning. Memory 17,220–232.

Nebes, R. D., Butters, M. A., Mulsant,B. H., Pollock, B. G., Zmuda, M.D., Houck, P. R., et al. (2000).Decreased working memory andprocessing speed mediate cognitiveimpairment in geriatric depression.Psychol. Med. 30, 679–691.

Nyberg, L., Lövdén, M., Riklund, K.,Lindenberger, U., and Bäckman, L.(2012). Memory aging and brainmaintenance. Trends Cogn. Sci. 16,292–305.

Nyberg, L., McIntosh, A. R., Houle,S., Nilsson, L. G., and Tulving, E.(1996). Activation of medial tempo-ral structures during episodic mem-ory retrieval. Nature 380, 715–717.

Ouldred, E., and Bryant, C. (2008).Dementia care. Part 1: guidance andthe assessment process. Br. J. Nurs.17, 138–145.

Park, D. C., Lautenschlager, G.,Hedden, T., Davidson, N. S., Smith,A. D., and Smith, P. K. (2002).Models of visuospatial and verbalmemory across the adult life span.Psychol. Aging 17, 299–320.

Pause, B., Jungbluth, C., Adolph, D.,Pietrowsky, R., and Dere, E. (2010).Induction and measurement of

episodic memories in healthyadults. J. Neurosci. Methods 189,88–96.

Persson, J., Nyberg, L., Lind, J., Larsson,A., Nilsson, L. G., Ingvar, M., et al.(2006). Structure-function corre-lates of cognitive decline in aging.Cereb. Cortex 16, 907–915.

Potter, G. G., and Steffens, D. C. (2007).Contribution of depression to cog-nitive impairment and dementiain older adults. Neurologist 13,105–117.

Rajah, M. N., Kromas, M., Han, J. E.,and Pruessner, J. C. (2010). Groupdifferences in anterior hippocam-pal volume and in the retrievalof spatial and temporal contextmemory in healthy young versusolder adults. Neuropsychologia 48,4020–4030.

Rönnlund, M., Nyberg, L., Bäckman,L., and Nilsson, L. G. (2005).Stability, growth, and decline inadult life span development ofdeclarative memory: cross-sectionaland longitudinal data from apopulation-based study. Psychol.Aging 20, 3–18.

Shing, Y. L., Werkle-Bergner, M.,Brehmer, Y., Müller, V., Li, S.C., and Lindenberger, U. (2010).Episodic memory across the lifes-pan: the contributions of associativeand strategic components. Neurosci.Biobehav. Rev. 34, 1080–1091.

Spielberger, C. D., Gorsuch, R.L., and Lushene, R. E. (1970).Manual for the State-Trait AnxietyInventory. Palo Alto, CA: ConsultingPsychologists Press.

St Jacques, P. L., Dolcos, F., and Cabeza,R. (2009). Effects of aging on func-tional connectivity of the amygdalafor subsequent memory of negativepictures: a network analysis of func-tional magnetic resonance imagingdata. Psychol. Sci. 20, 74–84.

Tsivilis, D., Vann, S. D., Denby, C.,Roberts, N., Mayes, A. R., Montaldi,D., et al. (2008). A disproportionaterole for the fornix and mammil-lary bodies in recall versus recog-nition memory. Nat. Neurosci. 11,834–842.

Tulving, E. (1983). Elements ofEpisodic Memory. London: OxfordUniversity Press.

Tulving, E. (2002). Episodic memory:from mind to brain. Annu. Rev.Psychol. 53, 1–25.

Tulving, E., and Markowitsch, H. J.(1998). Episodic and declarativememory: role of the hippocampus.Hippocampus 8, 198–204.

Unsworth, N., Brewer, G. A., andSpillers, G. J. (2011). Variationin working memory capacity andepisodic memory: examining the

Frontiers in Behavioral Neuroscience www.frontiersin.org February 2013 | Volume 7 | Article 2 | 11

Kinugawa et al. Episodic memory, aging, and emotion

importance of encoding specificity.Psychon. Bull. Rev. 18, 1113–1118.

Van Petten, C., Plante, E., Davidson,P. S., Kuo, T. Y., Bajuscak, L.,and Glisky, E. L. (2004). Memoryand executive function in olderadults: relationships with temporaland prefrontal gray matter volumesand white matter hyperintensities.Neuropsychologia 42, 1313–1335.

Wheeler, M. A., Stuss, D. T., andTulving, E. (1997). Toward a the-ory of episodic memory: the frontallobes and autonoetic consciousness.Psychol. Bull. 121, 331–354.

Williams-Gray, C. H., Foltynie, T.,Lewis, S. J., and Barker, R. A. (2006).

Cognitive deficits and psychosisin Parkinson’s disease: a reviewof pathophysiology and therapeuticoptions. CNS Drugs 20, 477–505.

Wolf, O. T. (2012). Immediate recallinfluences the effects of pre-encoding stress on emotionalepisodic long-term memory consol-idation in healthy young men. Stress15, 272–280.

Wolff, M., Loukavenko, E. A., Will,B. E., and Dalrymple-Alford, J. C.(2008). The extended hippocampal-diencephalic memory system:enriched housing promotes recov-ery of the flexible use of spatialrepresentations after anterior

thalamic lesions. Hippocampus 18,996–1007.

Conflict of Interest Statement: Theauthors declare that the researchwas conducted in the absence of anycommercial or financial relationshipsthat could be construed as a potentialconflict of interest.

Received: 09 November 2012; accepted:14 January 2013; published online: 01February 2013.Citation: Kinugawa K, Schumm S,Pollina M, Depre M, Jungbluth C,Doulazmi M, Sebban C, Zlomuzica

A, Pietrowsky R, Pause B, MarianiJ and Dere E (2013) Aging-relatedepisodic memory decline: are emotionsthe key? Front. Behav. Neurosci. 7:2. doi:10.3389/fnbeh.2013.00002Copyright © 2013 Kinugawa, Schumm,Pollina, Depre, Jungbluth, Doulazmi,Sebban, Zlomuzica, Pietrowsky, Pause,Mariani and Dere. This is an open-access article distributed under the termsof the Creative Commons AttributionLicense, which permits use, distributionand reproduction in other forums, pro-vided the original authors and sourceare credited and subject to any copy-right notices concerning any third-partygraphics etc.

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