Neuropsychologia 66 (2015) 10–17

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Neuropsychologia

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n Corr2006, A

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journal homepage: www.elsevier.com/locate/neuropsychologia

Autobiographical memory in children with Idiopathic GeneralisedEpilepsy

Michael B. Gascoigne a,d, Belinda Barton b, Richard Webster c, Deepak Gill c, Suncica Lah a,d,n

a School of Psychology, The University of Sydney, NSW 2006, Australiab Children's Hospital Education Research Institute, The Children's Hospital at Westmead and Discipline of Paediatrics and Child Health, Faculty of Medicine,University of Sydney, Australiac T.Y. Nelson Department of Neurology and Neurosurgery, The Children's Hospital at Westmead, Sydney, Australiad ARC Centre of Excellence in Cognition and its Disorders, Australia

a r t i c l e i n f o

Article history:Received 9 August 2014Received in revised form3 November 2014Accepted 8 November 2014Available online 13 November 2014

Keywords:Idiopathic Generalised EpilepsyAutobiographical memoryRecallConsolidationEpisodic memoryRemote memory

x.doi.org/10.1016/j.neuropsychologia.2014.11.032/& Elsevier Ltd. All rights reserved.

esponding author at: School of Psychology, Thustralia. Fax: þ61 2 9036 5223.ail address: suncica.lah@sydney.edu.au (S. Lah

a b s t r a c t

Autobiographical memory involves the recall of both personal facts (semantic memory) and the re-ex-periencing of past personal events (episodic memory). The recall of autobiographical episodic details hasbeen associated with a specific network, which involves the prefrontal and medial temporal lobes, inaddition to posterior regions of the brain. Seizure activity has been previously shown to disrupt theconsolidation of newly-learned information into long-term memory, but it is not yet known whetherprimary generalised seizures alone are also associated with deficits in the recall of autobiographicalmemories. Here we examined this recall in children who experience generalised rather than localisation-related seizures: children with Idiopathic Generalised Epilepsy (IGE). In this study, 18 children with IGEand 42 healthy controls of comparable age (6–16 years), sex and socio-economic status were adminis-tered the Children's Autobiographical Interview (CAI). Compared with controls, children with IGE re-called significantly fewer episodic details, even when retrieval prompts were provided. In contrast, nogroup difference was found for the recall of semantic autobiographic details. Within the IGE group,hierarchical regression analyses showed that patient age and earlier age of diagnosis were significantlyrelated to the recall of episodic autobiographical details over different conditions of the CAI, explainingup to 37% of variance. To our knowledge, this study provides the first evidence of autobiographicalepisodic memory deficits in patients with primary generalised seizures. As no evidence of localisation-related epilepsy is apparent in patients with IGE, our findings suggest that generalised seizures alone,especially when developed at an early age, could compromise memories for personally-experiencedevents.

& Elsevier Ltd. All rights reserved.

1. Introduction

Autobiographical memory is a complex ability that involvesmental “time travel” and re-experiencing of personal past eventscharacterised by unique constellations of specific emotional, per-ceptual, cognitive and temporal details: episodic memory (Levineet al., 2002; Tulving, 2002). Each autobiographical episode is en-countered once only and is typically embedded within a context ofpersonal factual information (Levine, 2004): semantic memory.Unlike episodic memory, semantic memory is acquired throughrepeated exposures and does not involve re-experiencing.

10

e University of Sydney, NSW

).

Given that episodic (but not semantic) memories are uniqueand, once compromised, cannot be completely re-established,episodic memories may be more sensitive to disruption than se-mantic memories by generalised seizures and/or diffuse pathologyunderlying generalised seizures. The possibility that generalisedseizures could compromise autobiographical episodic memorieshas received little attention. Research has largely focussed on theinvolvement of the hippocampus in retrieval of autobiographicalevent details, which is proposed to be temporally limited andtemporally unlimited, according to the classic consolidation theory(CCT, Squire et al., 1984) and multiple trace theory (MTT, Nadel andMoscovitch, 1997), respectively. In one study, however, Lah et al.(2006) compared adult patients with temporal lobe epilepsy (TLE)who experienced generalised seizures (in combination withcomplex partial seizures) with controls and also patients whoexperienced complex partial seizures only. Compared with controlparticipants, both TLE patient groups recalled significantly fewer

M.B. Gascoigne et al. / Neuropsychologia 66 (2015) 10–17 11

autobiographical episodes and less semantic information, al-though the two patient groups did not differ significantly fromeach other. However, in this study the temporal lobe seizure focus/abnormality alone could have compromised the recall of auto-biographical memories, as temporal lobe pathology has beenpreviously found to disrupt the recollection of episodic and se-mantic autobiographical details even in patients who do not havea history of seizures, such as those with Alzheimer's disease(Dorrego et al., 1999; Greene and Hodges, 1996; Irish et al., 2011,2013; Sexton et al., 2010) or semantic dementia (Graham et al.,1997; Irish et al., 2012; Matuszewski et al., 2009; Snowden et al.,1996).

To investigate whether autobiographical memory can poten-tially be disrupted by generalised seizures alone, patients whoexperience generalised seizures and no indication of localisation-related epilepsy (i.e., temporal lobe epilepsy), such as patientswith Idiopathic Generalised Epilepsy (IGE), would need to be as-sessed. This form of epilepsy is a common type of epilepsy inchildhood, representing approximately 20% of all epilepsies foundin children (Jallon and Latour, 2005). Accordingly, the currentstudy examined the autobiographical memory performance inchildren with IGE.

Epilepsy-related factors such as treatments can also adverselyimpact memory. One study found that adults with TLE who wereon antiepileptic drug polytherapy recalled significantly fewer au-tobiographical events relative to adults on monotherapy (Lah et al.,2006). However, a recent study found no relationship betweenpolytherapy and recall of autobiographical events in children withTLE (Gascoigne et al., 2013). Moreover, factors such as severity(Helmstaedter, 2002) and longer duration of epilepsy disorderhave been found to negatively impact learning and recall of in-formation in both adults (Mameniskiene et al., 2006) and children(Nolan et al., 2004) with epilepsy, but were not related to auto-biographical memory in children (Gascoigne et al., 2013) or adultswith epilepsy (Lah et al., 2004). Previous studies of children withTLE suggest that memory deficits emerge gradually over thecourse of development; that children “grow into their memorydeficits”. For example, a longitudinal study of children with leftTLE found that verbal memory deficits only became apparentduring their teenage years or young adulthood (Gonzalez et al.,2012) when no such deficits were obvious during childhood(Gonzalez et al., 2007). A large cross-sectional study involving1000 healthy control subjects (aged 6–80 years) and 1157 patientswith TLE (aged 6–68 years) also found that deficits in recall ofverbal information after short delays were not evident in children,but became noticeable (relative to healthy controls) during ado-lescence or young adulthood (Helmstaedter and Elger, 2009).

In addition to epilepsy-related factors, it has been suggestedthat autobiographical memory deficits in patients with epilepsymay also be secondary to other underlying cognitive deficits, suchas impaired short-term recall of newly-learned verbal materialsthat is evident on standardised memory tests (Lah et al., 2004,2006). Deficits in the recall of newly-learned information have alsobeen associated with autobiographical memory impairments innon-epilepsy patients, such as those with Korsakoff's syndrome(Mayes et al., 1997; Schmidtke and Vollmer, 1997; Shimamura andSquire, 1986). Interestingly, among patients with TLE, deficits inepisodic aspects of autobiographical memory and in short-termrecall of newly-learned materials have been found in both adults(Herfurth et al., 2010; Lah et al., 2004, 2006) and children (Gas-coigne et al., 2013). However, no significant association has beenfound between these two memory types. Compared with healthycontrols, children with IGE perform significantly more poorly onstandardised memory tests (Gascoigne et al., 2012), but whetherthese deficits compromise autobiographical recall in this patientpopulation is not known.

The aim of this study was to investigate the recall of auto-biographical memories in children with IGE. As episodic memoriesmay be more sensitive to disruption from seizure activity thansemantic memories, it was hypothesised that children with IGEwould exhibit poorer episodic recall than their healthy controlpeers on a test of autobiographical recall. The impact of other re-levant epilepsy variables (such as mono- vs. poly-therapy, epilepsyseverity, age at diagnosis and proportion of life with epilepsy) aswell as potential associations between performances on the au-tobiographical memory task, tests of new learning and short-termmemory, and chronological age were also examined.

2. Method

2.1. Participants

A total of 18 children with IGE and 42 control children wererecruited. All participants were fluent in English and aged between6 and 16 years at the time of assessment. Participants were ex-cluded for the following reasons: (i) Full Scale Intelligence Quo-tient (FSIQ)o80; (ii) presence of a major sensory deficit; (iii)significant neurodevelopmental disorder (e.g. autism, but notlearning disability or Attention Deficit Hyperactivity Disorder(ADHD)), or (iv) another neurological disorder.

All IGE participants were recruited from The Children's Hospitalat Westmead (CHW), after the ethics committees of both CHW andThe University of Sydney approved the study. Initially 24 partici-pants were seen for a neuropsychological assessment. Paediatricneurologists, who were blind to neuropsychological findings, re-viewed electroencephalography records, medical history, andclinical imaging data in order to identify participants who met theInternational League Against Epilepsy criteria for IGE (Commissionon Classification and Terminology of the International LeagueAgainst Epilepsy, 1989). On review, six patients were excluded, asthey did not completely meet the diagnostic criteria for IGE.Control participants were free of a history of epilepsy and re-cruited through the peer networks of the IGE patients and othercontrol participants (snowball recruitment).

Clinical data for the 18 IGE participants are summarised inTable 1. The average age of diagnosis was 6.2 (SD¼3.3) years andmean epilepsy severity rating was 2.3 (SD¼1.7), equivalent to arating between “A little severe” and “Somewhat severe”. One IGEparticipant had an existing diagnosis of ADHD. All participantswere taking anti-epileptic drugs (AEDs) at the time of assessment,16 were on monotherapy and 2 on polytherapy. Eight differentAEDs were represented within the IGE sample, with sodiumvalproate being the most commonly prescribed drug (n¼8). Of the18 children with IGE, 9 met criteria for the Childhood AbsenceEpilepsy syndrome, 3 with Febrile Seizures Plus, 2 with Epilepsywith Myoclonic Absences, 1 with Juvenile Absence Epilepsy and1 with Epilepsy with Generalised Tonic–Clonic Seizures alone. Twopatients could not be classified into an IGE syndrome.

2.2. Measures

The standardised clinical neuropsychological instruments usedin this study are summarised in Table 2 and standard scores arereported. Average years of parent/guardian education were used asa measure of socioeconomic status (SES).

The Global Assessment of Severity of Epilepsy (GASE; Speechleyet al., 2008) scale was used by treating paediatric neurologists toassess the severity of epilepsy in IGE participants. Epilepsy severityratings [ranging from 1 (not at all severe) to 7 (extremely severe)]were based on the frequency and intensity of seizures, injuriesduring seizures, number and side effects of antiepileptic drugs,

Table

1Pa

tien

tch

aracteristics.

Participan

tSy

ndrome

Com

orbiddisorder

Seizure

freq

uen

cyEE

GSe

izure

types

AED

sEp

ilepsy

seve

rity

Age

atdiagn

osis

Duration

(yea

rs)

1Child

hoo

dAbs

ence

Epile

psy

ADHD

Daily

Spikean

dwav

eAbs

ence

ETX

Veryseve

re2.5

3.7

2Child

hoo

dAbs

ence

Epile

psy

Non

eDaily

Spikean

dwav

eAbs

ence

VPA

Quiteseve

re3.6

5.3

3Child

hoo

dAbs

ence

Epile

psy

Non

eAnnually

Normal

Abs

ence

LTG

Alittleseve

re6.3

5.8

4Child

hoo

dAbs

ence

Epile

psy

Non

eDaily

Spikean

dwav

eAbs

ence

LTG

Mod

eratelyseve

re4.0

3.4

5Child

hoo

dAbs

ence

Epile

psy

Non

eDaily

Spikean

dwav

eAbs

ence,G

TCS

PHT

Not

atallseve

re6.5

5.9

6Child

hoo

dAbs

ence

Epile

psy

Non

eDaily

Spikean

dwav

eAbs

ence,G

TCS

CLB

Not

atallseve

re9.8

6.8

7Child

hoo

dAbs

ence

Epile

psy

Non

eBiannually

Spikean

dwav

eAbs

ence,G

TCS

CLB

Not

atallseve

re8.4

1.6

8Child

hoo

dAbs

ence

Epile

psy

Non

eDaily

Spikean

dwav

eAbs

ence

ACE,

LEV

Quiteseve

re8.0

1.3

9Child

hoo

dAbs

ence

Epile

psy

Non

eAnnually

Spikean

dwav

eAbs

ence,G

TCS

VPA

Alittleseve

re12

.60.6

10GEF

Sþ

Non

eBiannually

Normal

Abs

ence,G

TCS

VPA

Not

atallseve

re2.4

7.0

11GEF

Sþ

Non

eBiannually

Spikean

dwav

eGTC

SVPA

Alittleseve

re2.5

6.3

12GEF

Sþ

Non

eBiannually

Spikean

dwav

eGTC

SVPA

Not

atallseve

re4.0

4.4

13Ep

ilepsy

withMyo

clon

icAbs

ences

Non

eBiannually

Spikean

dwav

eAbs

ence,G

TCS

VPA

Not

atallseve

re2.4

8.6

14Ep

ilepsy

withMyo

clon

icAbs

ences

Non

eTw

icean

nually

Spikean

dwav

eAbs

ence,G

TCS

LEV

Mod

eratelyseve

re2.9

5.9

15Juve

nile

Abs

ence

Epile

psy

Non

eBiannually

Spikean

dwav

eAbs

ence

LEV

Not

atallseve

re7.3

4.4

16Ep

ilepsy

withGen

eralised

Tonic–Clonic

Seizuresalon

eNon

eQuarterly

Normal

GTC

SCBZ

Alittleseve

re12

.22.2

17Unclassified

Non

eAnnually

Multifoc

alsp

ikean

dwav

eAbs

ence

VPA

Alittleseve

re8.0

5.0

18Unclassified

Non

eBiannually

Normal

Abs

ence

LEV,V

PANot

atallseve

re7.5

7.2

ADHD,A

tten

tion

Defi

citHyp

eractivity

Disorder;ACE,

Acetazo

lamide;

AED

s,Anti-Epile

ptic

Drugs;CLB

,Cloba

zam;CBZ,

Carba

mazep

ine;

ETX,E

thosuximide;

GEF

Sþ,G

enetic

Epile

psy

withFe

brile

SeizuresPlus;

GTC

S,Gen

eralised

Tonic–Clonic

Seizures;

LEV,L

evetiracetam

;LTG,L

amotrigine;

PHT,

Phen

ytoin;VPA

,Sod

ium

Valproate.

Table 2Clinical neuropsychological instruments.

Domain Test: subtest Score used

Intelligence WASI: vocabulary &matrices

Full Scale Intelligence Quotient(FSIQ)M¼100, SD¼15

Short-term recall WRAML2 Story Memory Age scaled scoresM¼10, SD¼3

CMS Dot Location Age scaled scoresM¼10, SD¼3

CMS: Children's Memory Scale (Cohen, 1997); WASI: Wechsler Abbreviated Scale ofIntelligence (Wechsler, 1999); WRAML2: Wide Range Assessment of Memory andLearning: Second Edition (Sheslow and Adams, 2003).

M.B. Gascoigne et al. / Neuropsychologia 66 (2015) 10–1712

severity of postictal period, and interference of epilepsy or drugswith daily activities. This instrument has been shown to have goodconstruct validity in addition to high inter-rater (weighted j¼0.85)and test–retest reliability (weighted j¼0.90).

2.3. Children's Autobiographical Interview (CAI)

Autobiographical recall was assessed with the CAI (Willoughbyet al., 2012, manual acquired through personal communication), aversion of the Autobiographical Interview (AI; Levine et al., 2002)adapted for children. Originally developed for adults, the AI re-quires participants to recall and elaborate on personally-experi-enced events, specific to a time and place, from five separateperiods of their lives. In contrast, the CAI requires children to recalltwo separate events, experienced at any point in their relativelyshort lives (except from the month-long period immediately priorto assessment). All participants administered the CAI were alsoprovided with a sample list of life events, in order to help themidentify appropriate events to describe in the assessment, al-though participants were free to recall any event, irrespective ofthe suggestions contained in the list.

Each memory was recalled over three separate conditions ofthe CAI: (i) Free Recall, (ii) General Probe and (iii) Specific Probe.The initial condition, Free Recall, required participants to recall asmuch information as possible about an event (up to 5 min induration) without any interruptions from the interviewer. Duringthe General Probe condition, participants were prompted to recallany additional details. In the event of a vague or non-specificmemory being recalled, participants were asked to clarify theevent during this condition. Finally, during the Specific Probecondition, participants were asked a standardised series of ques-tions about the event, pertaining to time, location, sensory/per-ceptual and emotional/cognitive details. In order to prevent anycontamination, the Specific Probe condition was only administeredonce the Free Recall and General Probe conditions had been ad-ministered for both events.

On completion of all conditions of the CAI, participants wereasked to rate each memory on each of the following domains:ability to visualise the event (1¼cannot see it at all, 7¼reallyclear), change in emotions from before to after the event (1¼nochange, 7¼ lots of change), current personal importance of theevent (1¼not important, 7¼most important event), personal im-portance at time of event (1¼not important, 7¼most importantevent ), frequency of memory rehearsal (1¼once every few years,7¼everyday), confidence about the recollection (1¼not sure,7¼really sure) and memory strength (1¼not strong, 7¼reallystrong).Visual scales, which included pictures depicting possibleresponse options, were provided to participants, in order to aidtheir understanding of the rating task.

Table 3Demographic, cognitive and clinical characteristics.

IGE (n¼18)mean (SD)

Control(n¼42) mean(SD)

Test ofsignificance

p

Age 10.7 (2.5) 11.7 (2.8) t(57)¼�1.3 0.21Sex (F/M) 8/10 21/21 χ2¼0.16 0.69SES 12.4 (5.1) 10.1 (7.4) t(57)¼1.2 0.24FSIQ 101.8 (8.7) 112.4 (10.3) t(57)¼�3.8 o0.001

WRAML2 Story MemoryImmediate recall 9.7 (2.9) 12.2 (1.9) t(57)¼�4.0 o0.001Delayed recall(30 min)

9.0 (2.9) 11.9 (2.0) t(57)¼�4.3 o0.001

CMS Dot LocationsImmediate recall 9.6 (3.6) 10.2 (3.1) t(57)¼�0.7 0.49Delayed recall(30 min)

10.2 (3.2) 10.4 (3.0) t(57)¼�0.2 0.83

Mean number ofAEDs

1.2 (0.4) – – –

Age at epilepsydiagnosis

6.2 (3.3) – – –

Proportion of lifewith epilepsy

46.7%(22.6%)

– – –

Comorbid LD (yes/no)

1/17 – – –

ADHD (yes/no) 1/17 – – –

Epilepsy severityrating (GASE)

2.2 (1.8) – – –

AED: Anti-Epileptic Drug; CMS: Children's Memory Scale (Cohen, 1997); FSIQ: FullScale Intelligence Quotient; GASE: Global Assessment of Severity of Epilepsy(Speechley et al., 2008), IGE: Idiopathic Generalised Epilepsy; LD: Learning Dis-ability; SES: Socioeconomic status; WRAML2: Wide Range Assessment of Memoryand Learning, Second Edition (Sheslow and Adams, 2003).

M.B. Gascoigne et al. / Neuropsychologia 66 (2015) 10–17 13

The entire CAI was recorded and transcribed before eachmemory was scored according to the guidelines contained withinthe AI scoring manual (Levine et al., 2002). Details within eachmemory were classified as either (i) episodic (pertaining directlyto the main episode and placed in a particular spatio-temporalcontext, suggestive of the re-experiencing of the main event) or(ii) semantic (representing general knowledge about the world orthe participant that does not entail re-experiencing the event).Composite scores [(memory 1þmemory 2)/2] were obtained forboth episodic and semantic details for each condition of the CAIinterview: (i) Free Recall, (ii) General Probe (Free RecallþGeneralProbe) and (iii) Specific Probe (Free RecallþGeneral Pro-beþSpecific Probe). Finally, examiners also assigned a compositerating [ranging from 0 (not at all rich) to 18 (extremely rich)] toeach memory, in order to reflect the overall richness of the epi-sodic details within each memory (see Levine et al. (2002) for adescription of these ratings).

The transcript of each recalled memory was initially scored byone investigator (MG) before another investigator scored tenrandomly selected memories. Both experimenters had receivedtraining in scoring, having completed the practice set of memoriesprovided with the AI scoring manual (Levine et al., 2002) andachieved intra-class inter-rater correlations ranging from 0.89 to0.99. The intra-class inter-rater correlations for the compositescores obtained on the CAI were (i) Free Recall: 0.96 and 0.80 forepisodic and semantic details, respectively, (ii) General Probe: 0.96and 0.80 for internal and external details, respectively, and (iii)Specific Probe: 0.91 and 0.76 for internal and external details,respectively.

2.4. Procedure

Only participants who themselves agreed to take part andwhose parents gave informed written consent participated in thestudy. The medical records of participants with IGE were reviewedto obtain information of relevance for the study, which was laterverified by treating paediatric neurologists. A total of 21 childrenwith IGE were approached and 18 (86%) consented. A total of 15out of 18 patients with IGE underwent Magnetic Resonance Ima-ging (MRI), while one underwent a computed tomography scan.MRI examinations were carried out on a 1.5-T clinical MR system.No abnormalities were identified in any patient and no structuralabnormalities were seen in the temporal lobes. Two patients didnot undergo imaging as the clinical risks of a general anaestheticwere not justified by the patients' relatively mild generalisedepilepsy. Prior to the assessment, parents were interviewed abouttheir child's medical and developmental history, relevant epilepsyand SES variables, and asked to complete a set of questionnaires.All children were seen for an assessment on their own. The as-sessment took approximately 90 min to complete and included abattery of tests administered in a set order. The CAI took anaverage of 25 min to administer. One researcher (MG) adminis-tered all of the assessments.

2.5. Statistical analysis

For variables that were normally distributed, between groupdifferences were examined using independent t-tests and one-wayANOVA with Sidak post-hoc tests. Where normality assumptionswere not met, Mann–Whitney U tests were employed to examinebetween group differences. Correlations were conducted usingPearson's correlation coefficient or Spearman's rho (rs), whilepartial correlations were used to control for chronological age. Chi-square tests were used to assess between-group differences for sexdistribution. Finally, linear regressions were undertaken within theIGE group to identify predictor variables of CAI scores. Only

variables which significantly correlated with CAI scores or whichresulted in significant between-group differences were included inthe regression analyses. These variables were included in a hier-archical multiple regression (block entry) analysis, in order to as-sess their individual impact in predicting CAI scores. Their order ofentry into the regression analysis was determined by the strengthof their association with outcome variable. That is, the predictorvariable with the strongest association with autobiographical re-call was entered first, while the variable with the weakest asso-ciation was added last.

3. Results

3.1. Background demographic and clinical variables

The IGE and control groups did not differ significantly in age,sex distribution or SES (see Table 3). Compared with the controlgroup, the IGE group was found to have significantly lower FSIQscores (see Table 3). FSIQ was not included as a covariate in thesubsequent analyses for two main reasons. First, among the IGEparticipants, FSIQ was well within the average range and was notrelated to the recall of autobiographical memory details in the CAI,either during the Free Recall (Episodic: rs¼0.12, p¼0.63; Seman-tic: rs¼0.01, p¼0.96), General Probe (Episodic: rs¼0.09, p¼0.72;Semantic: rs¼0.02, p¼0.93) or Specific Probe conditions (Episodic:rs¼0.22, p¼0.38; Semantic: rs¼0.13, p¼0.62). Second, lower FSIQin the IGE group is an expected, integral part of this neurologicalcondition in children (Nolan et al., 2004; Singhi et al., 1992), inwhich case it was not necessary to include it as a covariate (Denniset al., 2009).

Fig. 1. Children's Autobiographical Interview: number of Episodic and Semanticdetails by group and recall condition. n po0.05; nn po0.01; IGE: Idiopathic Gen-eralised Epilepsy. Boxes represent the inter-quartile range, which contains databetween the 25th and 75th percentiles. The median is represented by a horizontalline within each box. Whiskers represent minimum and maximum values.

M.B. Gascoigne et al. / Neuropsychologia 66 (2015) 10–1714

3.2. Children's Autobiographical Interview (CAI)

Scores obtained across the three conditions of the CAI arepresented in Fig.1. The IGE group recalled significantly fewer epi-sodic details than the control group in the Free Recall condition[median (Mdn)¼14.5, interquartile range (IQR)¼13.0 vs.Mdn¼21.8, IQR¼20.9; p¼0.03], General Probe (Mdn¼16.0,IQR¼15.1 vs. Mdn¼22.0, IQR¼22.8; p¼0.02) and Specific Probe(Mdn¼24.3, IQR¼21.1 vs. Mdn¼38.0, IQR¼25.1; p¼0.001) con-ditions of the interview. In contrast, no differences were foundbetween the IGE and control groups in the recall of semantic de-tails at either the Free Recall (Mdn¼2.0, IQR¼5.0 vs. Mdn¼3.5,IQR¼4.5; p¼0.15), General Probe (Mdn¼2.0, IQR¼5.0 vs.Mdn¼3.5, IQR¼4.5; p¼0.17) or Specific Probe conditions(Mdn¼4.3, IQR¼6.3 vs. Mdn¼6.3, IQR¼9.3; p¼0.22).

As no between-group differences were found for the recall ofsemantic details during any condition of recall, and to reduce thenumber of unnecessary comparisons, we only undertook furtheranalyses on the recall of episodic details.

3.3. Relations with chronological age

Correlational analyses examining the association between ageand recall of episodic details were performed separately for theIGE and control groups. A significant positive correlation wasfound between age and the Free Recall of episodic details withinthe control (rs¼0.50, p¼0.001), but not IGE group (rs¼0.41,

Table 4Children's Autobiographical Interview: participants' ratings of phenomenological qualit

IGE (n¼18)

How clearly can you visualise this event? 4.9 (1.3)How much did your emotional state change after it happened? 4.3 (1.2)How personally important is this event to you now? 3.8 (1.6)How personally important was this event to you then? 4.8 (1.6)On average, how often do you think or talk about this event? 3.2 (1.7)How sure are you of what you just remembered? 5.0 (1.7)How strong is the memory of the event? 4.3 (1.7)

IGE: Idiopathic Generalised Epilepsy.

p¼0.09). However, significant correlations between age and epi-sodic recall were found for both the control and IGE groups duringthe General Probe (rs¼0.51, p¼0.001; rs¼0.49, p¼0.04, respec-tively) and Specific Probe conditions (rs¼0.54, po0.001; rs¼0.56,p¼0.02, respectively), indicating that older children recalled moreepisodic details.

3.4. Relations with learning of new material and short-term recall

The performance of both groups on standardised memory teststhat required recall of newly learned materials immediately afterexposure and following a short (30 min) delay is also shown inTable 3. Although no differences between the IGE and controlgroups were found on the CMS Dot Location subtest, the IGE groupobtained significantly lower scores in immediate and delayed re-call on the WRAML2 Story Memory subtest. As a between-groupdifference was found for the latter standardised test, correlationalanalyses within the IGE group were only undertaken betweenepisodic recall and scores obtained on WRAML2 Story Memory.Marginally non-significant correlations were found between therecall of episodic details at all conditions of the CAI and scoresobtained on the immediate (rs¼0.45–0.48, p¼0.051–0.07) anddelayed WRAML2 Story Memory recall (rs¼0.42–0.48, p¼0.051–0.09).

3.5. Relations between epilepsy-related factors and CAI

After using partial correlations to control for chronological age,a significant correlation was found between the recall of episodicdetails during the Free Recall condition and age at epilepsy diag-nosis (r¼0.54, p¼0.024), where children diagnosed later recalledmore episodic details. The length of time diagnosed with IGE alsocorrelated with the recall of episodic details during the Free Recallcondition (r¼�0.52, p¼0.034) with a longer proportion of lifewith IGE being associated with the recall of fewer episodic details.However, no significant correlations were found between age atdiagnosis/proportion of life with IGE and recall of episodic detailsin the General Probe (r¼0.48, p¼0.053/r¼�0.46, p¼0.062) orSpecific Probe conditions (r¼0.41, p¼0.10/r¼�0.40, p¼0.12). Fi-nally, no significant correlations were found between the recall ofepisodic details at any condition of the CAI and epilepsy severityratings on the GASE scale (ps40.81) or the number of anti-epi-leptic drugs taken (ps40.52).

3.6. Memory ratings

Examiner ratings of the overall richness of autobiographicalrecall were found to be significantly lower for the IGE groupcompared to the control group in the Free Recall (M¼5.7, SD¼2.3vs. M¼8.4, SD¼3.4, respectively; t¼�3.30, p¼0.002) and SpecificProbe conditions (M¼8.9, SD¼3.1 vs. M¼12.9, SD¼2.8, respec-tively; t¼�4.46, po0.001).

ies, by group.

mean (SD) Control (n¼42) mean (SD) t p

4.9 (1.1) �0.2 0.984.0 (1.5) 0.6 0.544.3 (1.4) �1.3 0.215.2(1.3) �1.0 0.343.9 (1.7) �1.2 0.235.6 (1.0) �1.2 0.245.4 (1.0) �2.9 0.01

Table 5Hierarchical multivariate regression analyses of epilepsy and cognitive variables forprediction of the Children's Autobiographical Interview: episodic details recalled inthree conditions (Free Recall, General Probe and Specific Probe).

B SE B β R2 Change inR2

Free recallAge at epilepsy diagnosis 1.47 0.49 0.61 0.37 0.009Proportion of life with epilepsy �8.38 18.61 �0.24 0.38 0.66WRAML2 Story Memory (im-mediate recall)

1.17 0.68 0.43 0.50 0.11

WRAML2 Story Memory (de-layed recall)

�1.4 1.19 �0.52 0.55 0.26

General probeAge 1.35 0.82 0.39 0.15 0.12Age at epilepsy diagnosis 1.65 0.82 0.64 0.34 0.06Proportion of life with epilepsy 1.35 50.44 0.04 0.34 0.84WRAML2 Story Memory (im-mediate recall)

1.14 0.81 0.39 0.44 0.16

WRAML2 Story Memory (de-layed recall)

�1.12 1.45 �0.38 0.47 0.44

Specific probeAge 2.67 1.11 0.53 0.28 0.03Age at epilepsy diagnosis 1.92 1.14 0.51 0.40 0.11Proportion of life with epilepsy 4.64 70.46 0.08 0.40 0.95WRAML2 Story Memory (im-mediate recall)

1.20 1.17 0.28 0.45 0.33

WRAML2 Story Memory (de-layed recall)

�2.01 2.07 �0.47 0.49 0.35

WRAML2: Wide Range Assessment of Memory and Learning, Second Edition.

M.B. Gascoigne et al. / Neuropsychologia 66 (2015) 10–17 15

Analysis of participants' ratings of the phenomenological qua-lities of recalled events showed that, within the memory strengthdomain, IGE participants' ratings were significantly lower com-pared to the controls (see Table 4). However, no between groupdifference was found on the remaining domains: visual intensity,emotional change, current importance, past importance andconfidence.

3.7. Regression analyses

Hierarchical regression analyses indicated that age at epilepsydiagnosis was a significant predictor of episodic recall during theFree Recall condition of the CAI (F(1,16)¼8.9, p¼0.009), explaining37% of its variance (see Table 5). Patient age was a significantpredictor of recall during the Specific Probe condition (F(1,16)¼5.8, p¼0.029), explaining 28% of its variance. None of the re-maining predictors made significant contributions in any recallcondition (all ps40.05), although age at epilepsy diagnosis wasmarginally non-significant in the General Probe condition.

4. Discussion

To our knowledge, this is the first study to examine recall ofautobiographical memories in patients with epilepsy who are freeof structural brain abnormalities, children with IGE. The studyyielded several novel findings. First, the most striking finding ofour study is of deficits in the recall of episodic, but not semantic,autobiographical details in children with IGE. This deficit wasevident, irrespective of whether children with IGE recalled episo-dic details spontaneously or if they received general or directedretrieval support. In addition, children with IGE rated theirmemories for personally-experienced events as being weaker thancontrols. Second, amongst epilepsy factors, the age at epilepsydiagnosis and proportion of life with epilepsy both were sig-nificantly associated with recall of episodic details, where an

earlier onset and greater proportion of life with epilepsy wereassociated with poorer recall, but only when no prompts weregiven. Third, the associations between recall of episodic detailsand anterograde verbal memory were moderate in size and mar-ginally significant. Fourth, regression analyses showed that onlyage at epilepsy diagnosis and patient age (but neither proportionof life with epilepsy nor anterograde memory performance), sig-nificantly predicted the spontaneous and prompted recall of epi-sodic autobiographical details, respectively. Finally, these findingshave considerable implications for established theories of mem-ory. In particular, they are at odds with MTT, which suggests thatthe formation and retrieval of autobiographical memories is de-termined by hippocampal integrity.

Several previous adult studies that involved patients withepilepsy have largely attributed deficits in recall of auto-biographical episodes to the presence of temporal lobe (especiallyhippocampal) seizure focus or pathology (Addis et al., 2007; Lahet al., 2006; St-Laurent et al., 2009; Viskontas et al., 2000; Volt-zenlogel et al., 2006). Temporal lobe pathology is not the onlyinstance when recall of episodic details may be disrupted in pa-tients with epilepsy. Our findings indicate that generalised seizureactivity may affect either the storage or retrieval of episodicmemory details, even in the absence of temporal lobe seizure fo-cus. It is possible that seizure activity has disrupted the function ofselect cortical areas within the distributed network that have beenassociated with the recall of autobiographical memories, such asthe prefrontal cortex (Conway et al., 1999; Maguire, 2001; Svobodaet al., 2006) or lateral and medial parietal cortices (Hassabis et al.,2007; Wagner et al., 2005). Alternatively, seizures may have in-terfered with the establishment of connections between variousbrain regions that may be required to form a gestalt of an episode.These findings may potentially have significant implications forcurrent theories of autobiographical memory. Notably, thesefindings are difficult to reconcile with MTT, which suggests thatthe hippocampus is critical not only for the formation but also forthe retrieval of autobiographical memories indefinitely.

Deficits in the recall of personally-experienced events were stillpresent, despite the provision of retrieval support, suggesting thatchildren with IGE may have difficulties with both the storage andretrieval of information. This result is consistent with other studiesthat have failed to find any beneficial effect of retrieval support onepisodic recall, either in adult patients with hippocampal damage(Rosenbaum et al., 2011; St-Laurent et al., 2009; Steinvorth et al.,2005) or transient epileptic amnesia (Milton et al., 2010), or inchildren with hippocampal dysfunction due to thyroid hormonedeficiency (Willoughby et al., 2013).

Like many (but not all) previous studies conducted with pa-tients with (albeit temporal lobe) epilepsy (e.g. Addis et al., 2007;St-Laurent et al., 2009; Viskontas et al., 2000; Voltzenlogel et al.,2006), we found that children with IGE had deficits in the recall ofepisodic, but not semantic details of personally-experienced epi-sodes. This finding may be due to the fact that the measure used inthe current study, the CAI, was originally developed to capturedetails that are internal to a specific episode, episodic details. TheCAI also provided a score for recalled details that were not internalto the specific event; semantic details. Nevertheless, this score isbased not only on facts, but also other extraneous data, such asrepetitions and editorialising statements, which suggest that amore precise measure of semantic details may be warranted.However, our findings could also be explained by the greatervulnerability of episodic memory to disruption. That is, episodicmemories are experienced only once, meaning that the record ofthe memory is unique and cannot be re-established. In addition,the ability to recall episodic details may also not have reached fullmaturity in some participants. Consistent with previous develop-mental studies (Picard et al., 2009; Piolino et al., 2007; Willoughby

M.B. Gascoigne et al. / Neuropsychologia 66 (2015) 10–1716

et al., 2012), significant associations were found between recall ofepisodic details and chronological age in both groups, except inthe spontaneous recall condition within the IGE group. Never-theless, the association within the spontaneous recall conditionwas of moderate size but was not statistically significant due to thesample size and hence limited power.

With respect to epilepsy variables, recall of fewer auto-biographical episodic details was associated with early age ofseizure diagnosis and greater proportion of life with epilepsydisorder, but not with the overall rating of epilepsy severity orpolytherapy. Early age of diagnosis, however, was found to be aparticularly potent predictor of impoverished recall of auto-biographical details. This finding suggests that seizures may in-terfere with formation of these types of memories in the first in-stance. In our study, these deficits may be secondary to the effectsof seizures on the distributed network of structures which, ac-cording to CCT (but not MTT), plays a role in the storage and re-trieval of autobiographical episodic details. Consistent with thispossibility is the observation of Kaaden and Helmstaedter (2009)who pointed out that in patients with TLE, early age of onset didnot appear to affect specific cognitive skills typically associatedwith temporomesial structures, but instead seemed to interruptdistant cortical networks, thereby affecting tasks which rely to adegree on extramesial or “whole-brain” functioning.

Surprisingly, but consistent with the previous adult (Lah et al.,2006) and child (Gascoigne et al., 2013) studies, deficits in newlearning and recall of information following short (20–30 min)delays that were evident on standardised memory tests did notpredict recall of episodic autobiographical details. Studies invol-ving patients with other neurological disorders (Mayes et al., 1997;Shimamura and Squire, 1986) found that the strength of the as-sociation between recall for newly-learned information and au-tobiographical details was dependent on the time period assessed;the association was stronger for more recent autobiographicalmemories, suggesting that remote autobiographical recall may bedistinct from and unrelated to new learning ability.

It is important to note that our study is not without limitations.Firstly, it is acknowledged that seizure activity may not be solelyresponsible for the memory deficit found in this study. It is pos-sible that both generalised seizures and this memory deficit mayhave both arisen from the same, albeit unknown (idiopathic)cause. Secondly, we did not measure seizures directly, insteadrelying on an epilepsy severity scale which considered a variety ofvariables, including seizure severity. Finally, as no hippocampalvolumetric data were collected, it was not possible to directly as-sess hippocampal integrity in the patients with IGE. Nevertheless,the MRI scans collected in 15 out of 18 patients who participatedin our study failed to reveal any evidence of structural brain ab-normalities, which is typical of patients with IGE (Wieshmann,2003). Moreover, other neurological data were not suggestive oftemporal lobe epilepsy focus.

Despite these limitations, our novel findings are of clinical re-levance, theoretical significance, and challenge the notion thatepisodic autobiographical recall is largely determined by hippo-campal integrity in patients with epilepsy. The apparent associa-tion between impoverished recall and early age of epilepsy diag-nosis suggests that the feasibility of developing and implementinginterventions aimed at enhancing autobiographical retrieval mayneed to be explored in children with epilepsy. The deficits in recallof episodic event details among patients with IGE is consistentwith CCT, but not MTT, as it suggests that generalised seizures oran underlying idiopathic factor causing these seizures may ad-versely affect a wider cortical network associated with the re-trieval of episodic details and may have a cumulative impact onautobiographical recall over time.

Acknowledgements

We would like to thank Ms. Chloe Gott from the University ofSydney for assisting with the CAI scoring and Dr. Jayne Antony atthe Children's Hospital at Westmead for assistance in recruitingpatients. MG was supported by a postgraduate scholarship fromthe University of Sydney and the ARC-CCD Ph.D. completionscholarship. Sunny Lah was in part supported by the University ofSydney Thompson Fellowship. Finally, we would like to expressour gratitude to all participants and their parents for taking part inthis study.

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