Neuropsychologia 49 (2011) 2417–2426

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

Accelerated long-term forgetting in temporal lobe but not idiopathic

generalised epilepsy
N. Muhlert a , R.A. Grünewald b , N.M. Hunkin a , M. Reuber b ,
S. Howell b , H. Reynders c , C.L. Isaac a,c,∗
a
Department of Psychology, University of Sheffield, Sheffield, UK
b
Department of Neurology, Sheffield Teaching Hospitals NHS Foundation Trust, Royal Hallamshire Hospital, Sheffield, UK
c
Clinical Neuropsychology Services, Sheffield Teaching Hospitals NHS Foundation Trust, Royal Hallamshire Hospital, Sheffield, UK

a r t i c l e i n f o a b s t r a c t

Article history: Temporal lobe epilepsy (TLE) has been associated with the phenomenon of accelerated long-term forget-
Received 19 January 2011 ting (ALF), in which memories are retained normally over short delays but are then lost at an accelerated
Received in revised form 5 April 2011 rate over days or weeks. The causes of ALF, and whether it represents a consolidation deficit distinct from
Accepted 14 April 2011
the one associated with forgetting over short delays, remain unclear. In addition, methodological issues
Available online 20 April 2011
have made results of some previous studies difficult to interpret. This study used improved methodology
to investigate the role of seizure activity in ALF. Forgetting was assessed in participants with TLE (who
Keywords:
have involvement of temporal lobe structures) and idiopathic generalised epilepsy (IGE; in which seizures
Temporal lobe epilepsy
Idiopathic generalised epilepsy
occur in the absence of identified structural pathology in the temporal lobes). Learning of novel stimuli
Memory was matched between patients with TLE, patients with IGE and healthy controls matched for age and IQ.
Accelerated long-term forgetting Results indicated that the TLE group showed accelerated forgetting between 30-min and three-weeks,
but not between 40-s and 30-min. In contrast, rates of forgetting did not differ between patients with
IGE and controls. We conclude that (1) ALF can be demonstrated in TLE in the absence of methodological
confounds; (2) ALF is unlikely to be related to the experience of epilepsy that does not involve the tem-
poral lobes; (3) neither seizures during the three-week delay nor polytherapy was associated with ALF.

© 2011 Elsevier Ltd. All rights reserved.

1. Introduction a slower consolidation process that normally operates over delays

Temporal lobe epilepsy (TLE) is characterised by recurrent
seizures originating in the temporal lobes. Given the involvement
of these structures in memory, it is unsurprising that TLE has fre-
quently been associated with memory impairments (Giovagnoli
& Avanzini, 1999; Giovagnoli, Cassaza, Broggi, & Avanzini, 1996;
Hendriks et al., 2003).
More recently TLE has been associated with the phenomenon
of accelerated long-term forgetting (ALF). This phenomenon, also
termed ‘long-term amnesia,’ is characterised by normal acquisition
and retention of memories over short delays of up to 30 min but
abnormally fast forgetting over a period of days or weeks thereafter
(Butler et al., 2007; Kapur et al., 1997). Abnormally fast forgetting
has typically been attributed to a deficit in consolidation processes
(e.g. Isaac & Mayes, 1999a, 1999b). ALF is theoretically important
because it implies that an initial consolidation process is normal but
∗ Corresponding author at: Clinical Psychology Unit, Department of Psychology,
University of Sheffield, S10 2HN, UK. Tel.: +44 114 222 6639; fax: +44 114 222 6610.
E-mail address: c.l.isaac@sheffield.ac.uk (C.L. Isaac).
of days or weeks is compromised. This explanation is consistent
with the theory of Alvarez and Squire (1994), which postulates
that initial consolidation of memories depends on medial tempo-
ral lobe structures but that over time memories gradually become
established in neocortex, eventually becoming independent of the
medial temporal lobe.
ALF was originally identified in a number of case studies.
These cases had varying aetiologies including anoxia (De Renzi &
Lucchelli, 1993), encephalitis associated with paraneoplastic dis-
ease (O’Connor, Sieggreen, Ahern, Schomer, & Mesulam, 1997),
head injury (Kapur et al., 1996; Mayes et al., 2003) and uniden-
tified aetiology (Kapur et al., 1997; Lucchelli & Spinnler, 1998).
However, all but one of these patients (De Renzi & Lucchelli, 1993)
also suffered from epilepsy. Mayes et al. (2003) identified a num-
ber of potential causes for ALF including the possibility that damage
to temporal lobe structures outside the medial temporal lobe pre-
vents later consolidation, that transfer to neocortex is disrupted by
seizure activity, that medial temporal lobe function is disrupted by
seizure activity, or that ALF is simply a mild form of amnesia associ-
ated with subtle medial temporal lobe lesions insufficient to cause
disruption at short delays.

0028-3932/$ – see front matter © 2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.neuropsychologia.2011.04.018
2418 N. Muhlert et al. / Neuropsychologia 49 (2011) 2417–2426
More recent studies have attempted to investigate the possi-
bility that ALF is related directly to TLE by investigating forgetting
in patients with TLE without the atypical aetiologies of the single-
case patients. Three studies (Blake, Wroe, Breen, & McCarthy, 2000;
Mameniskiene, Jatuzis, Kaubrys, & Budrys, 2006; Martin et al.,
1991) have reported ALF in groups with TLE and Jansari, Davis,
McGibbon, Firminger, and Kapur (2010) reported ALF in a case
study of a patient with TLE. In addition, three studies (Butler et al.,
2007; Manes, Graham, Zeman, Calcagno, & Hodges, 2005; Muhlert,
Milton, Butler, Kapur, & Zeman, 2010) have reported ALF in groups
with transient epileptic amnesia, a phenomenon related to TLE
and associated with recurrent attacks of transient amnesia in the
context of ongoing difficulties with autobiographical and remote
memory. However findings of ALF in groups with TLE have fre-
quently not been replicated (Bell, 2006; Bell, Fine, Dow, Seidenberg,
& Hermann, 2005; Giovagnoli, Cassaza, & Avanzini, 1995; Howard
et al., 2010). This implies either that (1) ALF is not necessarily char-
acteristic of TLE and may depend on individual epilepsy variables
or that (2) the phenomenon of ALF relates to methodological issues.
In relation to the first possibility, studies have investigated fac-
tors relating to structural pathology, antiepileptic medication and
seizure variables.
Structural lesions have been reported in a minority of patients
with ALF. Three of the 9 patients showed ALF in Blake et al. (2000);
11 of the 70 patients in Mameniskiene et al. (2006); 3 of the 10
patients in Manes et al. (2005); and none of the 24 patients in Butler
et al. (2007) had structural lesions. However, none of these stud-
ies included detailed structural brain analysis such as volumetric
measures. In one study that did include volumetry (Butler et al.,
2009), subtle hippocampal atrophy was reported in patients with
transient epileptic amnesia, a subgroup of whom showed ALF. This
atrophy correlated negatively with retention over 30-min but not
over one week (Butler et al., 2009). This indicates that hippocam-
pal function is important for retention over short delays. Whether
it underlies ALF remains uncertain.
The effects of antiepileptic medication on ALF have been
reported in a single case, in which ALF was demonstrated both
before and after the administration of antiepileptic medication
(Jansari et al., 2010). ALF has also been reported in patients with
transient epileptic amnesia in whom attacks usually resolve even
on relatively low doses of antiepileptic medication, doses which
would be unlikely to lead to memory problems (e.g. Butler et al.,
2007; Muhlert et al., 2010).
The relationship between seizures during the study period
and retention is variable. Patients with TLE who experience
seizures during retention periods have shown both greater for-
getting (Mameniskiene et al., 2006) and similar forgetting (Bergin,
Thompson, Fish, & Shorvon, 1995; Blake et al., 2000) to those who
were seizure-free. ALF has also been reported in patients who have
been seizure-free during, and for a minimum of four-months prior
to, testing (Butler et al., 2007; Muhlert et al., 2010).
The role of seizures in ALF can also be investigated by examining
forgetting in patients with extra-temporal forms of epilepsy. Idio-
pathic generalised epilepsies (IGE) are characterised by bilateral
seizure onset on electroencephalography without structural brain
lesions (Commission of ILAE, 1989). Evidence for ALF in IGE would
suggest that epilepsy variables other than lesions are sufficient to
cause ALF. This may include seizure-related activity, antiepileptic
medication, mood or other psychosocial disturbances.
In the only study of ALF in IGE, children with IGE showed
impaired one-week retention on story recall, but normal reten-
tion on story recognition and a visual recall task (Davidson, Dorris,
O’Regan, & Zuber, 2007). However, these authors attributed their
findings to inefficient learning rather than ALF.
The second possibility outlined above is that the presence or
absence of ALF is determined by methodological issues. It is well
known that investigation of forgetting rates in groups with memory
impairment involves serious methodological problems (see Isaac &
Mayes, 1999a, 1999b). Difficulties arise when comparing rates of
forgetting across groups that are performing at different levels as
it is known that forgetting curves are not linear and so comparing
performances which may be at different points on the forgetting
curve may result in scaling effects (e.g. Loftus, 1985). This difficulty
affects those studies in which performance of patients at the initial
delay is significantly poorer than that of controls (e.g. Bell, 2006;
Bell et al., 2005; Mameniskiene et al., 2006). One way of addressing
this difficulty is to employ a matching procedure. However, the pro-
cedure of learning to criterion employed by Martin et al. (1991) and
Blake et al. (2000) results in a ceiling effect at the short delays which
may mask group differences. In these cases overlearning (Krueger,
1929) may occur, whereby repeated study-test trials beyond 100%
recall can result in forgetting rates being underestimated over ini-
tial delays (e.g. Driskell, Willis, & Cooper, 1992). Bell (2006) has
attributed the positive findings of ALF in the Martin et al. (1991)
and Blake et al. (2000) studies to these issues, although it should
be noted that neither of these studies reported any group differ-
ences in a number of trials to reach criterion across patient and
control groups. Nevertheless, it remains to be established whether
ALF occurs in TLE in the absence of scaling effects, ceiling effects
and overlearning.
To address these methodological difficulties, we matched learn-
ing by giving poor learners extended exposure to stimuli during
learning. Titrating presentations in this manner have been used
previously to explore forgetting rates in groups with organic
amnesia syndromes (Isaac & Mayes, 1999a, 1999b). Using these
techniques this study had the following three aims. The first aim
was to compare forgetting over delays of up to three-weeks in
TLE, IGE and control groups to determine whether the presence
of generalised seizure activity in the absence of specific tempo-
ral lobe involvement is associated with abnormal forgetting. The
second aim was to conduct individual analyses of forgetting rates
within the three groups of participants to investigate the possibil-
ity of heterogeneity and possible bases for this. The third aim was
to investigate the relationship between rate of forgetting and per-
ceived memory, quality of life, mood and antiepileptic medication.
2. Methods
The study was approved by the South Sheffield Research Ethics Committee. All
participants gave informed consent to participate.
2.1. Participants
Fourteen patients with TLE (ten females and four males), and fourteen with IGE
(eight females and six males) were recruited from the local neurology department.
Fifteen healthy control participants (seven males and eight females) with no neu-
rological conditions or previous head injury were also studied. All participants met
the following inclusion criteria: (1) English as a native language; (2) age between
16 and 75 years; (3) Wechsler Abbreviated Scale of Intelligence (WASI; Wechsler,
1999) Full Scale IQ greater than 80. Patients were allocated to the TLE or IGE groups
by experienced epileptologists on the basis of all available clinical data. For further
clinical details see Table 1.
Patients in the TLE group reported a mean of 3.8 seizures per month. Two were
not on medication, six were on monotherapy, four were on two antiepileptic med-
ication, and two were on three antiepileptic medication (see Table 1).
In the IGE group, four patients had a diagnosis of juvenile myoclonic epilepsy,
one of generalised tonic–clonic seizures on awakening and the remainder of unclas-
sified IGE. These patients reported a mean of 5.4 seizures per month. One was not
on medication, eight were on monotherapy, three were on two antiepileptic medi-
cation, one was on three antiepileptic medication, and one was on four antiepileptic
medication (see Table 1).
A one-way analysis of variance (ANOVA) indicated a significant group difference
for age (F(2,42) = 5.1, p = .010). Post hoc Tukey’s test showed that the TLE group was
older than both IGE (t(26) = −3.0, p = .016) and control groups (t(27) = 2.7, p = .032),
but that there was no significant difference between IGE and control groups (p > .1).
To account for this difference, the TLE group was compared to a sub-group of age-
matched controls (termed CON group), using the age of the youngest patient in the
TLE group (21 years) as a lower limit for selection. The CON group included ten
 N. Muhlert et al. / Neuropsychologia 49 (2011) 2417–2426 2419

Table 1
Patient characteristics. MTS, mesial temporal sclerosis; SPS, simple partial seizure; CPS, complex partial seizure; GTCS, generalised tonic–clonic seizure; AEDs, antiepileptic
medication; LEV, levetiracetam; CRB, carbamazepine; PRG, pregabalin; PHY, phenytoin; LMT, lamotrigine; OXC, oxcarbazepine; SVP, sodium valproate; CLB, clobazam; TPR,
topiramate.

MRI EEG Age Seizure types experienced Age of onset Duration AEDs

TLE
1 Left MTS – 65 SPS, CPS 16 49 LEV
2 Right glioma – 51 SPS, GTCS 50 1
3 Left MTS Left 47 SPS, CPS, GTCS 3 44 CRB, PRG, PHY
4 Normal – 43 CPS 28 15 CRB
5 Right MTS Right 45 CPS, GTCS 25 25 LMT, OXC
6 Left MTS Left 55 SPS, CPS 7 48 CRB, PRG
7 Right MTS – 56 SPS, GTCS 10 46 CRB, PHY, LEV
8 Normal Bilaterala 52 SPS 36 16 PHY
9 Normal – 21 SPS, CPS 13 8
10 Right MTS Bilaterala 42 CPS 28 13 LEV, PRG
11 Right stroke – 37 SPS, GTCS 34 4 LEV
12 Normal Right 48 SPS, CPS, GTCS 19 29 PRG, LMT
13 Right epidermoid cyst – 55 CPS, GTCS 44 11 CRB
14 Left MTS – 32 CPS, GTCS 3 29 CRB
IGE
1 – – 56 GTCS, absence 11 45 LEV, SVP, LMT, CLB
2 – Spike and wave 23 GTCS 10 13 LMT, SVP
3 – – 22 GTCS 13 9 SVP
4 – Slow wave, spikes 27 GTCS, absence 7 20 LMT, TPR, SVP
5 – – 52 GTCS, absence 24 28 LEV
6 – – 35 GTCS 15 20
7 – – 20 GTCS 10 10 SVP, LMT
8 – Poly-spike and wave rhythmic slow-wave 21 GTCS, absence 14 7 LMT
9 – – 25 GTCS, absence 18 7 LEV
10 – Spike and wave 18 GTCS 17 1 LMT
11 – Poly-spike and wave 43 GTCS, absence 22 21 LMT
12 – – 18 GTCS 11 7 LEV, SVP
13 – – 58 GTCS 17 41 SVP
14 – Poly-spike and wave 24 GTCS 20 4 LMT
a
These patients had evidence of seizure onset in left and right temporal lobes on different occasions.

Table 2
Demographics, epilepsy characteristics, and standardised neuropsychological test scores for TLE, IGE, control, and CON groups. T1, independent samples t-tests comparing TLE
to CON groups on the relevant measures (df = 22). T2, independent samples t-tests comparing IGE to control groups on the relevant measures (df = 27). Figures in parentheses
show standard deviations. WASI, Wechsler Abbreviated Scale of Intelligence; WTAR, Wechsler Test of Adult Reading; HADS, Hospital Anxiety and Depression Scale; AMIPB,
Adult Memory and Information Processing Battery; WRMT, Warrington Recognition Memory Test.

TLE CON T1 IGE Control T2

N 14 10 14 15
Gender (M/F) 4/10 3/7 6/8 7/8
Age 46.4 (11.0) 40.0 (13.3) 1.3 31.6 (14.6) 33.3 (15.4) −0.3
Age of onset 22.1 (14.1) – 14.9 (5.0) –
Duration of epilepsy 24.3 (16.9) – 16.6 (13.5) –
WASI
Full scale 112.0 (13.5) 112.7 (10.8) −0.2 113.1 (15.5) 117.5 (12.2) −0.8
Verbal 111.2 (10.3) 111.0 (8.8) 0.3 114.4 (16.4) 116.1 (12.6) −0.3
Performance 106.1 (15.9) 111.6 (12.8) −0.6 108.8 (13.4) 114.8 (11.5) −1.3
WTAR 104.0 (6.7) 107.8 (3.4) −1.6 101.3 (11.2) 107.3 (5.4) −1.6
HADS
Anxiety 7.9 (3.6) 6.5 (3.0) 1.0 7.4 (5.2) 5.7 (3.2) 1.0
Depression 3.1 (2.3) 3.4 (2.6) −0.3 3.6 (2.9) 3.3 (2.4) 0.3
Test of Everyday Attention
Elevator Counting 6.9 (0.3) 7.0 (0) N/Aa 6.7 (0.7) 7.0 (0) N/Aa
Elevator Counting with Distraction 6.9 (3.1) 8.2 (2.9) 1.0 7.5 (2.7) 8.3 (2.7) 0.7
AMIPB list
Learning trials 52.9 (10.6) 60.7 (3.5) −2.1* 59.1 (9.0) 60.6 (3.7) −1.3
Post-interference recall 10.6 (2.8) 12.9 (1.5) −2.6* 12.6 (2.3) 12.6 (1.4) −1.9
Delayed recall 10.6 (2.8) 13.5 (1.7) −2.4* 10. 9 (7.8) 13.3 (1.7) −1.5
AMIPB figure
Copy 78.3 (2.8) 79.4 (0.8) N/A 78.6 (2.1) 79.3 (0.9) N/A
Imm recall 53.4 (17.2) 61.7 (16.6) −1.2 64.7 (13.2) 66.5 (15.2) −0.3
Delayed recall 50.1 (14.6) 60.1 (16.0) −1.6 65.7 (12.4) 59.1 (16.7) 0.9
WRMT
Words 46.1 (4.9) 49.4 (1.1) −2.1* 48.3 (2.1) 49.3 (1.1) −1.5
Faces 39.3 (4.8) 45.3 (3.2) −3.4** 42.1 (4.1) 45.1 (3.2) −1.9
a
Ceiling effects in controls on the Elevator Counting subtest prevented reliable statistical analysis. According to normalised scoring procedure one TLE patient and two
IGE patients performed in possibly abnormal range, and one IGE performed in abnormal range on this test.
*
p < .05.
**
p < .01.
2420 N. Muhlert et al. / Neuropsychologia 49 (2011) 2417–2426
Fig. 1. (a) Procedure for presentation of scenes. For each scene foreground objects were presented individually in front of the background for 2 s. Following presentation of
each of the five objects, the entire scene was presented for 10 s. (b) Recall sheet for beach scene.
participants and was matched to the TLE group for age and IQ. The IGE group was
matched to the controls for age and IQ (see Table 2).
2.2. Materials
Experimental materials were developed specifically for this study. The tests
were piloted on groups of undergraduate and postgraduate students to ensure that
floor and ceiling effects would be avoided as far as possible.
2.2.1. Visual scenes
This test was based on the Family Pictures subtest of the Wechsler Mem-
ory Scale-III (Wechsler, 1997). It was constructed using four background scenes
(beach, park, street, and stage), each with five foreground objects (see Fig. 1a).
The foreground objects were chosen to be relatively incongruent with the scene,
so they could not be guessed from knowledge of the scene alone. The images
for the scenes and objects were downloaded from Internet websites (e.g. Google
images, www.webshots.com). The test was created and presented using E-prime
(Psychology Software Tools, 2002) on a PC laptop. A practice trial preceded presen-
tation of the experimental scenes. This consisted of a safari scene, presented in the
same way as the experimental scenes.
Retention of visual scenes was tested using free recall and recognition
paradigms. Free recall for each scene was assessed on three measures: recall of
foreground objects (item recall: 1 point for each item recalled); recall of the location
of each recalled object (spatial recall: 1 point for each item recalled in the correct
location); and recall of details of each recalled object (descriptive recall: for each
recalled item, 2 points were awarded for two or more attributes of that item, 1
point was awarded if only one attribute was recalled). Free recall of all four scenes
was assessed at each delay.
Recognition for each foreground object was assessed using four-option, forced
choice recognition questions. Three sets of six questions were devised comprising
questions relating to all four scenes. A different set was presented at each delay
and the order was counterbalanced between participants. Two objects were not
tested to ensure equal numbers of questions at each delay (i.e. six images at each
delay = 18 images total). Each recognition question consisted of one target item and
three similar foils, presented against a white background. The position of the correct
answer was varied pseudorandomly between questions, so as to appear equally
often in each position.
2.2.2. Story recall and recognition
Verbal memory was assessed using story recall and recognition. The story
described the journey of a woman from Scotland to the jungles of Gambia and
contained 512 words and 152 units of detail. The story was recorded as a Win-
dows Media Audio file, lasting 2.34 min. At each delay participants were instructed
to recall as much about the story as possible. Participants’ recall of the story was
recorded, transcribed, and scored. A full point was awarded for each exact detail and
half a point was awarded for recall of the gist of an event without specific details.
Story recognition was assessed using four-option forced-choice recognition (e.g.
what was the name of the woman in the story: Stephanie Hunter; Stephanie John-
ston; Sharon Hunter; and Sharon Johnstone). Three sets of twelve questions were
devised and a different set was presented at each delay. The order of sets was
counterbalanced between participants. Each set included questions about informa-
tion presented in the beginning, middle and end parts of the story. The questions
were ordered within each set so that earlier questions would not cue later answers.
The position of the correct answer was varied pseudorandomly between questions,
appearing equally often in each position.
2.2.3. Long-Term Memory Questionnaire
A self-report questionnaire designed for clinical use in the local epilepsy service
was adapted for this study. This consisted of 26 questions each requiring participants
to rate their memory from 1 (very poor) to 10 (perfect). Questions enquired about
memory for places, people, television and reading, public and personal events, time
and appointments, and everyday information. An overall perceived memory rating
was calculated based on the mean score across all questions.
2.2.4. Seizure diary
This was designed to allow patients to record overt seizure activity during the
three-week delay. If patients had seizures, they were asked to record what type of
seizure it was (e.g. generalised tonic–clonic, absences or auras/simple partial), and
the day it occurred.
2.2.5. Quality of life questionnaire
This was assessed in patients using the Quality of Life in Epilepsy question-
naire (QoLIE-31; Vickrey et al., 1993). This contains seven multi-item scales which
assess emotional well-being, social functioning, energy/fatigue, cognitive function-
ing, seizure worry, medication effects, and overall quality of life. An overall QoLIE-31
score, giving a weighted mean of the multi-item scale scores, was used in analyses.
2.2.6. Standard neuropsychological assessment
A battery of standard neuropsychological tests was administered to patients
and controls. This comprised the Wechsler Test of Adult Reading (WTAR; Wechsler,
2001) to provide an estimate of pre-morbid intellectual functioning; the Wech-
sler Abbreviated Scale of Intelligence (WASI; Wechsler, 1999), to assess current
intellectual functioning; the List Learning and Complex Figure subtests of the Adult
Memory and Information Processing Battery (AMIPB; Coughlan & Hollows, 1985), to
assess immediate and short delay verbal and visual recall; the Recognition Memory
Test (RMT; Warrington, 1984), to assess verbal and visual recognition; the Elevator
Counting and Elevator Counting with Distraction subtests of the Test of Everyday
Attention (Robertson, Ward, Ridgeway, & Nimmo-Smith, 1994), to provide a mea-
sure of attention; and the Hospital Anxiety and Depression Scale (HADS; Zigmond
& Snaith, 1983) to assess anxiety and depression.
2.3. Procedure
Testing took place over three sessions, each lasting approximately 2 h. In the
first session demographic and epilepsy-related variables were recorded. Background
neuropsychological tests were then administered in the following order: WASI,
WTAR, list learning and complex figure subtests of the AMIPB. Performances on
the AMIPB memory tests were used to titrate presentations of the experimental
stimuli. The score for each individual was calculated into percentile bands for their
age group, according to normative data. Participants performing above the 25th
percentile were given one presentation of the experimental stimuli, those perform-
ing between 10th and 25th percentiles were given two presentations, and those
performing below the 10th percentile were given three presentations.
In the second session the visual scenes and story experimental tasks were
administered, with the order of presentation counterbalanced to minimise order
effects. Recall and recognition were assessed following a 40-s filled delay (see below)
 N. Muhlert et al. / Neuropsychologia 49 (2011) 2417–2426
and a 30-min filled delay. During the 30-min delay, participants were administered
subtests from the Test of Everyday Attention. After 30-min delayed testing, patients
completed the QoLIE-31 and were given a diary to record any seizures between
the second and third sessions. The participants were not informed that memory for
the stimuli would be subsequently assessed, so as to minimise rehearsal during the
delay.
In the third session which took place three-weeks later, retention of the exper-
imental tests was assessed. In addition, seizure diaries were reviewed, participants
completed the Words and Faces subtests of the RMT, the HADS, and the Long-Term
Memory Questionnaire.
2.3.1. Visual scenes
Administration of the visual scenes test was preceded by training on an inter-
ference task. Participants were presented with arrays of 20–45 symbols featuring
&, £ and X. For each array, participants were asked to state the total number of £
symbols on the screen as quickly as possible. The elements of visual searching and
working memory involved were intended to prevent rehearsal of the visual scenes.
Participants carried out the visual array interference task between presentation of
the visual scenes and initial recall.
Participants were told they would see some scenes, each containing five objects,
and that they should try to remember as many of the objects as possible, their
location and their appearance. The practice scene was presented initially to ensure
participants understood the instructions. The scenes were then shown in a fixed
order: beach scene, park scene, stage scene and street scene. For each scene, fore-
ground objects were presented individually in front of the background for 2 s to
highlight each object (see Fig. 1a). Following presentation of all five objects the
entire scene was presented for 10 s. The four scenes appeared consecutively without
pauses. Scenes were presented one, two, or three times according to the partic-
ipants’ performance on the AMIPB. Participants then carried out the visual array
interference task for 40 s and subsequently recalled the items in each scene, their
spatial location (using bespoke recall sheets; see Fig. 1b), and their appearance. This
procedure was repeated for each of the four scenes and was self-paced.
Visual scenes recognition was carried out at each delay after the recall con-
dition. Participants were administered one of the three sets of recognition trials.
During each trial, four pictures remained on the screen until participants selected
the picture they believed they had seen before.
2.3.2. Story
The story task was preceded by training on an odd/even judgement task
designed to prevent rehearsal of verbal information. This required participants to
read aloud three-digit numbers and say whether they were odd or even as quickly
as possible. Participants were then informed that they would hear a story and that
they should try to remember as many of the details contained in it as possible. The
story was played one, two, or three times based on performance on the AMIPB.
Afterwards, participants completed the odd/even judgement interference task for
40-s. Free recall of the story was then assessed by asking the participant to recall as
much as possible about the story, without cues or prompts.
Story recognition was carried out at each delay after the recall condition.
Questions appeared on the screen and were read aloud by the experimenter. The
participant was asked to select the correct answer to each question from the list of
four answers. Each question remained on the screen until the participant selected a
response.
2.4. Statistical analyses
The performances of patients and their respective controls on the standardised
neuropsychological tests were compared using independent samples t-tests. Perfor-
mances on the experimental tests were then compared between patients and their
respective control by repeated-measures ANOVAs. The Greenhouse-Geisser correc-
tion was applied for non-sphericity where appropriate and can be identified where
there are non-integers in the degrees of freedom. Effect sizes for the ANOVAs were
determined using partial 2 , where .14 is a large effect (Stevens, 2002).
Spatial and descriptive recalls on the visual scenes recall test were scored using
corrected measures (Sp and Des, respectively; see Appendix A) to account for differ-
ences in the number of items recalled.
An individual analysis of retention assessed the number of participants in each
group (TLE, IGE and control) whose retention was greater than 1.96 standard devia-
tions below the mean of the controls (corresponding to an alpha level of 0.05) over
the 30-min delay or over the three-week delay. This was carried out for two pur-
poses. First, it tested Bell’s (2006) finding that there was no significant difference
between control and TLE groups in the number of individual cases showing ALF.
Second, they informed the effects of laterality of epilepsy on forgetting rates. For
this, retention was calculated using residual change score:
1 − (X1 − X2 )
Residual change = × 100
X1
where X1 is performance at the earlier delay, and X2 is performance at the later delay.
This calculated change between 40-s and 30-min delays and between 30-min and
three-week delays.
2421
Table 3
Percentage of TLE, IGE and control participants given one, two or three presentations
of the experimental stimuli.
Number of presentations of stimuli Frequency
TLE IGE Control CON
1 29% 71% 73% 70%
2 64% 29% 20% 20%
3 7% 0% 7% 1%
3. Results
3.1. Standardised tests
Means and standard deviations for performance on the stan-
dardised tests for TLE, IGE, control and CON groups can be seen in
Table 2. Results of independent samples t-tests comparing patients
to their respective control group on these measures are also shown.
Patients with TLE showed significantly worse performance than
the CON group on AMIPB list learning total score, post-interference
recall, and 30-min delayed recall trials and on RMT Face Recog-
nition (see Table 2) but there were no significant differences on
the other standardised tests. IGE and control groups did not differ
significantly in their performance on any of the standardised tests.
3.2. Experimental tests
Numbers of presentations of stimuli given to participants in each
group based on their performance on standardised tests can be
seen in Table 3. Performance on the experimental tests is shown
in Figs. 2 and 3.
Scores on the tests were normally distributed, except on visual
scenes recognition. On this test ceiling effects were seen in TLE,
IGE, control and CON groups at the 40 s and 30 min delays, with
median scores of 6 (i.e. maximum) for each group at these times.
Performance on this test was therefore not entered into any of the
following analyses but can be seen in Fig. 3a.
Performance on the other experimental tests was analysed by
repeated-measures multivariate analysis of variance (MANOVA)
with factors of group (TLE and CON) and delay (40 s, 30 min,
and three-week) across all five tests (item recall, spatial recall,
descriptive recall, story recall, and story recognition). There
was a significant delay by group interaction (Pillai’s trace = 0.46,
F(10,82) = 2.5, p = .014, 2p = .234) indicating that retention differed
significantly between TLE and CON groups.
A MANOVA comparing the performance of IGE and control
groups showed no significant delay by group interaction (Pillai’s
trace = 0.18, F(10,102) = 1.0, p = .427, 2p = .078) indicating no sig-
nificant difference in forgetting rates between the IGE and control
groups on the experimental tests.
Further analyses investigated the significant delay by group (TLE
and CON) interaction by comparing the groups on individual tests.
3.2.1. Individual experimental tests
Independent t-tests were carried out on the data after the 40 s
delay (i.e. initial recall) for each of the experimental tests to assess
whether the TLE and CON groups were performing at similar levels.
The TLE group performed worse than the CON group on spatial
recall at 40 s (t(22) = −2.1, p = .046, r = .41; see Fig. 2b). The perfor-
mances of the two groups on the other tests were not significantly
different (ps > .05).
For each experimental test, performance of TLE and CON
groups was analysed by repeated-measures ANOVA at the three
delays (40 s, 30 min, and three-week). The ANOVAs revealed
significant main effects of delay on each of the experimental
tests (item recall [F(1.0,23.7) = 23.5, p < .001, 2p = .52]; spatial
2422 N. Muhlert et al. / Neuropsychologia 49 (2011) 2417–2426

a Visual Scenes Item Recall a Visual Scenes Recognition

20 6

Mean recognition (Max = 6)

Mean recall score (raw)

15
4 TLE
TLE
10 IGE IGE
Control Control
CON 2 CON
5

0 0
40 second 30 Minute 3 Week 40 second 30 Minute 3 Week

b Story Recall
b Spatial Discrimination Memory (Sp) 80

Mean Recall (Max = 152)

8
Mean spatial score (Sp)

60
TLE
6 TLE IGE
IGE 40
Control
4 Control
CON
CON
20
2

0
0
40 second 30 Minute 3 Week
40 second 30 Minute 3 Week

c Story Recognition
c Corrected Descriptive Recall (Des) 12
Mean Recognition (Max = 12)
Mean descriptive score (Des)

100
9
TLE
75 IGE
TLE
6
IGE Control
50 Control CON
CON 3
25
0
0 40 second 30 Minute 3 Week
40 second 30 Minute 3 Week
Fig. 3. Mean performance of TLE, IGE, control and CON groups on the visual scenes
Fig. 2. Mean performance of TLE, IGE, control and CON groups on the visual scenes recall test. (a) Performances on item recall. (b) Performances on spatial recall. (c)
recall test. (a) Performances on item recall. (b) Performances on spatial recall. (c) Performances on descriptive recall. Error bars show 95% confidence intervals.
Performances on descriptive recall. Error bars show 95% confidence intervals. Sp:
spatial score. Des: descriptive score. Both spatial score and descriptive score are
contingent upon successful recall of items (see Appendix A).
3.3. Effects of seizures

recall [F(1.1,23.8) = 17.6, p < .001, 2p = .53]; descriptive recall

Twelve patients (seven with TLE and five with IGE) experienced
[F(1.1,24.2) = 5.0, p = .031, 2p = .18]; story recall [F(2,44) = 103.1, seizures during the three-week delay (see Table 4). Because of the
p < .001, 2p = .82]; and story recognition [F(2,44) = 31.5, p < .001, small numbers, the different seizure types were collapsed into a
2p = .59]). There were also significant delay by group interac- single variable (seizure or seizure-free).
tions for item recall (F(1.0,23.7) = 4.6, p = .015, 2p = .17), descriptive A MANOVA comparing performances across the five experi-
recall (F(1.1,24.2) = 3.8, p = .049, 2p = 15), and story recogni- mental tests found no delay by group (seizure and seizure-free)
tion (F(2,44) = 4.9, p = .012, 2p = .18), but not for spatial recall interaction over the three delays (Pillai’s trace = 0.19, F(10,98) = 1.0,
p = .420, 2p = .10). Similarly, the delay by group interaction was
(F(1.1,23.8) = 1.5, p = .229, 2p = .06; Fig. 3b) or story recall
not significant when analysing patients with TLE alone (Pillai’s
(F(2,44) = 2.8, p = .074, 2p = .11; Fig. 3b).
The significant interactions for item recall, descriptive recall
and story recognition were investigated using planned inter- Table 4
action contrasts between consecutive delays. Between 40 s and Number and types of seizures reported over the three-week delay by patients with
30 min delays there were no significant delay by group inter- TLE and IGE. Numbers in parentheses indicate the number of seizures experienced
by each patient, respectively.
actions on any of these tests (item recall [F(1,22) = 4.0, p = .058,
2p = .15], descriptive recall [F(1,22) < .01, p = .891, 2p = .01], story TLE IGE
recognition [F(1,22) = .7, p = .415, 2p = .03]). Between 30 min and Simple partial seizures 4 patients (5, 1, 1, and 1)a –
three-week delays there were significant delay by group interac- Complex partial seizures 4 patients (7, 4, 2, and 1)a –
tions on item recall (F(1,22) = 6.2, p = .021, 2p = .22), descriptive Generalised tonic–clonic – 1 patient (1)
seizures
recall (F(1,22) = 4.5, p = .046, 2p = .17), and story recognition Absence seizures – 4 patients
(F(1,22) = 5.1, p = .034, 2p = .18). In each case, this resulted from (76, 18, 3, and 2)
greater forgetting between 30 min and three-weeks in the TLE a
One patient with TLE reported both one simple partial seizure and one complex
group (see Figs. 2a, c, and 3c, respectively). partial seizure.

100
Percentage of participants impaired
80
60
40
20
0
30 Min 3 Week
Item recall
Fig. 4. Percentage of participants in each group impaired between 40-s and 30-min delays (30 min) and between 30-min and three-week delays (3 week) on each of the
experimental tests. Participants performing worse than 1.96 SDs from the mean of the controls were considered impaired.
trace = 0.43, F(10,42) = 1.2, p = .332, 2p = .21) or patients with IGE
alone (Pillai’s trace = 0.63, F(10,42) = 1.9, p = .071, 2p = .31), indicat-
ing that experiencing seizures during the delay did not significantly
affect retention.
3.4. Effects of medication
To assess the effects of medication on memory, patients on
mono-therapy (six TLE and eight IGE) were compared to those on
poly-therapy (six TLE and five IGE). The two patients with TLE who
were not taking antiepileptic medication at the time of testing were
omitted from these analyses.
A MANOVA comparing performances across the five experimen-
tal tests found no delay by group (monotherapy and polytherapy)
interaction over the three delays (Pillai’s trace = 0.11, F(10,86) = .5,
p = .859, 2p = .06). Similar MANOVAs found no delay by group inter-
action in the TLE group alone (Pillai’s trace = 0.65, F(10,34) = 1.7,
p = .130, 2p = .33) or in the IGE group alone (Pillai’s trace = 0.54,
F(10,38) = 1.4, p = .217, 2p = .27).
3.5. Analysis of performance of individuals in the study
The percentage of TLE, IGE and control participants with
impaired retention (defined as forgetting greater than 1.96 stan-
dard deviations from the mean of the control group) over 30 min
and three-week delays can be seen in Fig. 4.
Whereas a similar number of IGE and control participants
showed impaired retention over the three-week delay, a greater
percentage of TLE participants showed impaired retention over this
time (see Fig. 4). Both left and right TLE patients were impaired on
visual scenes and story tests. A greater number of patients with
mesial temporal sclerosis showed impaired retention than non-
mesial temporal sclerosis TLE patients (see Table 5).
3.6. Perceived memory and quality of life
All of the patients and ten of the controls (7 CON) completed
the perceived memory questionnaire. Self-ratings of memory
were lower in the TLE (mean = 5.7, SD = 0.9) than CON group
(mean = 7.8, SD = 1.3; t(19) = −4.2, p < .001, r = .69), and lower in the
IGE (mean = 6.5, SD = 1.4) than control group (mean = 7.7, SD = 1.1;
t(22) = −2.2, p = .041, r = .42).
As with Butler et al. (2009), composite measures of reten-
tion over 30-min (termed ‘zMEM’) and three-week delays (termed
‘zALF’) were calculated. Retention scores were summed on the
three experimental tests on which patients with TLE showed ALF
N. Muhlert et al. / Neuropsychologia 49 (2011) 2417–2426 2423
IGE
Control
TLE
30 Min 3 Week 30 Min 3 Week 30 Min 3 Week 30 Min 3 Week
Spatial recall Descriptive recall Story Recall Story Recognition
(visual scenes item and descriptive recall, and story recognition)
between 40 s and 30 min delays (zMEM), and between 30 min and
three-week delays (zALF), respectively. This summarised forgetting
across the different tests and reduced the number of variables used
in analyses.
Pearson product–moment correlations in patients showed a sig-
nificant correlation between zMEM and perceived memory (r = .4,
p = .014) but there were no significant correlations with QoLIE-
31 full score (r(28) = .2, p = .598), or total HADS score (r(28) = −.1,
p = .843). Similarly, zALF did not correlate with perceived memory
(r(28) = .2, p = .155), QoLIE-31 full score (r(28) = .2, p = .232), or total
HADS score (r(28) = −.1, p = .626).
4. Discussion
This study explored forgetting rates in TLE, IGE and control
groups after matching for learning using titrated presentations.
Once matched for learning, patients with TLE showed normal reten-
tion on all tests over 30-min. Over three weeks, they showed
significantly greater forgetting on visual scenes item recall, descrip-
tive recall and story recognition, compared with age-matched
controls. They exhibited normal retention on spatial recall and story
recall tests. Patients with IGE showed no evidence of increased for-
getting at either 30 min or three-week delays. Seizures during the
delay were not associated with worse retention in either group, nor
was polytherapy, although it should be noted that these analyses
were based on small sample sizes. Forgetting was not significantly
related to perceived memory or quality of life.
The IGE group was not impaired on either standardised or exper-
imental tests. These findings are in line with the view that memory
deficits are rare in IGE (e.g. Hommet, Sauerwein, De Toffol, &
Lassande, 2006). They also indicate that when learning is matched
in the absence of overlearning, patients with IGE show normal
retention. Our findings support those of Davidson et al. (2007)
and also lend credence to their hypothesis that impaired reten-
tion on story recall in their study was related to impaired learning
efficiency.
The TLE group showed significantly worse retention than
controls over the three-week delay on an omnibus assessment.
Analysis of results from the individual tests indicated ALF in three of
the five measures that were included in this analysis (visual scenes
recognition was not included because of a ceiling effect). These
were visual scenes item recall, visual scenes descriptive recall and
story recognition. On one of the two tests on which ALF was not
found (spatial recall), performance of the groups was not success-
fully matched at the short delay and so the results could have been
2424 N. Muhlert et al. / Neuropsychologia 49 (2011) 2417–2426
subject to a scaling effect. On the other (story recall) four patients
with TLE performed at floor level at the three-week delay and so
floor effects may have masked differences in retention on this test.
Furthermore, although group analysis indicated that retention on
spatial recall and story recall tests was not impaired in patients
with TLE, analyses at the individual level showed greater evidence
of impaired three-week retention in individuals with TLE compared
to the controls on these tests. This indicates that, contrary to the
hypothesis of Bell (2006), ALF can occur in TLE in the absence of
overlearning.
Individual analyses may help to explain the discrepancy
between studies. Bell (2006) found no significant difference
between percentage of participants with TLE and percentage of
control participants who showed ALF over two weeks. In con-
trast, our individual analyses indicated that a greater percentage
of participants with TLE showed impaired retention over three
weeks in comparison with controls. This inconsistency may reflect
the fact that in Bell’s study, even at the short delay, patients
performed worse than controls and so results may have been
influenced by a scaling effect. However, our individual anal-
ysis revealed heterogeneity in forgetting rates within the TLE
group, as approximately half of these patients (four to eight
patients across the tests) showed impaired retention. It is also
possible, therefore, that rather than methodological differences
alone, Bell’s finding may relate to inclusion of a sample with
a number of patients who did not show ALF. Although the
results of these individual analyses should be made tentatively
they could give valuable insights into the potential causes of
ALF.
In the individual analysis, impaired retention between 30 min
and three-weeks was more frequently identified in patients with
mesial temporal sclerosis (from 4 out of 7 patients on story recall
to 7 out of 7 patients on visual scenes spatial recall) than patients
without mesial temporal sclerosis (from 1 out of 7 patients on visual
scenes spatial recall to 2 out of 7 patients on visual scenes item
recall), across the tests. These results could be consistent with those
of Butler et al. (2009) who reported significant hippocampal atro-
phy in patients with transient epileptic amnesia who showed ALF.
Although they found no direct relationship between hippocampal
volume and ALF, their findings and the present results suggest that
ALF may in some way be associated with hippocampal dysfunction.
It is possible that ALF is not directly related to hippocampal/medial
temporal sclerosis but that it relates to a third underlying variable,
such as diffuse temporal lobe pathology, which has been reported
to be associated with hippocampal sclerosis (e.g. Yogarajah et al.,
2008). This explanation could also account for the fact that ALF
has not been associated with hippocampal damage in cases in
whom the primary aetiology has not been temporal lobe epilepsy.
Further research comparing forgetting rates in larger samples of
Table 5
Number of patients with left and right TLE, with and without mesial temporal sclerosis (MTS), who showed impaired retention between 40 s and 30 min delays, and between
30 min and three-week delays.
Tests Timeframe
Visual scenes item 40 s to 30 min
30 min to 3 wk
Visual scenes spatial 40 s to 30 min
30 min to 3 wk
Visual scenes descriptive 40 s to 30 min
30 min to 3 wk
Story recall 40 s to 30 min
30 min to 3 wk
Story recognition 40 s to 30 min
30 min to 3 wk
a
One patient with bilateral TLE without MTS also showed impaired retention on these tests over three-weeks.
patients with and without mesial temporal sclerosis including
measures of diffuse temporal lobe pathology will be important
to establish the relationship between mesial temporal sclerosis
and ALF.
The individual level analyses were not consistent with the
material-specific memory model. According to this model, right
temporal lobe damage is associated with impaired visuo-spatial
memory (e.g. Milner, 1965), whereas left temporal lobe damage is
associated with impaired verbal memory (Delaney, Rosen, Mattson,
& Novelly, 1980; Mungas, Ehlers, Walton, & McCutchen, 1985). This
model can explain some findings in studies of ALF, as left but not
right TLE has been associated with greater forgetting of a story
(Blake et al., 2000), but other studies have found no effect of lat-
erality on ALF (Bell, 2006; Bell et al., 2005; Giovagnoli et al., 1995;
Martin et al., 1991). Although numbers were small, individual anal-
yses revealed ALF on both the visual scenes and story recognition
tests regardless of the lateralisation of TLE. The absence of a later-
ality effect on visual scenes recall tests may reflect a strong verbal
component to this task. Indeed Dulay et al. (2002) report that the
task’s homologue, the Family Pictures test from the WMS-III, may
involve verbalisation of information. Retention on story recogni-
tion was also impaired in both left and right TLE, arguing against
a strong effect of laterality of seizure onset on the experimental
results.
Most studies of ALF have found similar patterns of forgetting in
patients who experience seizures during a retention period and
those who remain seizure-free (Bergin et al., 1995; Blake et al.,
2000), and ALF is reported in patients who have been seizure-
free for six months or more (Butler et al., 2007). Our results are
in line with these studies: patients experiencing seizures showed
similar forgetting to those who remained seizure-free. This find-
ing held when assessing the TLE group, the IGE group, or both.
These findings are however inconsistent with those of a large group
study by Mameniskiene et al. (2006), who report greater forget-
ting in patients experiencing seizures. They also found significant
relationships between the quantity and type of seizures; patients
experiencing more than four seizures forgot more material than
those experiencing fewer than four, and seizures affecting con-
sciousness (complex partial or secondarily generalised seizures)
were associated with more forgetting than seizures not affecting
consciousness (simple partial seizures). It should be noted, how-
ever, that this study did not differentiate participants showing ALF
from those who forgot across both short and long delays. It is pos-
sible, therefore that the effects of seizures on ALF are reflective
of a correlate of more severe epilepsy than seizures per se. Our
results suggest that overt seizures are unlikely to play a major
role in ALF. It is not possible to exclude the possibility that sub-
clinical epileptiform activity may disrupt consolidation processes,
however.
Left Right
MTS Non-MTS MTS Non-MTS
– – – –
4 – 2 1a
1 – 1 1
4 – 3 1
1 – – –
3 – 2 1
– – 1 –
3 – 1 –
– – – –
2 – 3 1a
 N. Muhlert et al. / Neuropsychologia 49 (2011) 2417–2426
At present the cause of ALF is unclear, although the temporal
lobe is clearly implicated. The timescale over which ALF occurs is
also unclear. This is mainly due to methodological difficulties in
assessing ALF over multiple delays when participants may antic-
ipate testing and rehearse material which may then obliterate
the effect (e.g. Jansari et al., 2010). This difficulty has resulted
in the vast majority of studies including assessment at only one
long delay. Nevertheless ALF has been reported at delays as short
as 24 h (Jansari et al., 2010; Martin et al., 1991; Muhlert et al.,
2010; O’Connor et al., 1997). This raises the possibility that sleep
disruption may play a role as it is well known that sleep plays
an important role in memory consolidation (e.g. Stickgold, 2005).
Recently Westerberg et al. (2010) reported that in a group of peo-
ple with amnestic mild cognitive impairment, poorer recognition of
items learned 24 h previously was associated with reports of poorer
quality sleep. In relation to epilepsy it has been reported that people
with simple and complex partial seizures have a higher incidence
of sleep complaints than healthy controls (De Weerd et al., 2004).
In addition Machline Carrion, Lahorgue Nunes, Longo Martinez,
Wetters Portuguez, and da Costa (2010) reported a trend for poorer
sleep quality to be associated with nocturnal seizures in a group of
patients with TLE pre-surgery. Subjective sleep quality improved
post-surgery along with seizure reduction. These studies raise the
possibility that sleep disruption may play a role in ALF. Whether
this can be attributed to structural damage or nocturnal seizure
activity remains unclear.
We found that patients’ subjectively perceived memory cor-
related with their retention over 30-min on the tests that were
sensitive to ALF. In contrast, perceived memory did not signif-
icantly correlate with retention over three weeks. Blake et al.
(2000) also found no significant relationship between ALF and
perceived memory. However their findings were not replicated
in Butler et al. (2009), who found that a composite measure of
ALF predicted self-ratings of memory on the everyday memory
questionnaire in patients with transient epileptic amnesia. It may
be that the negative findings between ALF and subjectively per-
ceived memory in patients with TLE (but not transient epileptic
amnesia) relate to the small sample sizes used in these analyses.
Subjectively perceived memory in TLE may also relate to forgetting
over shorter, 30 min delays, as shown in this study. Alternatively,
reports of poor subjective memory in TLE may relate to mood
and adjustment related issues (see Hall, Isaac, & Harris, 2009 for
a review).
Quality of life and mood were also not correlated with mea-
sures of retention over 30-min or three-week delays. This suggests
that ALF may have no greater impact on patients’ mood and
quality of life than other epilepsy-related issues (e.g. seizure-
worry). It should be noted, however, that this result was based
on a small sample. Further research in larger samples may
help to fully establish the influence of forgetting on quality of
life.
5. Conclusion
This study demonstrated evidence for ALF in TLE but not IGE
in the absence of overlearning and ceiling effects. Forgetting did
not appear to be related to the experience of overt seizures
between learning and testing. This suggests that ALF was not
caused by a history of seizures, overt seizures during retention
periods, antiepileptic medication, or mood disturbance. ALF was
not correlated with subjectively perceived memory or quality of
life. Preliminary findings suggest an association between forget-
ting over three-weeks in TLE and the presence of mesial temporal
sclerosis which could form the focus of future research into this
phenomenon.
2425
Appendix A. Correction for spatial and descriptive memory
discrimination scores
Spatial information was scored using a corrected measure
because the possible spatial score varied as a function of the num-
ber of items recalled (see Hunkin, Parkin, & Longmore, 1994). For
example, recall of one item with correct spatial location would lead
to a higher score (100%) than recall of six items with correct spa-
tial location for five of those items (80%). To compensate for the
possibility of attaining extreme scores (0% or 100%), Hunkin et al.’s
discrimination score (Sp) was used. This is calculated as:
r−x
Sp =
SD
where r is the correct spatial responses; x = n·p; n is the number of
items recalled; p is the probability of recalling spatial information
by chance; SD is the square root of (n·p·q); and q = (1 − p).
Descriptive recall was also measured using Des. This was calcu-
lated as
d/2
Des = × 100
i
where d is the descriptive recall raw score (halved as two points
were available for each item); i is the item recall raw score.
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