Posted: September 16th, 2017

Transient epileptic amnesia: a description of the clinical and neuropsychological features in 10 cases and a review of the literature

Transient epileptic amnesia: a description of the
clinical and neuropsychological features in 10
cases and a review of the literature
Adam Z J Zeman, Simon J Boniface, John R Hodges
Abstract
Objectives—To clarify the clinical and
neuropsychological aspects of transient
epileptic amnesia (TEA) based on 10 personally
studied cases as well as review of
21 previously published cases; and to propose
tentative diagnostic criteria for the
diagnosis of TEA.
Methods—All 10 patients and informants
underwent a standardised clinical interview.
The radiological and neurophysiological
(EEG) data were also reviewed in
all cases. The diagnosis of transient epileptic
amnesia was made on the basis of
the following criteria: (1) there was a history
of recurrent witnessed episodes of
transient amnesia; (2) cognitive functions
other than memory were judged to be
intact during typical episodes by a reliable
witness; (3) there was evidence for a diagnosis
of epilepsy. This evidence was provided
by either (a) wake or sleep EEG, or
(b) the co-occurrence of other seizure
types (if their roughly concurrent onset or
close association with episodes of transient
amnesia suggested a connection), or
(c) a clear cut response to anticonvulsant
therapy, or by a combination of these
three factors. In addition all patients were
administered a comprehensive neuropsychological
test battery designed to assess
verbal and non-verbal anterograde
memory and retrograde memory for
famous personalities and personal events.
Their results were compared with those of
25 age and IQ matched normal controls.
Results—TEA usually begins in later life,
with a mean age of 65 years in this series.
Episodes are typically brief, lasting less
than one hour, and recurrent, with amean
frequency of three a year. Attacks on waking
are characteristic. Repetitive questioning
occurs commonly during attacks.
The anterograde amnesia during episodes
is, however, often incomplete so that
patients may later be able to “remember
not being able to remember”. The extent
of the retrograde amnesia during attacks
varies from days to years. Most patients
experience other seizure types compatible
with an origin in the temporal lobes, but
transient amnesia is the only manifestation
of epilepsy in about one third of
patients. Epileptiform abnormalities arising
from the temporal lobes are most
often detected on interictal sleep EEG.
Despite normal performance on tests of
anterograde memory,many patients complain
of persistent interictal disturbance
of autobiographical memory, involving a
significant but variable loss of recall for
salient personal episodes. The epochs
affected may predate the onset of epilepsy
by many years.
Conclusions—TEA is an identifiable syndrome
and comprises episodic transient
amnesia with an epileptic basis, without
impairment of other aspects of cognitive
function. Future studies should consider
the question of whether TEA reflects ictal
activity or a postictal state, and the mechanism
of the persistent autobiographical
amnesia. It is hypothesised that the latter
may result in part from impairment of
very long term memory consolidation as a
result of epileptic activity in mesial temporal
structures.
(J Neurol Neurosurg Psychiatry 1998;64:435–443)
Keywords:Transient epileptic amnesia; electroencephalography
It has been recognised for over 100 years that
amnesia for episodes of complex and well integrated
behaviour can occur in association with
temporal lobe epilepsy.1 2 More recent reports
have suggested that transient amnesia is sometimes
the only manifestation of a temporal lobe
seizure, and indeed that it may be the only seizure
type to occur in some patients.3–6 Seizures
causing prominent amnesia are easily mistaken
for episodes of transient global amnesia
(TGA)7 or of psychogenic amnesia.8 Various
terms has been used to describe these attacks
including pure amnestic seizures,9 ictal
amnesia,10 epileptic amnesia,11 epileptic amnesic
attacks,4 12 epileptic transient amnesia,13 and
transient epileptic amnesia or TEA.6 14 We have
adopted the last of these terms to highlight the
similarity of this syndrome to, but also its
distinction from, TGA.Our aims were to clarify
the clinical and neuropsychological features of
this disorder in the light of 10 cases of TEA
studied prospectively, and to compare these
with the features suggested by 15 previously
published reports of 21 cases. The largest previous
series describes four cases.6 We focus on
the following questions: (1) Is transient amnesia
a distinctive presentation of temporal lobe
epilepsy? If so, what are its characteristic
features? (2) What is the pathophysiology of
TEA, and in particular is it an ictal or postictal
phenomenon? (3) Is TEA associated, as Kapur
has suggested,6 with a persistent interictal
J Neurol Neurosurg Psychiatry 1998;64:435–443 435
University of
Cambridge Neurology
Unit
A Z J Zeman
J R Hodges
Department of Clinical
Neurophysiology,
Addenbrooke’s
Hospital, Hills Road,
Cambridge, UK
S J Boniface
MRC Applied
Psychology Unit, 15
Chaucer Rd,
Cambridge, UK
J R Hodges
Correspondence to:
Professor J R Hodges, MRC
Applied Psychology Unit, 15
Chaucer Rd,Cambridge CB2
2QQ, UK. Telephone 0044
1223 245151; fax: 0044
1223 336941.
Received 30 April 1997 and
in revised form 21 July 1997
Accepted 29 July 1997
disturbance of retrograde memory? If so, what
mechanism is responsible?
Methods
PATIENTS AND DIAGNOSTIC CRITERIA
Patients had initially been referred to the
Memory and Cognitive Disorders Clinic at
Addenbrooke’s Hospital, Cambridge (four) or
seen in general neurology clinics in East Anglia
by the authors (four) or their colleagues (two).
The diagnosis of transient epileptic amnesia
was made on the basis of the following criteria:
(1) there was a history of recurrent witnessed
episodes of transient amnesia; (2) cognitive
functions other than memory were judged to
be intact during typical episodes by a reliable
witness; (3) there was evidence for a diagnosis
of epilepsy. This evidence was provided by
either (a) wake or sleep EEG, or (b) the
co-occurrence of other seizure types (if their
roughly concurrent onset and/or close association
with episodes of transient amnesia
suggested a connection), or (c) a clear cut
response to anticonvulsant therapy, or by a
combination of these three factors.
STUDY PROTOCOL
History and examination
We reviewed the history of attacks in detail with
the patient and with a witness (who was a
spouse in every case) independently, and
enquired whether any other memory problems
had been noticed by either patient or spouse,
following the methods described by Hodges.15
Other information regarding handedness, education
and work history, risk factors for
epilepsy (for example, birth history, febrile
convulsions, head injury, CNS infections, alcohol
use, family history), other medical history,
psychiatric history, and drug history was
collected using a proforma designed for the
study. The patients underwent a standard
neurological examination.
Investigations
All EEGs (16 channel digital and/or analogue
with a 10/20 montage) were assessed by one of
us (SB). If a sleep EEG (sleep deprived or drug
induced) had not already been performed, one
was arranged. Sleep deprived EEGs were
performed after three to four hours of sleep
deprivation on the preceding night. Drug
induced sleep EEGs were performed after the
administration of 300 mg amylobarbitone by
mouth. Interictal EEG features were classified
as follows:16 (1) epileptiform, with reproducible
examples (>2) of unequivocal focal epileptiform
complexes; (2) non-reproducible, with
two or less unequivocal epileptiform focal
abnormalities of comparable waveform in 30
minutes; (3) polyrhythmic, with brief polyrhythmic
abnormalities of no diagnostic relevance;
(4) normal, with none of the above
abnormalities. Normal small sharp spikes and
regional slow wave rhythms or complexes
attributable to the effects of aging or vascular
lesions were all excluded. Neuroimaging was
reviewed.
Neuropsychology
A battery of tests designed to assess verbal and
non-verbal anterograde recall and recognition
memory, and retrograde memory for public
and personal events, was administered to each
patient. These were the national adult reading
test,17 immediate and delayed story recall from
the Wechsler memory scale revised,18 reproduction
and delayed recall of the Rey-
Osterrieth complex figure,19 the recognition
memory test for words and faces,20 famous
faces and famous names tests,21 and the
autobiographical memory interview.22 the patients’
results were compared with those from
25 normal controls from the MRC Applied
Psychology Unit’s panel matched for age, years
of education, and NART score using one tailed
tests (see below). To examine the performance
of individual patients, we also identified
instances in which the patients’ scores fell
below 2 SD of the controls’ mean on any test.
Results
DEMOGRAPHY
Table 1 shows that nine of our 10 patients were
men. Their ages ranged from 49–73 with a
mean of 65. The aetiology of their epilepsy was
uncertain, but preceding vascular events were
common: three patients (cases 3, 5, and 7) had
a history of myocardial infarction, one patient
(case 6) had recently undergone aortic valve
replacement, and another (case 9) coronary
artery bypass grafting. Two patients (cases 1
and 8) reported significant head injuries with
loss of consciousness in early adulthood: the
post-traumatic amnesia had been negligible in
the first case and had lasted two hours in the
second.
CRITERIA FOR DIAGNOSIS
Table 1 shows that four patients had unequivocal
reproducible abnormalities referable to the
temporal lobes on wake or sleep EEG (see
below). Of the remaining six patients, five had
other seizure types which lent support to the
diagnosis of epilepsy (see below), and in the
remaining case anticonvulsant treatment abolished
the amnesic episodes. In six of the 10
patients more than one factor supported the
diagnosis of epilepsy.
CHARACTERISTICS OF THE AMNESIC EPISODES
Table 1 shows that at the time of the diagnosis
of TEA, the history of amnesic episodes ranged
in duration from four months to 14 years, with
a mean of three years. The number of episodes
ranged from three to 20 with a mean of nine. In
six patients all episodes had lasted for one hour
or less, in two patients some but not all attacks
had lasted for an hour or less, whereas in the
remaining two patients attacks had always
lasted hours, and sometimes days. Anterograde
and retrograde memory were both disturbed in
typical episodes, but five patients had partial
recall for at least some attacks, suggesting that
the anterograde amnesia was incomplete. Nine
of the 10 patients had questioned their
companions repetitively during episodes. The
retrograde amnesia during attacks was sometimes
brief, but all patients had experienced
436 Zeman, Boniface, Hodges
attacks in which it extended over several
months. It is noteworthy that in six of the 10
the retrograde amnesia sometimes extended
over many years. In every case at least one episode
had occurred on waking. Nine patients
were treated with anticonvulsant drugs and one
declined treatment; in seven there was clear cut
benefit, with abolition of overt attacks in six
and pronounced reduction of frequency in the
seventh. In the remaining two patients the
effects of treatment are uncertain, in one
patient because of a short period of follow up,
in the other because attacks had occurred only
at long intervals before the initiation of
treatment.
OTHER SEIZURE TYPES
Table 1 shows that seven of the 10 patients
reported other types of epileptic phenomena.
These comprised olfactory hallucinations in
two patients (cases 1 and 3), frequent episodes
of déjà vu in one patient (case 6), episodes of
vertigo in one patient (case 2), complex partial
seizures in three (cases 3, 9, and 10), and
tonic-clonic seizures in two patients (cases 8
and 10). In four patients (cases 1, 2, 6, and 9)
these phenomena sometimes preceded amnesic
episodes. In all cases the other seizure types
had first occurred at around the same time as
the amnesic episodes with the exception of
patient 6 who recalled a brief flurry of episodes
of déjà vu occurring about 45 years ago. In
three patients (cases 4, 5, and 7) there was no
history from either patient or spouse to suggest
the occurrence of any epileptic phenomena
apart from the amnesic episodes themselves.
RETROGRADE AMNESIA AND OTHER MEMORY
COMPLAINTS
Table 1 shows that seven of the 10 patients
complained spontaneously of an unusual and
persistent impairment of remote memory. In
every case this included an inability to recall
some salient episodes from their personal lives.
This was often first noted when the patients
encountered photographs of episodes from
recent holidays and realised that they had no
recollection of them. In all cases, the patients
and their spouses thought that this impairment
was “patchy”, with preservation of recall for
some, but loss of recall for other, episodes. The
impairment was more severe for episodes from
recent years than for the distant past, but in five
of the seven cases the impairment affected
recall for episodes which predated the clinical
onset of TEA. In these five patients, the retrograde
memory disorder extended from a minimum
of 18 months to a maximum of about 30
years (case 3). Six patients gave a history
suggestive of topographical amnesia, with
failure to recognise familiar landmarks and to
recall familiar routes. Three complained of difficulty
in recalling the names of longstanding
friends and acquaintances, and two complained
that they had lost their grasp of
techniques which they had used professionally
for many years. Patients were asked to assess
their day to day anterograde memory as well as
their recall for more remote events: only one of
the seven patients who complained of an
impairment of retrograde memory (case 10)
thought that he had a comparable disturbance
of day to day memory.
PSYCHIATRIC BACKGROUND
Two patients gave a history of mood disorder.
Patient 9 experienced lowering of his mood
after retirement and was being treated with
sertraline at the onset of his episodes of
transient amnesia; patient 10 had a long history
of intermittent depression, preceding the onset
of his episodic amnesia. He had received treatment
with paroxetine for an exacerbation of
depression some months after the onset of
amnesic episodes. A history of possible past
psychiatric disorder was obtained in two other
patients: patient 1 had been seen by a neurologist
on two occasions, seven and 24 years
before the onset of his current illness, with
symptoms which were attributed to stress.
Patient 6 had a history of excessive alcohol but
his episodes of amnesia had not occurred in the
context of alcohol misuse.
NEUROPHYSIOLOGY
Table 1 shows that all patients had sleep EEGs;
in eight of the 10 cases these were preceded by
wake records. Amylobarbitone was used to
induce sleep in five patients, and five patients
were sleep deprived. Four patients had clear
cut epileptiform EEG abnormalities as defined
above. In one of these (case 4) the wake EEG
was normal, in two (cases 2 and 3) the wake
EEGs showed non-reproducible epileptifom
abnormalities. The remaining patient (case 5)
did not have a wake EEG: epileptiform
discharges were detected in both the wake and
sleep portions of his sleep deprived EEG.
Table 1 Current series: clinical, EEG, and neuropsychological features
Case Age Sex
History
(duration) Attacks
Attack
(duration)
Repetitive
questioning
Sleep
related EEG findings Rx response
Other
epilepsy
TEA
aura
Focal retrograde
amnesia
1 63 M 3 y 20 1 h + + – + CBZ sps +/- +
2 49 M 4 months 12 <1 h + + +Bilateral + CBZ sps +/- +
3 68 M 8 months 5 h-days + + +Bilateral + SVP sps,cps – +
4 66 F 14 5 <1 h>1 h + + +L E CBZ – – –
5 79 M 15 months 3 h-days + + +Bilateral E CBZ – – +
6 70 M 2 y 13 <1 h + + Polyr no Rx sps +/- –
7 73 M 6 months 5 1-2 h – + Polyr + P – – –
8 60 M 6 months 3 <1 h>1 h + + – + SVP tcl – +
9 69 M 4 months 3 <1 h + + – + CBZ cps +/- +
10 56 M 9 months 20 <1 h + + – + CBZ cps, tcl – +
Polyr = polyrhythmic abnormalities present; Rx response = treatment response (+ = abolition or substantial reduction of episodes, E = equivocal reduction, CBZ =
carbamazepine; P = phenytoin, SVP = sodium valproate); sps = simple partial seizures; cps = complex partial seizures; tcl = tonic-clonic seizures; TEA aura = occurrence
of co-occurring seizure type as prodrome of amesic episode (+ = co-occurring seizure type always precedes TEA, +/- = co-occurring seizure type sometimes
precedes TEA, – = no co-occurring seizure type).
Transient epileptic amnesia 437
Patients 3 and 4 had drug induced sleep EEGs;
patients 2 and 5 were sleep deprived. In all
cases the discharges were referable to the anterior
or mid-temporal lobe. They were bilateral
and independent in three of the four patients
(cases 2, 3, and 5). Two of the six remaining
records (cases 6 and 7) showed sparse focal
polyrhythmic abnormalities on sleep EEG.
NEUROIMAGING
All patients had CT except for patient 1. These
were within normal limits. Four patients had
MRI; these were normal in patients 1 and 2; in
patient 5 there was evidence of focal infarction
in the posterior corpus callosum and in patient
10 there was focal atrophy of the anterior and
mid-hippocampus on the right. HMPAOSPECT
was performed in patients 1 and 3;
both showed a minor degree of frontal lobe
hypoperfusion.
NEUROPSYCHOLOGY
Table 2 shows that although there were no significant
differences between the group data for
patients and controls on any of the demographic
or neuropsychological variables, analysis
of individual patient’s scores disclosed that
seven had impaired performance on at least
one test (as judged by obtaining a score more
than 2 SD below the control group mean).
Interestingly, all but one of these tests examined
retrograde memory: the famous faces test
(two patients), the famous names test (four
patients), the autobiographical memory interview
(three patients), and the recognition
memory test (one patient). In total, five
patients showed impairment of one or more
tests of remote memory but in most cases, their
scores were only just below the 2 SD cut off.
Only one score (for the autobiographical
memory interview in patient 2, described
below) fell more than 3 SD below the control
mean.
The cases are briefly summarised below:
Case 1
A 63 year old engineer had experienced about
20 episodes of transient amnesia lasting for
around one hour each over the past three years.
Most had occurred on waking. He would characteristically
say “I’m not sure where I am” at
the onset; his conversation would then disclose
a retrograde amnesia extending back for about
10 years. He has no recall for events during the
attacks. In other respects, he converses and
behaves normally during attacks. Over the year
before presenting to us he had complained to
his wife of a “strange smell or taste” which he
noticed at the onset of attacks. He had been
knocked out by a fly press in 1966. MRI and
wake and sleep EEG were normal. Treatment
with carbamazepine abolished the attacks.
Case 2
A 49 year old businessman presented with a
four month history of brief episodes of vertigo
accompanied by “ringing in the ears”, which
usually woke him from sleep and which was
often followed by a period of amnesia lasting
for less than one hour. Amnesia on waking
sometimes occurred without the prodrome of
vertigo. The amnesic episodes involved retrograde
amnesia for up to 30 years accompanied
by incomplete anterograde amnesia. Apart
from repetitive questioning to his wife, behaviour
during attacks was normal. During this
period he has developed a patchy persistent
amnesia for recent events. Brain MRI was normal
but sleep and wake EEG showed independent
unequivocal bitemporal epileptiform
abnormalities. Treatment with carbamazepine
has abolished the amnesic episodes.
Case 3
A 68 year old retired engineer gave an eight
month history of episodes of amnesia which
usually occurred on waking, and involved
extensive retrograde amnesia with incomplete
anterograde amnesia for the episodes themselves.
Apart from occasional repetitive questioning
his behaviour was normal during the
initial attacks. He sometimes complained of an
odd taste or smell. Seven months after the first
attack he had an episode of amnesia during
which he was clearly confused and unable to
dress himself; after this, his wife described episodes
in which he became inaccessible for a few
minutes, with no subsequent recall of events
during the episodes. During this period it
became clear that he had developed an
extensive patchy retrograde amnesia for events
of the past 30 years. He had a history of myocardial
infarctions seven and nine years ago.
Brain CT was normal and SPECT showed
minor reduction in uptake frontally.Wake EEG
showed sharpened theta activity in both
temporal lobes; sleep deprived EEG showed
independent bitemporal unequivocal epileptiform
abnormalities. Treatment with sodium
valproate abolished the episodes of overt
amnesia.
Table 2 Neuropsychological test results
TEA
mean (SD)
Controls
mean (SD)
Anterograde memory tests (maximum score in parenthesis):
Age 65 (9) 70 (8)
Education (y) 12 (2) 11 (2)
NART 115 (6) 119 (7)
Story recall WMS:
Immediate (21) 13 (4) 12 (4)
Delayed (21) 10 (3) 9 (3)
Rey-Ostereith figure:
Copy (36) 35 (1) 34 (3)
Delayed recall (36) 20 (4) 15 (8)
Recognition memory test:
Words (50) 46 (3) 47 (3)
Faces (50) 43 (4) 44 (4)
Retrograde memory tests (maximum scores in parenthesis):
Famous faces test
Recognition (50) 47 (2) 43 (7)
Identification (50) 38 (5) 39 (9)
Naming (50) 26 (10) 31 (4)
Famous names test
Recognition (50) 49 (1) 50 (1)
Identification (50) 46 (2) 49 (1)
Autobiographical memory interview:
Personal semantic:
Childhood (21) 19 (2) 20 (2)
Early adulthood (21) 18 (2) 20 (2)
Late adulthood (21) 20 (2) 20 (1)
Personal incident:
Childhood (9) 8 (2) 7 (2)
Early adulthood (9) 7 (2) 8 (2)
Late adulthood (9) 7 (3) 7 (2)
438 Zeman, Boniface, Hodges
Case 4
A 67 year old housewife experienced four episodes
of transient amnesia, lasting from a few
minutes to several hours, over the course of 15
years. Anterograde amnesia was incomplete in
the first two episodes but the third and fourth
were clinically indistinguishable from transient
global amnesia. Behaviour was normal during
the episodes apart from repetitive questioning.
Brain CT and wake EEG were normal, but a
sleep record showed unequivocal left temporal
epileptiform abnormalities. On treatment with
carbamazepine she had had one further
episode lasting 20 minutes.
Case 5
A 79 year old retired manager experienced several
episodes of amnesia lasting hours or days.
At least one episode occurred on wakening. He
asked questions repetitively during the episodes.
Over the same period he developed a
patchy amnesia for recent events. Two and a
half years before presentation he had had a
myocardial infarct. Brain MRI disclosed an
area of infarction in the posterior corpus callosum.
EEG showed independent bitemporal
unequivocal independent epileptiform abnormalities.
Follow up after starting treatment
with carbamazepine has been too brief to judge
the response.
Case 6
A 70 year old retired surveyor had experienced
unusually frequent episodes of déjà vu in his
mid-20s. He presented to us with a two year
history of numerous episodes of dense anterograde
amnesia lasting minutes, with some
retrograde amnesia, sometimes occurring on
waking and often preceded by a sense of déjà
vu. He questioned his wife repetitively during
these episodes, but could perform complex
tasks—for example, playing cards. He was
drinking up to 10 units of alcohol a day at the
onset of these episodes and required an aortic
valve replacement during this period. An EEG
showed right temporal polyrhythmic abnormalities;
brain CT was normal. He declined
treatment.
Case 7
A 73 year old retired electrician presented with
a history of five attacks of amnesia lasting one
to two hours over the preceding six months.He
typically complained of feeling odd at the
onset, and sometimes of a strange feeling over
the left side of his face. He would then ask
“What are we doing here?”, and question his
wife repetitively. His questions sometimes
betrayed amnesia for recent events. One attack
occurred on waking in the early hours. Brain
CT was normal; EEG showed right temporal
polyrhythmic abnormalities. Treatment with
phenytoin abolished the attacks.
Case 8
A 60 year old printer presented after three episodes
of amnesia in the last six months. The
first occurred on waking and involved repetitive
questioning, lasting for at least one hour.
Shortly after this he had a tonic-clonic seizure
in sleep. The third amnesic episode culminated
in a series of brief generalised convulsions. He
developed a patchy retrograde amnesia for
recent events, familiar faces, and places. He
had a history of head injury with loss of
consciousness in a motorbike accident at the
age of 18. Brain CT and wake and sleep EEGs
were normal. There have been no more attacks
since treatment with sodium valproate was
started.
Case 9
A 69 year old retired civil engineer had experienced
three episodes of amnesia in four
Table 3 Previously reported cases: clinical, EEG, and neuropsychological features
Reference Age Sex
History
(duration) Attacks (n)
Attack
(duration)
Repetitive
questioning
Sleep
related
EEG
findings
Rx
response
Other
epilepsy
TEA
aura
Focal
retrograde
amnesia
Memory
tests
Lou50 61 M ? 9 15 min>h + + +R +OXZ – – – Ant
Shuping24 60 M ? 3 <1 h ? ? – – tcl – – ND
Deisenhammer23 11 F 1 month 4 <1 h + + +R + CBZ – – – ND
Dugan et al3 82 M 2 months 3 3–4 h + ? +Bilateral + P – – – ND
Pritchard et al4:
i 65 M 4 y 10 <15 min – ? +Bilateral + P – – ? ND
ii 64 M 6 months 3 1–24 h – ? +Bilateral + CBZ – – ? ND
Meador et al25 47 F 10 months 2 <1 h – – +Bilateral + P/surg cps – Normal
Galassi et al12 67 M 2 y 25 <1 h + + ThetaR E P sps/cps + Imp mem Verb
Gallassi et al36:
i 70 F 3 y 2-3/weeks <1 h + ? +R + CBZ cps + Imp mem Vis/verb
ii 66 M 2 y 1/m <1 h + ? ThetaL + CBZ cps + Imp mem Verb
Miller et al5:
i 62 M 14 months 8 <30 mins + + +Bilateral + P – – – ND
ii 22 ? Weeks Several <1 h ? ? +L + ? cps +/- ? ND
Stracciari et al13 70 F 8 months 8 10 min–7 h + – +L + CBZ cps +/- Imp mem Vis/verb
Kapur37 74 M 5 y 20 30 min>h ? + +Bilateral ? cps +/- + Retro
Kapur6:
i 63 F 3 y 35 Mins>h – ? ThetaL + SVP cps +/- Imp mem Vis/retro
ii 67 F 4 months 6 30 min–1 h – ? ThetaL + P – – – Normal
iii 28 M ? 20 1–2 day + + +Bilateral + CBZ/P cps +/- ? Vis/verb
iv 61 F ? 2 Min ? + +L + CBZ cps +/- Imp mem ?
v 60 M 3 y Many 10–15 min + ? +Bilateral + CBZ sps, cps + ? Verb
vi 54 M 21 months 8 30 min–1 h + ? +Bilateral + P cps +/- + Ant
Vuilleumier et al34 41 F >20 y Many Hours – + +Bilateral + CBZ sps + – Normal
Rx response = treatment response (+ = abolition or substantial reduction of episodes, E = equivocal reduction, CBZ = carbamazepine, P = phenytoin, SVP = sodium
valproate, OXZ = oxazepam, surg = surgery); other epilepsy = other co-occurring seizure types, (sps = simple partial seizures, cps = complex partial seizures, tcl =
tonic-clonic seizures); TEA aura = occurrence of co-occurring seizure type as prodrome of amesic episode, (+ = co-occurring seizure type always precedes TEA, +/-
= co-occurring seizure type sometimes precedes TEA, – = no co-occurring seizure type); Imp mem = complaint of impaired memory not further specified; vis/verb
= deficits on tests of anterograde visual/verbal memory; ant = anterograde memory impairment not further specified; retro = deficits on tests of retrograde memory.
Transient epileptic amnesia 439
months. Two of these occurred on waking and
involved anterograde amnesia, with repetitive
questioning, and retrograde amnesia for recent
events. Several subsequent episodes of amnesia
followed brief spells of loss of consciousness
which were sometimes preceded by lip smacking
and sometimes associated with scanty convulsive
movements. Over the same period he
developed a patchy amnesia for events of the
past three years. He had had triple coronary
artery bypass surgery two years before. Shortly
before the onset of these episodes sertraline
had been prescribed for depression. Brain CT
and wake and sleep EEGs were normal. There
have been no further attacks since starting
treatment with carbamazepine.
Case 10
A 56 year old lecturer reported numerous episodes
of anterograde amnesia, accompanied by
retrograde amnesia for recent events, lasting for
less than one hour, over a nine month period.
These commonly occurred on waking from
naps.On other occasions, however, his wife saw
him “drift off into a trance and make choking
noises for a second or two”, after which he
would be amnesic. He went on to have three
witnessed tonic-clonic convulsions, shortly
after starting paroxetine for depression. He
complained of poor memory for day to day
events and for familiar places, and of abnormal
forgetting over time. Brain MRI showed focal
atrophy of the right hippocampus. Sleep EEG
was normal. Since starting treatment with carbamazepine
there have been no further episodes
of amnesia or overt seizures.
Discussion
VALIDATION OF TEA AS A DISTINCT
NEUROLOGICAL ENTITY
Table 3 shows several previous reports that
have suggested that episodes of transient
amnesia, often closely resembling the syndrome
of transient global amnesia, can have an
epileptic basis, but this fact has not received
wide acceptance. Our 10 cases provide further
evidence for the existence of TEA which we
argue is a distinctive manifestation of temporal
lobe epilepsy.The evidence is most persuasive
in those patients with support from all three
criteria adopted in this study: epileptiform discharges
on EEG, concurrent onset of other seizure
types, and a response to anticonvulsant
therapy.Of these three criteria, the first two are
the strongest. Two of the patients in this study
(cases 2 and 3) satisfy all three criteria; four
others (cases 2, 8, 9, and 10) satisfy two; cases
4, 5, 6, and 7 satisfy one criterion each.We have
included the third group, in which the diagnosis
is least certain, on the hypothesis that the
clinical features of their attacks are identical to
those in the first two groups and reflect, therefore,
a common mechanism of transient amnesia.
CLINICAL CHARACTERISTICS OF TEA
Table 3 summarises these previously reported
cases. The reports have generally applied similar
criteria for diagnosis to those we have used,
with some exceptions: in four of the 21
patients,11–13 amnesic episodes always followed
complex partial seizures; some reports do not
mention whether a description from a witness
was available. The onset of attacks is commonly
in middle or old age. Only one case in
the literature,23 and none in the present series
had amnesic episodes below the age of 40. The
aetiology of the epilepsy is usually obscure,
with negative results from neuroimaging,
although two previous cases were associated
with tumour,24 25 and right hippocampal atrophy
was noted in one of our patients (case 10).
A history of cardiac disease was common
among our patients, suggesting that cardiac
related hypoxic damage to mesial temporal
lobe structures may be mediating their epilepsy.
The attacks themselves have several distinctive
features:
(1) they tend to be more numerous than episodes
of TGA. In our series the mean number
of attacks was nine, at a rate of three attacks a
year. This compares with a recurrence rate of
about 3% a year for episodes of TGA.7
(2) Episodes of TEA are usually relatively
brief: eight of 10 of our patients and 17 of 21 of
the previously reported cases had at least some
attacks lasting less than one hour. This
compares with a mean duration of four to six
hours for attacks of TGA.7
(3) The occurrence of attacks on waking is
characteristic. Every patient in our series
reported at least one such attack; they were a
typical feature in six of 10. Likewise attacks on
waking were noted in eight of 10 previously
reported cases for which this information is
available. By contrast, episodes of TGA sometimes
occur on rising in the morning, but
probably no more often than would be
expected by chance.26 By contrast with Kapur’s
finding,6 that repetitive questioning is unusual
in TEA, all but one of our patients had
questioned a companion repetitively during at
least one attack. One feature which may distinguish
TEA from TGA is, however, the ability to
recall some details about the amnesic episode:
half of our patients had some recall for their
attacks. In particular, they were “able to
remember not being able to remember” recent
events during attacks, indicating that their
anterograde amnesia during the attack was
sometimes incomplete. Whereas this feature
may distinguish TEA from TGA, a careful
standardised comparison between patients
with the two conditions is required to reach a
definite conclusion on this point. Retrograde
amnesia of variable duration is undoubtedly a
common feature during attacks of TEA. It was
noted in all our cases, and in all those cases in
the literature in which the issue is discussed,
with the exception of the cases described by
Palmini et al.9 whereas their findings show that
inconspicuous or unnoticed anterograde amnesia
may be the sole manifestation of temporal
lobe epilepsy, the claim that all “amnestic
seizures” are of this kind is not compelling:
patients included in this study were highly
selected, and all had a pre-existing diagnosis of
intractable temporal lobe epilepsy.We return to
this issue below. Isolated transient amnesia
may, on occasions, be the sole manifestation of
440 Zeman, Boniface, Hodges
epilepsy. In three of our 10 patients, and in
seven of 21 cases in the literature (32%
overall), episodic amnesia was the only manifestation
of epilepsy.We disagree therefore with
Palmini et al9 who concluded that pure amnestic
seizures “never represent the only type of
seizures” in patients with temporal lobe
epilepsy. Their study considered only patients
with pre-existing temporal lobe epilepsy. Our
findings suggest that temporal lobe epilepsy is
an important diagnosis to consider in patients
with brief recurrent episodes of amnesia, especially
if they occur on waking. This is consistent
with the results of Hodges7 who reported that
eight of 114 patients satisfying strict criteria for
TGA subsequently developed epilepsy; six of
these had complex partial seizures. In this
study patients with more than one episode of
“TGA” and/or episodes of less than hour were
at an increased risk of subsequent epilepsy by
comparison with patients with single protracted
episodes. A recent study by Melo et al27
disputed this view on the grounds that only one
of their five patients with brief recurrent
episodes diagnosed as TGA proved to have
epilepsy. We would not claim that all brief
recurrent amnesic episodes have an epileptic
basis. It could be relevant that Melo et al did
not report the results of sleep EEGs.
PATHOPHYSIOLOGY OF TEA
Interictal temporal lobe epileptiform abnormalities
are sometimes non-localising because
of either neurophysiological propagation or
volume conduction. In combination with the
clinical features of associated seizures, however,
these features imply that TEA is a pathophysiological
phenomenon of the temporal
lobe.
Does TEA result from mesial temporal
dysfunction?
The critical role of the mesial temporal lobes
(hippocampus subiculum, parahippocampal
gyrus, and entorhinal cortex) in the acquisition
of new memories and the retrieval of recent
ones is well established.28 29 It is plausible,
therefore, that dysfunction of these structures
is responsible for TEA. The preponderance of
anterior and mid-temporal abnormalities in
our series is consistent with a mesial temporal
origin, but these may have been propagated
rather than volume conducted. Surface EEGs
do not permit precise localisation of the underlying
electrical focus, as three dimensional
localisation of the epileptogenic region from
digital surface EEG is model dependent and
independent bitemporal interictal abnormalities
do not necessarily imply bilateral pathology.
Information from a few in depth studies
supports the view that epileptic amnesia results
from current or recent paroxysmal activity in
the mesial temporal lobes.9 30–32
IS TEA AN ICTAL OR A POST-ICTAL STATE?
Several reports bear on the question of whether
TEA is likely to be an ictal or a postictal state.
Palmini et al9 describe a brief episode of
bilateral mesial temporal epileptiform activity
associated with disruption of anterograde
memory. The patient successfully conducted a
telephone conversation during this episode for
which she later had no recall. She had been
unaware at the time that anything was wrong.
This case shows that a period of pure
anterograde amnesia can be the manifestation
of a mesial temporal seizure. On the other
hand, it has also been shown that recently
acquired memories are vulnerable to transient
temporal lobe seizures. Bridgman et al30
reported that a subclinical unilateral hippocampal
seizure, without spread to the temporal
neocortex, disrupted recall of a previously
learned word list. Similarly, Halgren et al33
showed that brief bilateral stimulation of mesial
temporal structures at either the time of
memory acquisition, or the time of memory
retrieval, could disrupt performance without
any other effect on behaviour. Taken together,
these findings suggest that ictal activity in
mesial temporal structures is capable of
disrupting both anterograde and retrograde
memory, and that this disruption may go
unnoticed by the subject. Can longer periods of
amnesia occur as an ictal phenomenon or are
these always postictal? Lee et al32 describe the
remarkable case of a previously well 38 year old
woman in whom a 12 day period of continuous
anterograde amnesia, with additional retrograde
amnesia for events of the past four
months, occurred as a manifestation of partial
status epilepticus: nasopharyngeal electrodes
showed frequent bilateral spikes and runs of
ictal activity arising independently in both
mesiotemporal lobes. Thus ictal amnesia
closely resembling TGA can occur as a
manifestation of semicontinuous temporal lobe
discharges. Similarly, Vuilleumier et al34 have
recently described a 41 year old woman with a
history of numerous episodes of profound retrograde
and apparent retrograde amnesia,
occurring since adolescence, which had been
regarded as hysterical. Attacks often started on
waking, and were preceded by an epigastric
aura. An EEG during a severe attack disclosed
generalised epileptiform spikes with spike and
wave activity at a frequency of 3.5–4 Hz,
involving occasional frontotemporal phase reversal.
Intravenous clonazepam abolished both
the EEG discharges and the amnesia, disclosing
unexpectedly clear recall for events occurring
during the seizure. Tassinari et al35 and
Morrell31 describe somewhat similar cases, but
these authors emphasise the persistence of the
amnesic state at times when no epileptiform
activity was apparent on the EEG, comparing it
to a “Todd’s paralysis” of memory. Palmini et
al9 cite the case of a patient with a postictal
period of combined anterograde and retrograde
amnesia lasting more than a month after
a flurry of temporal lobe seizures over a 24
hour period. In conclusion, both brief and prolonged
episodes of amnesia, affecting anterograde
and/or retrograde memory, can occur as
ictal phenomena, but prolonged amnesic states
can also occur in the aftermath of ictal activity.
It is uncertain, therefore, whether the recurrent
episodes of amnesia experienced by our
patients represent ictal or postictal phenomena.
Ictal EEG studies of patients during
Transient epileptic amnesia 441
amnesic episodes might help to clarify these
issues. Such studies may also help to disclose
the factors which determine whether or not a
period of amnesia comes to the patient’s
notice.
INTERICTAL RETROGRADE MEMORY IMPAIRMENT
IN TEA
Some previous case reports mention “difficulty
with memory” occurring between attacks of
TEA.13 36 The occurrence of a pronounced
persisting impairment of retrograde memory in
association with TEA has been highlighted
recently by Kapur,37 and by Kopelman et al.8
Despite the striking complaints of retrograde
memory impairment in our patients, performance
on objective tests of both anterograde and
retrograde memory was largely within normal
limits. The principal exceptions were tests of
retrograde memory, on which five patients had
a defective score (greater than 2 SD below the
controls’ mean) on at least one test, although
the degree of impairment was modest except in
one patient (case 2). Kapur, likewise, found
that tests of anterograde memory were normal
in his patient with striking complaints of retrograde
memory impairment37; scores on tests of
retrograde memory were depressed. Kopelman’s
patient8 obtained borderline scores on
tests of retrograde memory with somewhat
poor anterograde memory in relation to his
high IQ. Interestingly, a similar combination of
impaired retrograde memory with symptoms
of poor autobiographical memory but good
performance on anterograde memory tests has
been reported in a patient with paraneoplastic
limbic encephalitis.38 Our failure to demonstrate
consistent deficits on objective tests of
retrograde memory may reflect the patchy
nature of the impairment. Several of the
patients report lacunes in their autobiographical
memory, extending back over a decade or
more. Preliminary results of detailed testing of
one patient (patient 3), using tailor-made tests
of the type used in other similar single case
studies,37 39 40 suggest a profound impoverishment
of autobiographical memory for events of
the past 30 years. Islands of preserved recall
permitted a misleadingly normal score on the
AMI in this patient.
What is the explanation for this patchy
impairment of remote memory? There are
three possibilities: failure to encode episodes
into long term memory, failure to consolidate
and maintain memories, and failure to retrieve
memories which have been successfully acquired.
Some factors could potentially impair
memory acquisition in such patients including
impairment of consciousness in the course of
complex partial seizures, anterograde amnesia
in the immediate postictal phase, unnoticed
episodes of TEA giving rise to anterograde
amnesia, or a generalised impairment of
anterograde memory. These all seem unlikely
explanations for our patients’ subjective complaints
of retrograde amnesia given that
autobiographical memories which predate the
clinical onset of their epilepsy—sometimes by a
number of years—are affected, and the lack of
evidence for impairment of anterograde
memory on standard tests. It is clearly difficult
to exclude the possibility that patients may
have had subclinical seizures for some time
before the onset of their TEA attacks, but this
seems an unlikely explanation as in one patient
(case 3) the retrograde amnesia extended back
over 30 years.
The second possibility, that an impairment
of long term consolidation underlies this
persistent retrograde amnesia, merits further
consideration. Some patients in our series have
told us that their memories for recent personal
events seem to be intact initially but may then
disappear without trace, suggesting that acquisition
is normal but consolidation is impaired.
This is in keeping with their normal performance
on standard tests of anterograde memory
which typically test recall over 30 minutes or so
rather than over long periods. Current computational
neural network models of long term
memory processing, based on human neuropsychological
and animal data,41–43 suggest
that the medial temporal lobe complex plays a
critical, but temporally limited, part in the
encoding and storage of new episodic memories.
Over time a process of long term consolidation
or information transfer occurs whereby
memories become independent of the hippocampus
by the development of direct corticocortico
links. Ictal activity in the mesial temporal
lobes or involving the temporal neocortex
might be capable of disrupting recent memories
during this vulnerable stage of consolidation.
In this context, it is of interest that TEA
often occurs in relation to sleep, as there is
accumulating evidence that processes of
memory consolidation may be particularly
active in sleep.44 45 The fact that many patients
have early morning TEA attacks and show
abnormal sleep EEGs suggests that disturbed
consolidation during sleep may be a critical
factor. In keeping with this hypothesis is the
finding of impaired memory at long, but not
short, retention intervals in patients with temporal
lobe epilepsy.46 It is, however, open to
question whether disruption of consolidation is
an adequate explanation for the impaired recall
of very remote episodic and more semantic
type memories seen in some of our patients.
The occurrence of topographical amnesia for
extremely familiar places, impaired recognition
of familiar faces, and degradation of established
professional abilities points to pathology
in the more lateral temporal neocortex in addition
to mesial temporal structures. The neural
basis of very long term autobiographical and
semantic memory remains unclear. Current
evidence points to a critical role for the left
inferolateral temporal neocortex in the storage
of general semantic knowledge46–48; the equivalent
right sided structure may be specialised for
person based knowledge.49 It is possible that
pathology in these regions which have, for
example, a hypoxic basis, could give rise both
to epilepsy and to retrograde amnesia. In the
absence of more detailed neuroimaging such as
volumetric MRI or PET we cannot exclude the
possibility of subtle medial or temporal lobe
pathology in our cases. Failure of retrieval may
be difficult to distinguish from failure of
442 Zeman, Boniface, Hodges
storage. Preliminary work with a patient with
particularly severe retrograde amnesia (case 3)
indicates that his retrograde memory gaps are
consistent over time and little improved by
cueing: these features argue for a primary failure
of consolidation or storage rather than a
retrieval deficit.
In conclusion, a persistent impairment of
retrograde memory is a common accompaniment
of TEA. There is circumstantial evidence
that this may be the result of disruption of
memory consolidation, related to recurrent
ictal activity in mesial temporal structures.
Detailed neuropsychological study of individual
cases, particularly including analysis of
long term forgetting rates, combined with
ambulatory EEG recording in patients with
ongoing memory disturbance, will be of value
in testing this hypothesis.
We thank Dr Peter Harvey, Dr David Dick, Dr Colin Brown,
and Dr Iain Wilkinson who referred patients included in this
series; Dr Kristen Breen and Dr German Berrios who contributed
to the assessment of patients in the Cambridge Memory
Clinic; Naida Graham and Dr John Greene for providing
neuropsychological control data, and Nick Carvill for his technical
assistance with the EEGs.
1 Hughlings-Jackson J. On a particular variety of epilepsy
(intellectual aura), one case with symptoms of organic brain
disease. Brain 1989;11:179–207.
2 Penfield W, Mathieson G. Memory: autopsy findings and
comments on the role of hippocampus in experiential
recall. Arch Neurol 1974;31:145–54.
3 Dugan TM, Nordgren RE, O’Leary P. Transient global
amnesia associated with bradycardia and temporal lobe
spikes. Cortex 1981;17:633–8.
4 Pritchard PB, Holmstrom VL, Roitzsch JC, et al. Epileptic
amnesic attacks: benefit from antiepileptic drugs. Neurology
1985;35:1188–9.
5 Miller JW, Yanagihara T, Petersen RC, et al.Transient global
amnesia and epilepsy: electroencephalographic distinction.
Arch Neurol 1987;44:629–33.
6 Kapur N. Transient epileptic amnesia—a clinical update
and a reformulation. J Neurol Neurosurg Psychiatry
1993;56:1184–90.
7 Hodges JR. Transient global amnesia. London:WB Saunders,
1991.
8 Kopelman MD, Panayiotopoulos CP, Lewis P. Transient
epileptic amnesia differentiated from psychogenic “fugue”:
neuropsychological, EEG and PET findings. J Neurol Neurosurg
Psychiatry 1994;57:1002–4.
9 Palmini AL, Gloor P, Jones-Gotman M. Pure amnestic seizures
in temporal lobe epilepsy. Brain 1992;115:749–69.
10 Rowan AJ. Ictal amnesia and fugue states. In: Smith D,
Treiman D, Trimble M, eds. Neurobehavioural problems in
epilepsy. New York: Raven Press, 1991:357–67.
11 Gallassi R, Morreale A. Transient global amnesia and
epilepsy. In: Markowitsch HJ, ed. Transient global amnesia
and related disorders.Toronto: Hogrefe and Huber, 1990.
12 Gallassi R, Pazzaglia P, Lorusso S, et al. Neuropsychological
findings in epileptic amnesic attacks. Eur Neurol 1986;25:
299–303.
13 Stracciari A,Ciucci G, Bianchedi G, et al. Epileptic transient
amnesia. Eur Neurol 1990;30:176–9.
14 Kapur N. Transient epileptic amnesia: a clinically distinct
form of neurological memory disorder. In: Markowitsch H,
ed. Transient global amnesia and related disorders. New York:
Hogrefe and Huber, 1990:140–51.
15 Hodges JR. Cognitive assessment for clinicians. Oxford:Oxford
University Press, 1994.
16 Blume WT, Kaibara M. Atlas of adult encephalography. New
York: Raven Press, 1995.
17 Nelson HE, O’Connell A. Dementia: the estimation of levels
of premorbid intelligence using the new adult reading
test. Cortex 1978;14:234–44.
18 Wechsler DA. Wechsler memory scale-revised. New York: The
Psychological Corporation, 1987.
19 Osterrieth P, Rey A. Le test de copie d’une figure complexe.
Arch Psychol 1944;30:205–20.
20 Warrington EK. The recognition memory test. Windsor:
NFER, 1984.
21 Greene JDW, Hodges JR. Identification of famous faces and
famous names in early Alzheimer’s disease. Brain 1996;19:
111–28.
22 Kopelman MD, Wilson BA, Baddeley AD. The autobiographical
memory interview. Bury St Edmunds: Thames
Valley Test Company, 1990.
23 Deisenhammer E. Transient global amnesia as an epileptic
manifestation. Neurology 1981;225:289–92.
24 Shuping JR. Transient global amnesia due to glioma in the
dominant hemisphere. Neurology 1980;30:88–90.
25 Meador KJ, Adams RJ, Flanigin HF. Transient global
amnesia and meningioma. Neurology 1985;35:769–71.
26 Fisher CM. Transient global amnesia: precipitating activities
and other observations. Arch Neurol 1982;39:605–8.
27 Melo TP. Are brief or recurrent transient global amnesias of
epileptic origin? J Neurol Neurosurg Psychiatry 1994;57:
622–5.
28 Squire LR. Memory and the hippocampus: a synthesis from
findings with rats, monkeys, and humans. Physiol Rev
1962;99:195–231.
29 Squire LR, Alvarez P. Retrograde amnesia and memory
consolidation: a neurobiological perspective. Curr Opin
Neurobiol 1995;5:178–83.
30 Bridgman PA, Malamut BL, Sperling MR, et al. Memory
during subclinical hippocampal seizures.Neurology 1989;
39:853–6.
31 Morrell F. Memory loss as a Todd’s paralysis. Epilepsia
1980;21:185.
32 Lee BI, Lee BC, Hwang YM, et al. Prolonged ictal amnesia
with transient focal abnormlaities on magnetic resonance
imaging. Epilepsia 1992;33:1042–6.
33 Halgren E, Wilson CL, Stapleton JM. Human medial temporal
lobe stimulation disrupts both formation and
retrieval of human memories. Brain Cogn 1985;4:287–95.
34 Vuilleumier P, Desplane PA, Regli F. Failure to recall (but
not to remember): pure transient amnesia during nonconvulsive
status epilepticus. Neurology 1996;46:1036–9.
35 Tassinari CA, Ciarmatori C, Alesi C, et al. Transient global
amnesia as a postictal state from recurrent partial seizures.
Epilepsia 1991;32:882–5.
36 Gallassi R, Morreale A, Lorusso S, et al. Epilepsy presenting
as memory disturbances. Epilepsia 1988;29:624–9.
37 Kapur N. Focal retrograde amnesia: a long term clinical and
neuropsychological follow up. Cortex 1989;25:387–402.
38 Ahern GL,O’Connor M, Dalmau J, et al. Paraneoplastic
temporal lobe epilepsy with testicular neoplasm and atypical
amnesia. Neurology 1994;44:1270–4.
39 Hodges JR, McCarthy R. Autobiographical amnesia resulting
from bilateral paramedian thalamic infarction. Brain
1993;116:921–40.
40 Evans JJ, Breen EK, Antoun N, et al. Focal retrograde
amnesia for autobiographical events following cerebral
vasculitis: a connectionist account. Neurocase 1996;2:1–12.
41 Alvarez P, Squire LR. Memory consolidation and the medial
temporal lobe: a simple network model. Proc Natl Acad Sci
USA 1994;91:7041–5.
42 McClelland JL, McNaughton BL, O’Reilly RC. Why are
there complementary learning systems in the hippocampus
and neocortex: insights from the successes and failures of
connectionist models of learning and memory. Psychol Rev
1995;102:419–37.
43 Murre JMJ. Implicit and explicit memory in amnesia: some
explanations and predictions by the tracelink model.
Memory 1997;5:213–32.
44 Karni A. Dependence on REM sleep of overnight improvement
of a perceptual skill. Science 1994;265:679–82.
45 Wilson MA. Reactivation of hippocampal ensemble memories
during sleep. Science 1994;265:676–9.
46 Martin RC, Loring DW, Meador KJ, et al. Impaired
long-term retention despite normal verbal learning in
patients with temporal lobe dysfunction.Neuropsychology
1991;5:3–12.
47 Patterson K, Hodges JR.Disorders of semantic memory. In:
Baddeley AD, Wilson BA, Watts FN, eds. Handbook of
memory disorders: John Wiley, 1995:167–86.
48 Garrard P, Perry R, Hodges JR. Disorders of semantic
memory. J Neurol Neurosurg Psychiatry 1997;62:431–5
49 Evans JJ, Heggs AJ, Antoun N, et al. Progressive prosopagnosia
associated with selective right temporal lobe atrophy:
a new syndrome? Brain 1995;118:1–13.
50 Lou HOC. Repeated episodes of transient global amnesia.
Acta Neurol Scand 1968;44:612–7.
Transient epileptic amnesia 443
PLACE THIS ORDER OR A SIMILAR ORDER WITH US TODAY AND GET AN AMAZING DISCOUNT 🙂