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1998, Vol. 12, No. 1,52-64
Short-Term and Long-Term Memory in Early
Temporal Lobe Dysfunction
Suzanne Craft
Tamara Hershey
Washington University
Seattle-American Lake Veterans Affairs Medical Center
and University of Washington
Tracy A. Glauser
Sandra Hale
Washington University
Children's Hospital Medical Center
Cincinnati, Ohio
Following medial temporal damage, mature humans are impaired in retaining new information
over long delays but not short delays. The question of whether a similar dissociation occurs in
children was addressed by testing children (ages 7-16) with unilateral temporal lobe epilepsy
(TLE) and controls on short- and long-term memory tasks, including a spatial delayed
response task (SDR). Early-onset TLE did not affect performance on short delays on SDR, but
it did impair performance at the longest delay (60 s), similar to adults with unilateral medial
temporal damage. In addition, early-onset TLE affected performance on pattern recall, spatial
span, and verbal span with rehearsal interference. No differences were found on story recall or
on a response inhibition task.
The study of memory systems and their representation in
the brain has often focused on identifying dissociable
subsystems. Many types of memory distinctions have been
proposed on the basis of cognitive, neuropsychological, and
neurophysiological evidence, such as semantic-episodic
memory (Tulving, Kapur, Craik, Moscovitch, & Houle,
1994X declarative-nondeclarative memory (Squire, 1992),
implicit-explicit memory (Schacter, Chiu, & Ochsner, 1993),
and short-term-long-term memory (Alvarez, Zola-Morgan,
& Squire, 1994). The present study focuses on the distinction between short- and long-term memory following early
temporal lobe dysfunction in children.
Short-term memory, the ability to represent information
internally for brief periods of time, is considered to be a
fundamental feature of working memory (Baddeley, 1992;
Goldman-Rakic, 1987). This ability is commonly not affected by medial temporal region damage in adult humans
and animals. Long-term memory, the ability to store information for later recall, is impaired following damage to or
disruption of components of the medial temporal region. A
variety of tasks have been used in both animals and humans
to demonstrate this distinction, most notably the delayed
nonmatch to sample (DNMS), delayed match to sample
(DMS), and spatial delayed response (SDR) tasks. These
tasks involve the brief presentation of a piece of information
followed by a delay. For the DNMS and DMS tasks, objects
or colors are generally used; for the SDR task, spatial
locations are used. After the delay has ended, participants
must recognize or recall the piece of information presented
prior to the delay. On such tasks, adult animals and humans
with medial temporal damage are able to perform accurately
on trials with short delays yet are impaired on trials with
longer delays (DNMS: Alvarez et al., 1994; Bachevalier &
Mishkin, 1989; Overman, Ormsby, & Mishkin, 1990; Squire,
Knowlton, & Musen, 1993; Squire, Zola-Morgan, & Chen,
1988; Zola-Morgan & Squire, 1985; DMS: Aggleton, Nicol,
Huston, & Fairbairn, 1988; Prisko, 1963; Sidman, Stoddard,
& Mohr, 1968; SDR: Backer Cave & Squire, 1992; Kowalska, 1995; Rains & Milner, 1994; Zola-Morgan & Squire,
1985). In general, delays greater than 15-30 s on these tasks
are sensitive to medial temporal damage (Alvarez et al.,
1994; Rains & Milner, 1994; Squire et al., 1988), although
this may differ across specific task demands, materials,
species, and the extent and exact placement of the lesion
(Angeli, Murray, & Mishkin, 1993; Eichenbaum, Otto, &
Cohen, 1994; Leonard, Amaral, Squire, & Zola-Morgan,
1995; Muri, Rivaud, Timsit, Cornu, & Pierrot-Deseilligny,
1994; Sidman et al., 1968).
Tamara Hershey and Sandra Hale, Department of Psychology,
Washington University in St. Louis; Suzanne Craft, The Geriatric
Research, Education and Clinical Center of the Seattle-American
Lake Veterans Affairs Medical Center, and the Department of
Psychiatry and Behavioral Sciences, University of Washington;
Tracy A. Glauser, Department of Neurology, Children's Hospital
Medical Center, Cincinnati, Ohio.
This study was conducted in partial fulfillment of the requirements for Tamara Hershey's doctoral degree and was supported in
part by a Washington University Dissertation Fellowship. Preliminary results from this study were presented at the Second Annual
Meeting of the Cognitive Neuroscience Society held in San
Francisco, California, in 1995. We would like to thank the students
and teachers at the Governor French Academy and the Pediatric
Neurology and Psychology Departments at St. Louis Children's
Hospital for their assistance. We also thank the reviewers for their
thoughtful and helpful comments.
Correspondence concerning this article should be addressed to
Tamara Hershey, who is now at Washington University School of
Medicine, Department of Psychiatry, 4940 Children's Place, St.
Louis, Missouri 63110. Electronic mail may be sent via Internet to
[email protected].
52
MEMORY IN EARLY TEMPORAL LOBE DYSFUNCTION
Short-term memory, as measured by the SDR task, has
been associated with the dorsolateral prefrontal cortex.
Following dorsolateral prefrontal damage, performance on
the SDR task is impaired on trials with the shortest delay
(Bauer & Fuster, 1976; Freedman & Oscar-Berman, 1986;
Funahashi, Bruce, & Goldman-Rakic, 1993; Joyce & Robbins, 1991). In addition, studies have demonstrated that cells
in the dorsolateral prefrontal cortex fire selectively during
the delay period of the SDR task (Funahashi et al., 1993;
Goldman-Rakic, 1987). The dorsolateral prefrontal cortex is
thought to be responsible for holding spatial information
on-line, particularly for short periods of time. Further,
inferior frontal cortex has been associated with short-term
memory for repeated or unique objects on the DMS task
(Fuster, 1990; Wilson, Scalaidhe, & Goldman-Rakic, 1993).
Performance on the DNMS task using unique stimuli is
unimpaired following prefrontal cortex damage (GoldmanRakic, 1987). It has been proposed that the dorsolateral
prefrontal cortex is highly involved in the short-term memory
of spatial information, whereas the inferior frontal cortex is
involved in the short-term memory of object information
(Goldman-Rakic, 1987; Wilson et al., 1993). Thus, shortand long-term spatial and object recognition memory as
measured by DMS, but not DNMS, appear to be dissociable
following lesions to medial temporal versus dorsolateral or
inferior prefrontal cortex (Alvarez et al., 1994; Winocur,
1992).
This general pattern has also been reported in adult
humans with temporal lobe epilepsy (TLE), a disorder
associated with medial temporal dysfunction and neuropathology. Notably, these studies have focused on unilateral
TLE, which may make comparisons somewhat difficult with
animal work, in which bilateral lesions are generally present.
Short-term memory measures (immediate recall, span tasks,
consonant or pattern trigram tasks) generally have not
revealed consistent differences between left and right temporal lobe epileptics and their normal control groups (Delaney,
Prevey & Mattson, 1982; Delaney, Rosen, Mattson, &
Novelly, 1980; Lavadas, Umilta, & Provincial!, 1979). If
differences have been found, they have occurred at delays of
greater than 9 s (Delaney et al., 1982; Prevey et al., 1994)
and only with auditory verbal material (Delaney et al., 1982;
Samuels, Butters, & Fedio, 1972). After resection of the
medial temporal region to treat intractable seizures, longterm memory generally becomes more impaired on clinical
memory tasks (Ojemann & Dodrill, 1985; Wechsler, 1987).
One recent study has addressed the impact of medial
temporal excisions in seizure patients on tasks similar to
those used in animal studies, such as DMS and SDR. Among
other interesting results, Owen et al. (Owen, Sahakian,
Semple, Polkey, & Robbins, 1995) found that patients with
amygdala-hippocampal excision were impaired on the longest delay of the DMS task (12 s), with relatively normal
performance on shorter delays and a simultaneous matching
condition. On a spatial recognition task, participants were
shown a list of spatial locations and then given two-choice
recognition trials 3-72 s later. Patients with amygdalahippocampal excisions performed significantly worse than
controls on this task. However, the data were not analyzed
53
according to delay, so it is difficult to know if performance
was spared for trials with short delays. Notably, left and right
excision patients performed similarly on both of these tasks.
Research on the neural representation of short- and
long-term memory in developing animals and humans has
been less extensively reported. Bachevalier (1990) and
Mahut and Moss (1984) found that damage to the medial
temporal region in young monkeys produces long-term
memory impairment as measured by the DNMS task, similar
to results in adult monkeys. There have also been several
reports of childhood bilateral or unilateral medial temporal
damage that has led to dense amnesia (Ostergaard, 1987;
Tonsgard, Harwicke, & Levine, 1987; Wood, Brown, &
Felton, 1989). However, the neuropsychological evaluations
of these children have been limited at best, and no careful
analyses of short- and long-term memory have been conducted. In contrast, case studies of unilateral or bilateral
temporal lobe agenesis have reported no apparent memory
deficits, although, again, testing was limited (Karvounis,
Chiu, Parsa, & Gilbert, 1970; Lang, Lehrl, & Huk, 1981). A
number of studies on TLE have addressed similar developmental questions hi adults (Saykin, Gur, Sussman, O'Conner,
& Gur, 1989; Saykin et al., 1992; Wishart, Warmflash, Barr,
& Schaul, 1995) and children (Cohen, 1992; Fedio &
Mirsky, 1969; Jambaque, Dellatolas, Dulac, Ponsot, &
Signoret, 1993). These studies have generally documented
that unilateral TLE patients with early-onset seizures or an
early insult, such as febrile seizures, have more severe
memory deficits (Saykin et al., 1989; Saykin et al., 1992;
Wishart et al., 1995) and more overt hippocampal damage
(McMillan, Powell, Janota, & Polkey, 1987; Trenerry et al.,
1993; Zaidel, Esiri, & Oxbury, 1993; Mathern, Pretorius, &
Babb, 1995). In addition, one study by Saykin et al. (1989)
found that TLE patients with early onset of seizures were
impaired on both immediate and delayed recall conditions of
traditional memory tasks. However, tasks such as DMS and
SDR have not been used to examine the effects of earlyversus late-onset TLE on short- and long-term memory.
Further, only one study (Fedio & Mirsky, 1969) has examhied short- and long-term memory in children with TLE.
They found no difference between left temporal, right
temporal, and normal control children on span measures.
However, on supraspan tasks (a presumed long-term memory
task), the left temporal group performed worse on the verbal
task and the right temporal group performed worse on the
visual-spatial task. Unfortunately, there was a significant
difference in severity of disease between the two TLE
groups.
Thus, it is somewhat unclear whether disruption of the
medial temporal system during development impairs or
spares short-term memory performance in immature animals
or humans as measured by delayed response or delayed
recognition tasks. Given that memory systems and their
neural mechanisms undergo profound changes in both
capacity and organization during all stages of development
(Chugani, Phelps, & Mazziotta, 1987; Flavell, 1977; Huttenlocher, 1990; Janowsky, 1992; Kail, 1979), it is possible that
the representation of short- and long-term memory changes
across development. Medial temporal damage early in life
54
HERSHEY, CRAFT, GLAUSER, AND HALE
has been reported to produce deficits traditionally associated
with prefrontal dysfunction, whereas the same damage later
in life does not. Bachevalier (1994) has reported that early,
bilateral medial temporal damage in monkeys produces
emotional and social dysfunction as well as deficits in
learning and memory. She attributes this pattern to the
possibility that early medial temporal damage stimulates
reorganization of closely associated areas, such as the
prefrontal cortex. Another study on humans with TLE
reported that early-onset left TLE (LTLE) is associated with
significantly more perseverative responses on the Wisconsin
Card Sorting Test (generally sensitive to prefrontal dysfunction) than late-onset TLE. Right TLE (RTLE) was associated
with mild impairment regardless of age of onset (Strauss,
Hunter, & Wada, 1993). Further, Bilder et al. (1995) have
found strong correlations between anterior hippocampal
volumes and executive functions, such as planning skills and
response inhibition, in schizophrenics. They speculate that
early damage to the anterior hippocampus disrupts connections to the prefrontal cortex, affecting the entire frontolimbic system. The short-term memory system, another
prefrontally mediated skill, may also be affected by early
medial temporal damage.
Short-term spatial memory appears to rely heavily on
dorsolateral prefrontal cortex in adulthood and across development. The dorsolateral prefrontal cortex is reciprocally
connected to the medial temporal region and the inferior
parietal cortex, and the medial temporal region receives
projections from the inferior parietal cortex. All three areas
are activated during spatial delayed response tasks (Friedman & Goldman-Rakic, 1991; Goldman-Rakic, 1987; Goldman-Rakic, Selemon, & Schwartz, 1984). The medial temporal region and prefrontal cortex appear to be responsible for
the mnemonic aspects of the SDR task, whereas the inferior
parietal region appears to be responsible for initial nonmnemonic spatial processing (Goldman-Rakic, 1987). GoldmanRakic (1987) has hypothesized that the hippocampal and
prefrontal regions coordinate the management of memory
demands, with the prefrontal cortex responsible for shortdelay memory processing and the hippocampal region
responsible for longer term or larger capacity memory
processing. Short-term object recognition memory, as measured by die DMS task, is also supported by the reciprocally
connected areas of medial temporal and inferior frontal
cortex (Fuster, 1990; Mishkin & Murray, 1994).
It is possible that the relationship between medial temporal and prefrontal regions and their mnemonic responsibilities may change across development. Because the medial
temporal region develops relatively earlier than prefrontal
cortex, it may be responsible for short-term memory early in
development. As the prefrontal cortex develops, it may be
able to take over shorter term and less demanding memory
tasks, leaving more difficult and demanding tasks for medial
temporal processing. Early damage to the medial temporal
system could interrupt this transfer of functional specificity
and could thus affect short-term memory functioning. Therefore, we predict that children with early-onset TLE would
show deficits on SDR and DMS tasks at short delays,
demonstrating less sparing for short-term memory. More
traditional measures of human short- and long-term memory
(e.g., immediate and delayed recall of complex information,
span tasks) do not have animal analogues and so are difficult
to compare to SDR and DMS. However, based on the idea of
reduced short-term memory following early medial temporal damage, we also predicted that children with early-onset
TLE would perform poorly on immediate recall trials and
span tasks compared to controls.
Method
Participants
Participants consisted of 15 children with LTLE (10 males, 5
females; 12 right-handed, 3 left-handed) and 13 children with
RTLE (8 males, 5 females; all right-handed). These children were
recruited from the Pediatric Neurology Clinics at St. Louis
Children's Hospital and Children's Hospital Medical Center in
Cincinnati, Ohio. The children had no other medical diagnosis with
central nervous system effects; no evidence of mental retardation;
and no previous neurosurgery, head injury, or stroke. All children
with epilepsy had undergone BEG for localization of their seizures
within 2 years prior to testing, and, in most cases (26/28), they also
had magnetic resonance imaging (MRI). Of the 26 scans, 7 had
abnormal MRI readings ipsilateral to their epileptic foci (4 scans
showed distinct medial temporal atrophy ipsilateral to their epileptic foci, 1 showed anterior temporal atrophy, 1 showed lateral
ventricle enlargement, and 1 had poor myelination throughout). All
other scans were judged to be within normal limits. Seizures were
identified as unilateral, unifocal complex partial seizures emanating from the temporal lobe by a pediatric neurologist based on
seizure descriptions, observations, and EEG. It was not possible to
determine the precise location of patients' seizure foci within the
temporal lobe from these techniques, as both lateral and medial
temporal foci can lead to similar seizures and medial temporal
atrophy (Ebersole & Pacia, 1996). See Tables 1 and 2 for additional
group information.
TLE groups were statistically equivalent on every variable
measured that related to severity of the seizure disorder (duration,
age of onset, age at first risk factor for seizures, seizures within the
month prior to testing, seizures within the last year, and number of
generalized seizures in lifetime) and medication (number of
medications, and number of hours between last dose of medication
and testing start time). These results indicate that our two TLE
groups were well matched on these clinical variables. However,
there was a high level of variance in the number of seizures in the
Table 1
Means and Standard Deviations
of Demographic Variables by Group
Normal
control
(n = 19)
Left
temporal
(n = IS)
Right
temporal
(n = 13)
Variable
M
SD
M
SD
M
SD
Age
Grade
Parents' average years
ofeducation
Information
Block Design
11.53
5.32
2.7
2.4
11.24
5.00
2.6
2.5
11.16
5.17
2.4
2.2
13.71
12.68
10.79
2.2
2.6
3.6
13.93
10.00*
8.73
2.4
3.2
4.1
13.27
8.62*
8.77
2.0
2.1
2.5
*p < .05, a significant difference from the normal control group.
MEMORY IN EARLY TEMPORAL LOBE DYSFUNCTION
Table 2
55
Measures
Means and Standard Deviations of Clinical Variables
by Epilepsy Group
Left temporal
Wechsler Intelligence Scale for Children—3rd Edition
Right temporal
Variable
M
SD
M
Age of onset
Age at first risk factor
Duration of seizure disorder
Months since last seizure
Hours since last medication dose
Number of medications
Number of seizures in last
month
5.6
2.7
2.9
3.0
5.7
3.5
3.7
2.9
5.8
11.3
3.9
9.9
5.5
18.4
4.9
25.9
SD
b
2.7"
1.1
1.2
0.6
3.8
0.9
1.8
0.5
0.0
0.0
0.5
1.2
"n = 13. "re - 11.
year prior to testing in the LTLE group due to one outlier.1 Analyses
were computed both with and without this participant, and no
differences were obtained in any of the results. All analyses
reported here included this participant.
As expected, duration and age of onset were significantly
inversely correlated with each other within both LTLE (r = -.75,
p < .01) and RTLE (r = -.88, p < .01) groups. Due to these
strong correlations, any effects of age of onset must be considered
to be partly due to effects of duration. Duration and age at time of
testing were correlated (LTLE: r = +.65,p < .01; RTLE: r = +.67,
p = .01). See Table 2 for means and standard deviations.
A normal comparison (NC) group consisted of 19 participants,
who were matched on the basis of age, sex, and parents' years of
education (11 males, 8 females; 18 right-handed, 1 left-handed).
Children in the NC group had no history of brain injury, stroke, or
epilepsy, were not on any medications, and did not have any other
medical diagnoses with central nervous system effects. These
children were recruited from local private and parochial schools
and from the community. NC and epilepsy participants were
between the ages of 7 and 16. For all children, a parent gave written
informed consent prior to their participation.
Mean age at time of testing and mean years of education for
mother and father were statistically equivalent across all three
groups. Three mothers in the NC group and one mother in the
LTLE group reported only their educational level, due to the
fathers' absence from the home and lack of knowledge regarding
the fathers' present level of education and occupation. To reflect the
educational level of each child's household more accurately, a
mean parents' years of education variable was calculated. For
households with two parents, an average years of education was
calculated. For households with only the mother, the mother's
years of education was used for the mean parents' years of
education. This variable was not significantly different between the
groups. See Table 1 for means and standard deviations.
Procedure
Children with epilepsy were tested at St. Louis Children's
Hospital or Children's Hospital Medical Center in Cincinnati,
Ohio. NC children were tested either at St. Louis Children's
Hospital or at their school. All tasks (with the exception of the
WISC-III subtests) were developed with two equivalent versions,
because some participants were tested twice for the purposes of
another study. Only the first session is reported here. The two
versions were counterbalanced across groups.
(WISC-III; Wechsler, 1991)
Two subtests (Information, Block Design) were given as a
measure of general cognitive functioning. Performance on these
tests provided an estimate of each child's basic verbal and spatial
functioning as compared to an age-matched normative group.
SDR
This task was used to measure participants' spatial memory
across short and long delays. It involves the ability to hold spatial
information in memory for a brief or extended amount of time and
to update that information repeatedly. The basic components of this
task were adapted for use in humans by Luciana et al. (Luciana,
Depue, Arbisi, & Leon, 1992). This methodology was used with
some modification for our purposes. Participants were required to
focus on a central fixation point on a computer screen, While they
remained fixated, a cue appeared in one of 32 possible locations at a
4.5-in. (10.8 cm) radius from a central fixation point for 150 ms, a
duration too brief for any eye movements to occur. The fixation
cross then turned gray for a delay period of either 2 s, 30 s, or 60 s.
During the delay, participants were required to fixate on the center
cross while they listened to a tape on which a voice spoke letters at
the rate of one per second. They were instructed to say "yes" out
loud whenever a letter A was heard. The experimenter monitored
the children's eye movements and verbally cued the children to
fixate on the cross whenever they appeared to move their eyes.
After the delay, the fixation cue turned black, and they were asked
to point to the place on the computer screen where they remembered seeing the cue. The experimenter then moved the cursor with
a mouse to the point where the children were pointing and recorded
that location. Responses were measured in X and Y coordinates and
compared to the actual location of the cue. Thirty-two experimental
trials were presented, eight trials at each delay, plus eight trials with
no mnemonic load. On these "cue-present" trials, the cue was
present during the delay and response phase. This set of trials
allowed some indication of the children' pointing accuracy. Mean
error (distance from target) was calculated for each child for each
type of trial (2 s, 30 s, 60 s, cue-present).
DMS
A DMS task was used to measure pattern recognition memory
across short and long delays. The general task specifications were
derived from Diamond (1990), but different stimuli were used to
make this a more challenging task. In this task, participants were
seated in front of the computer screen. A trial consisted of the
following: A line drawing appeared in the center of the computer
screen for 2 s. Participants were instructed to study the drawing.
These drawings were abstract, geometrical figures that were
matched for major figural components and thus required effort to
distinguish. Unique drawings were used on each trial. The drawing
disappeared and a central fixation point remained on the screen for
varying delays (2 s, 30 s, 60 s). During the delay, participants were
lr
This child had over a thousand seizures in the year preceding
her participation in this study. However, most of these seizures
were in the first half of the year. After changing medications, she
achieved excellent seizure control and had no seizures in the few
months preceding her testing session.
56
HERSHEY, CRAFT, GLAUSER, AND HALE
instructed to listen to a tape and say "yes" whenever they heard a
letter A. When the fixation point disappeared, two drawings
appeared, one left of center and one right of center. One of these
was the drawing that appeared just prior in the trial. The participants were instructed to press the computer key corresponding to
the old drawing (the left key or the right key). Three practice trials
were given. The experimental segment consisted of 8 trials at each
delay period for a total of 24 trials. Total number of errors and
median response time were calculated for each participant for each
delay condition (2 s, 30 s, 60 s).
Story Recall Task
The story recall task was used to test verbal declarative memory.
Immediate and delayed recall trials in free recall formats were
given. Participants heard two brief narratives containing 18 informational bits each. They were then asked to recall as much of each
story as possible immediately after hearing each paragraph (immediate recall) and following a 25 to 30-min delay (delayed recall).
Credit was given for each informational bit recalled verbatim and
half credit was given for accurate paraphrases. Confabulations
(recalling information clearly not related to the story) were also
recorded. Total verbatim, paraphrase, and confabulation scores
were calculated for immediate and delayed recall conditions. The
paragraph recall task has been used extensively in previous
investigations on memory (Craft, Zallen, & Baker, 1992; Newcomer, Craft, Hershey, Askins, & Bardgett, 1994) and is a
well-validated declarative memory task (Squire, Shimamura, &
Graf, 1987).
Pattern Recall Task
The pattern recall task was used to test visual declarative
memory. Immediate and delayed recall trials were administered.
Children were presented with a page consisting of three separate
patterns constructed of four dark-colored blocks each on a 3 X 3
matrix (12 colored blocks out of 27 total blocks). They were
instructed to study the patterns for later recall. After the children
viewed the page for 10 s, it was removed from sight. The children
then were asked to reproduce the three patterns and their locations
on the page on another piece of paper with three blank 3 x 3
matrices. After a 25 to 30-min delay, participants were asked to
recall the patterns once more. On all recall trials, 1 point was given
for each correctly placed block in a pattern, A total correct score
was calculated for immediate and delayed recall conditions. This
total correct score was reduced by 1 point for every extra block
beyond 12 that the child marked. Performance on this task has
shown to be sensitive to changes in memory functioning in a
previous study (Craft et al., 1992).
Verbal Span
Verbal span was administered as described in Hale et al. (Hale,
Myerson, Rhee, Weiss, & Abrams, 1996) and is consistent with
Baddeley's model of verbal short-term memory (Baddeley, 1992).
This task was used as a measure of verbal short-term memory with
and without an interference condition. The interference condition
served to place a higher load on the working memory system.
Without interference.
Participants observed a series of digits
that appeared one at a time inside a 4 X 4 matrix on the left side of
the screen. Each digit appeared for 2 s with a 1-s intertrial interval.
When an empty matrix appeared at the end of the series, participants had to recall the series of numbers in the same order that they
appeared. The series began with one digit and could potentially end
with a series of nine digits. Two trials were given at each series
length. If the children correctly recalled one or both trials at a given
series length, they advanced to the next series length. If both trials
were failed at a given length, the task ended, and 1 point was given
for every correct response.
With interference.
This version was similar to the previous
version except that participants also had to name the colors in
which the digits appeared. Digits were one of three colors: red,
white, or blue. Participants were familiarized with the colors before
beginning any trials. As each digit appeared, participants were
required to name the color of the digit. When the blank matrix
appeared, they were instructed to recall the series of digits that
preceded it. Response scoring and the discontinuation criteria were
as stated previously.
Spatial Span
Spatial span was administered as described in Hale et al. (1996)
and is consistent with Baddeley's model of spatial short-term
memory (Baddeley, 1992). This task was used as a measure of
spatial short-term memory with and without an interference
condition. The interference condition served to place a higher load
on the working memory system.
Without interference.
Participants were seated in front of a
computer on which they were shown a series of Xs in different
locations within a 4 X 4 matrix, one at a time. Each X appeared for
2 s with an intertrial interval of 1 s. When a blank matrix appeared,
participants were required to mark on the computer screen where
the Xs in the previous series had appeared. There was a limited time
in which they could recall the series. The series began with one X
and could potentially end with a series of nine Xs. Two trials were
given at each series length. If participants correctly recalled one or
both trials at a given series length, they advanced to the next series
length. If both trials were failed at a given length, the task ended,
and 1 point was given for every correct response.
With interference.
The basic structure of this task was similar
to spatial span without interference except that the Xs appeared in
one of three colors (red, white, or blue). Participants were
instructed to identify which color each X was drawn in by pointing
to a palette of the three possible colors to the right of the matrix.
When the empty matrix appeared, participants were required to
mark the locations in which the Xs in the series appeared. Response
scoring and discontinuation criteria were as stated previously.
Response Inhibition Task
The Stroop Color and Word Test has been shown to be sensitive
to frontal lobe dysfunction and requires response inhibition (Ferret,
1974). The standard version of this task involves reading words.
Because our participants varied in reading ability due to their age,
we developed a task that involves response inhibition but does not
require word reading. In this task, participants were first shown a
2 X 2-in. ( 5 X 5 cm) block of color (either red, blue, or green)
against a black background, which appeared randomly in one of
four quadrants on a computer screen, and they were asked to name
the color (alone condition). Voice onset time was recorded by a
voice key interfaced with the computer, and participants' verbal
responses were recorded on the computer after every trial by an
experimenter. Thirty trials, 10 of each color, were given. Then
participants were shown the same size block of color outlined in
black in the center of a larger ( 5 X 5 in., 9.5 X 9.5 cm) block of
color, again appearing randomly in one of four quadrants of the
computer screen. Participants were again asked to name the color
of the small block (the block in the middle). Sixty trials were given.
57
MEMORY IN EARLY TEMPORAL LOBE DYSFUNCTION
On half of the trials, both blocks were the same color (congruent
condition); on the other half of the trials, the blocks were different
colors (discongruent condition), requiring the children to inhibit
their response to the larger, more prominent color. Reaction time
and accuracy were recorded and compared between conditions.
Results
Memory Measures
SDR Task
A repeated measures general linear models analysis was
conducted on SDR error scores (millimeters between the
target and the response) with group (NC, LTLE, RTLE) as
the independent variable and delay (cue-present, 2 s, 30 s, 60
s) as the repeated measure. A significant main effect was
obtained for delay, F(2,44) = 117.72, p< .01, as well as an
effect of group, F(2, 44) = 3.32, p = .05. In addition, a
significant interaction between group and delay was obtained, F(6,44) = 4.44, p < .01. Repeated measures general
linear models analyses were also carried out on pairs of
groups (NC and LTLE, NC and RTLE, LTLE and RTLE).
These analyses revealed that the interaction between group
and delay was present when comparing NC and LTLE, F(3,
32) = 7.76, p < .01, and NC and RTLE, F(3, 30) = 6.34,
p < .01, but not when comparing the two epilepsy groups.
Finally, separate general linear models analyses was conducted on all groups at each delay condition. There were
strong group effects at the 60-s delay only, F (2,44) = 5.87,
p < .01. Bonferroni corrected post hoc comparisons were
conducted that revealed that the RTLE and the LTLE groups
performed significantly worse than the normal controls at
the 60-s delay (see Figure 1). No group had any apparent
60 -,
50 -
•
Normal Control
•
Left Temporal
A
Right Temporal
40-
30 -
20 -
10 -
Table 3
Means and Standard Deviations ofDMS Error
Rates by Group
Normal
control
(« = 19)
Left
temporal
(n = 14)
Right
temporal
(« = 13)
Delay
M
SD
M
SD
M
SD
2s
30s
60s
.07
.05
.01
.11
.06
.04
.14
.09
.11
.16
.12
.11
.09
.09
.07
.15
.13
.13
Note.
DMS = delayed match to sample.
difficulty with the sensory or perceptual aspects of the task,
demonstrated by their accurate performance at the cuepresent condition. In addition, age of onset was not associated with performance at any delay for the two epilepsy
groups.
DMS
A repeated measures general linear models analysis was
conducted on DMS error rates (ratio of number of incorrect
responses to total number of trials in that condition) with
group (NC, LTLE, RTLE) as the independent variable and
delay (2 s, 30 s, 60 s) as the repeated measure. There was no
significant main effect of delay, but there was a main effect
of group, F(2,44) = 3.45, p < .05. The interaction between
group and delay was not significant. Inspection of the data
revealed that one LTLE participant performed at chance
levels (50%), which was much worse than the other
participants. When this participant's data were removed
from the analysis, the main effect of group was no longer
present (p = .09). See Table 3 for means and standard
deviations of these corrected data. As can be seen from these
data, the DMS task was insensitive to group differences most
likely due to ceiling effects. To examine the relationship of
age to the rate of ceiling performance, a median split on age
was performed for each group. On average, 28% of younger
participants and 34% of older participants achieved ceiling
performance across conditions, indicating that age was not
the predominant reason for ceiling level performance.
A repeated measures general linear models analysis was
also conducted on DMS response times with group (NC,
LTLE, RTLE) as the independent variable and delay (2 s, 30
s, 60 s) as the repeated measure. There was a significant
main effect of delay, F(2, 88) = 39.06, p < .001 (response
times increased across delay conditions), but the main effect
of group and the interaction between group and delay were
not significant.
Story Recall
Cue-present
2
30
60
Delays (seconds)
Figure 1. Spatial delayed response: Mean error scores and
standard errors for each group at each delay. Asterisks denote a
significant difference from the normal control group.
Data from immediate and delayed recall trials were
analyzed using a repeated measures general linear models
analysis with group (NC, LTLE, RTLE) as the independent
variable and delay (immediate, delayed recall) as the
repeated measure. The dependent measure was the number
of verbatim points plus paraphrase points obtained at recall.
58
HERSHEY, CRAFT, GLAUSER, AND HALE
A significant effect of delay, F(2, 44) = 30.15, p < .01
(immediate recall greater than delayed recall) was obtained,
but the effect of group and the interaction were not
significant (see Figure 2).
Confabulation errors were also analyzed with the same
repeated measures analysis as described previously. This
analysis revealed a significant effect of delay on number of
confabulations during recall, F(l, 44) = 9.64, p < .05, with
more confabulatory responses present in delayed recall than
in immediate recall. No effect of group or interaction
between group and delay was obtained.
Pattern Recall
Data from immediate and delayed recall trials were
analyzed using a repeated measures general linear models
analysis with group (NC, LTLE, RTLE) as the independent
variable and delay (immediate and delayed recall) as the
repeated variable. The dependent measure was the number
of correctly placed boxes (out of 12) with a penalty of 1
point for every extra box (above 12) that was marked. This
type of error occurred equally frequently across groups.
Analyses were conducted on both penalized and unpenalized
scores; the results were the same. The results reported here
are for the penalized scores.
A significant main effect for group, F(2, 44) = 4.52, p <
.05, was obtained, but the main effect for delay was not
significant. The interaction between group and delay was
borderline significant, F(2, 44) = 3.13, p = .05. Repeated
measures general linear models analyses were carried out on
pairs of groups (NC and LTLE, NC and RTLE, LTLE and
RTLE). These analyses revealed that the interaction between
group and delay was present when comparing the normal
control group against the LTLE group, F(l,32) = 5.11,p<
.05, but not when comparing the NC against the RTLE
groups or when comparing two epilepsy groups against each
30 _,
25 -
20 -
15 -
10 -
Normal Control
11 E
10
5
1 9
*
8-
y
7-
.
E
6 -
Normal Control
Left Temporal
Z
Right Temporal
Immediate Recall
Delayed Recall
Figure 3. Pattern recall: Mean number of correctly recalled
pattern elements and standard errors for each group at immediate
and delayed recall conditions. Asterisks denote a significant
difference from the normal control group.
other. Finally, general linear models analyses were conducted on all groups on each condition separately. Strong
group effects were found for the immediate recall condition
only, F(2, 44) = 5.83, p < .01. Post hoc Bonferroni corrected t tests were conducted on immediate recall scores that
revealed that both epilepsy groups scored significantly lower
than the NC group on immediate recall (see Figure 3).
Verbal Span
A repeated measures general linear models analysis was
performed on verbal span scores with group (NC, LTLE,
RTLE) as the independent variable and condition (without
interference, with interference) as the repeated measure.
This analysis revealed a significant effect of condition, F(l,
44) = 41.26, p < .01 (with interference < without interference), and group, F(2, 44) = 4.14, p < .05. The interaction
between group and condition was nonsignificant. Bonferroni
corrected post hoc comparisons between pairs of groups
revealed that the RTLE group performed significantly worse
than the NC group on the with interference condition. The
LTLE group was impaired relative to the NC group at a trend
level on the with interference condition (p = .07; see
Table 4).
Left Temporal
Right Temporal
Spatial Span
5 -
Immediate Recall
Delayed Recall
Figure 2. Story recall: Mean bits recalled and standard errors for
each group at immediate and delayed recall conditions.
A repeated measures general linear models analysis was
performed on spatial span scores with group (NC, LTLE,
RTLE) as the independent variable and condition (without
interference, with interference) as the repeated measure. The
analysis revealed a significant effect of condition, F(2,44) =
127.90, p < .01 (with interference < without interference;
see Table 4), but no effect of group. However, due to the
59
MEMORY IN EARLY TEMPORAL LOBE DYSFUNCTION
Table 4
Means and Standard Deviations of Span Task Performance by Group
Task
Verbal span
No interference
Interference
Spatial span
No interference
Interference
Normal control
(n = 19)
Left temporal
(" = 15)
Right temporal
(n = 13)
M
SD
M
SD
M
SD
10.8
9.4
2.3
2.5
10.1
7.8**
2.1
2.3
9.3
6.3*
2.7
3.3
10.3
6.6
3.2
4.1
7.7**
4.3**
2.7
2.7
8.5***
4.9***
3.5
3.5
*p < .05, a significant difference from the normal control group. **p < .07, different from normal
control group, trend level. ***/> < .09, different from normal control group when outlier is
removed, trend level.
effects in the verbal span task, and the apparently lower
performance of the epilepsy groups compared to controls in
this task, exploratory comparisons were performed between
each epilepsy group and the control group. For the left
temporal group, performance on both conditions was different from controls at a trend level (ps < .07). Although the
right temporal group's mean scores were generally equivalent to the left temporal group, their standard deviations
were higher. When the data were inspected on a participantby-participant basis, an outlier was discovered. When this
participant's data were removed, there was a trend level
difference between this revised group and the control group
for both conditions (ps < .09).
Response Inhibition Task
Two participants (1 in the LTLE group and 1 in the RTLE
group) had missing data on this task due to technical
problems. A repeated measures general linear models analysis was conducted on response inhibition median reaction
times with group (NC, LTLE, RTLE) as the independent
variable and condition (alone, congruent, discongruent) as
the repeated measure. This analysis revealed a significant
effect of condition, F(2, 42) = 78.32, p < .01, but no main
effect of group and no interaction between group and
condition. All conditions were significantly different from
each other, with average reaction time increasing across
conditions (alone, congruent, discongruent; see Figure 4).
A repeated measures general linear models analysis was
conducted on accuracy rates with group (NC, LTLE, RTLE)
as the independent variable and condition (alone, concordant, discordant) as the repeated measure. This analysis
revealed that the main effect of group was not significant,
but the main effect for condition was significant, F(2, 42) =
10.27, p < .01. Participants were significantly more accurate
in the alone condition as compared to the discongruent
condition, and in the congruent condition as compared to the
discongruent condition. The difference between the alone
and congruent conditions was not significant. The interaction between group and condition was not significant.
RTLE) as the independent variable. This analysis revealed a
significant effect of group, F(2, 44) = 9.56, p < .01. Post
hoc Bonferroni corrected comparisons revealed that the two
epilepsy groups scored significantly lower than the NC
group but were not significantly different from each other,
although the RTLE group had relatively lower scores than
the LTLE group (see Table 1).
A general linear models analysis was also conducted on
Block Design scaled scores with group (NC, LTLE, RTLE)
as the independent variable. The main effect of group was
not significant (see Table 1).
To understand the possible relationship between IQ and
performance on memory tasks, we conducted Pearson
correlations between Information scaled scores and performance on the conditions of the SDR and pattern recall tasks
that demonstrated significant group differences. For all three
groups, these correlations were nonsignificant.
Clinical Variables
Age of onset was also correlated with all task performance variables to determine its effect. None of these
900 -,
800 -
700 -
600 -
500 -
400 -
•
•
A
Normal Control
Left Temporal
Right Temporal
300
0
General Cognitive Measures
A general linear models analysis was conducted on
Information scaled scores with group (NC, LTLE, and
Alone
Congruent Discongruent
Figure 4. Response inhibition: Median reaction times and standard errors for each group by condition.
60
HERSHEY, CRAFT, GLAUSER, AND HALE
correlations were significant for either epilepsy group or for
both groups combined. Age at first risk factor was also
correlated with task performance variables. These correlations were conducted in an effort to determine if the timing
of the first insult to the brain is associated with performance
in children with epilepsy. These correlations were not
significant. Thus, in this sample, neither age at first insult nor
age at first seizure was associated with cognitive functioning. The nonsignificance of these correlations could be
affected by our relatively small sample sizes and the wide
age ranges. Because age has a strong effect on cognitive
functioning, it may overpower any more subtle effects of
these clinical variables.
Finally, to determine the effect of medication dosage on
performance, we correlated total daily dose with select
performance variables (SDR, pattern recall, and story recall)
for children only on Tegretol (n = 18). None of these
correlations was significant. Thus, it is unlikely that medication dosage alone can account for any group differences.
Discussion
The present study examined the pattern of short- and
long-term memory function in children with early-onset
TLE with two tasks used extensively in animal work (SDR
and DMS) as well as with a supporting battery of clinical
and experimental measures. When the data from all tasks are
considered (see Table 5), the results can be grouped into
three major findings: (a) Children with focal TLE were not
impaired on short-delay memory tasks associated with the
prefrontal cortex working memory system; their performance was variable on short-term memory tasks with
heavier working memory demands, (b) Children with focal
TLE were impaired on spatial tasks with high memory loads
or long delays, demand characteristics that have been
previously associated with the medial temporal memory
system (Gabrieli, Keane, & Stebbins, 1993; Squire, 1992).
(c) Children with focal TLE were less impaired on comparable verbal medial temporal-related memory tasks.
Variably Spared Short-Term Memory
The primary hypothesis of this study was that children
with early-onset TLE would show short- and long-term
memory deficits due to developmental disruption of the
medial temporal-prefrontal memory system. On the tasks
most closely linked to prefrontal cortex and short-term
memory in animals and humans (short-delay conditions on
SDR and DMS), this hypothesis was not supported. Childhood TLE did not affect short-term memory performance,
but it did affect longer term memory on the SDR task. This
pattern is consistent with the performance of adult monkeys
and humans with medial temporal damage on spatial delayed response tasks (Backer Cave & Squire, 1992; Kowalska, 1995; Rains & Milner, 1994; Zola-Morgan & Squire,
1985). Ceiling effects on our version of the DMS impeded
our ability to detect any effects using this paradigm. Thus, it
is unlikely that early temporal lobe dysfunction affects the
development of prefrontally mediated short-term memory as
measured by these two tasks.
However, on the span tasks, a more complex pattern was
evident. Children with TLE were unimpaired on simple
verbal span (no interference condition) relative to controls,
but they were impaired on simple spatial span (trend level
significance). All three groups performed better on the
verbal span task than on the spatial span task, indicating that
manipulating the spatial material was inherently more
demanding than manipulating the verbal material. When a
dual task (interference condition) was added to the span
tasks, the children with TLE performed poorly with both
types of material compared to controls. It is possible that the
more demanding nature of the spatial span task overloaded
the prefrontally mediated short-term memory system, even
without an added interference condition. This possibly is
consistent with the following discussion of other high-load
or long-delay spatial tasks.
Spatial Medial Temporal-Related Memory Deficits
The SDR task, long-delay condition only, pattern recall
task, and spatial span with interference all have heavy
demands on the declarative memory system. It is not
surprising that participants who have difficulty holding one
location on-line for 60 s (as in the SDR task) also have
difficulty holding 12 locations on-line for 10-15 s (as in the
pattern recall task) or 4 to 5 locations under dual task
conditions (spatial span with interference). Gabrieli and
Table 5
Summary of Task Performance by Seizure Groups Relative to Controls
Left temporal
(n = 15)
Right temporal
(n = 13)
SDR
DMS
Impaired at 60-s delay
Impaired at 60-s delay
Story recall
Pattern recall
•
—
Impaired— immediate
recall
Impaired— interference condition2
Impaired"
Task
Verbal span
Spatial span
Response inhibition
Information
Block design
—
—
—
Impaired—immediate
recall
Impaired— interference condition
Impaired3
—
Lower
Lower
—
Note. SDR = spatial delayed response; DMS = delayed match to sample.
"Trend level effect.
—
—
MEMORY IN EARLY TEMPORAL LOBE DYSFUNCTION
61
colleagues (1993) reported that patients with amnesia due to
Consortium, 1995; Novelly et al., 1984). Of the three
medial temporal damage performed adequately on a lowload short-term memory task, but they were impaired on a
high-load short-term memory task. The researchers speculated that the medial temporal lobe system does play a role in
short-term memory tasks, particularly when the information
load exceeds what they call "primary memory buffers in
frontal and other cortical regions" (p. 1002). Similar ideas
published studies on the memory skills of children with
TLE, one found the same pattern as adults (Fedio & Mirsky,
1969) and the other two found a similar pattern, although
less distinct (Cohen, 1992; Jambaque et al., 1993). However,
have also been proposed by Eichenbaum et al. (1994), who
stated that the parahippocampal gyrus may play the role of
intermediate memory, holding information on-line that the
neocortical short-term memory system cannot, either due to
delay length or capacity limitations.
Based on these speculations, children with TLE would be
impaired on short-term memory tasks compared to normal
controls, but only under high memory demands. When
children are required to hold a large amount of information
on-line for later recall, the immature prefrontal memory
system's capacity may be overwhelmed. The information
would then be held on-line by the medial temporal lobe
memory system, which, in the case of children with TLE, is
impaired and is thus unable to accurately handle the
information.
It may be that in the domain of memory, early medial
temporal damage does not affect the prefrontal cortex or
tasks that can be performed exclusively in that region.
However, due to the immaturity of the prefrontal cortex in
children, certain memory tasks may not be handled as well
or as exclusively by the prefrontal cortex and may rely more
on earlier developed and closely connected aspects of the
memory system, such as the medial temporal region. Thus,
the patterns of impairment on memory tasks that involve
both regions are different from those seen in adults with fully
developed cortex and dysfunctional medial temporal regions. As these children undergo the development of their
prefrontal cortex, we speculate that they would demonstrate
less impairment on some of the less demanding "frontal"
memory tasks, such as the simple spatial span task.
Relatively Intact Verbal Medial
Temporal-Related Memory Skills
Children with TLE were impaired on verbal span with
interference but not on a traditional and well-validated
verbal declarative memory task, story recall. Interestingly,
many types of focal, developmental injuries to either the left
or right hemisphere result in greater impairment on spatial
tasks than on verbal tasks (Stiles & Thai, 1993). Thus, it is
not surprising that our left and right temporal lobe seizures
groups performed equivalently across a wide variety of
spatial and verbal tasks. In contrast, many studies of adults
with unilateral TLE have supported the idea of the lateralization of material-specific memory deficits. Generally, LTLE
is associated with verbal delayed memory deficits, and
RTLE is associated with visuospatial delayed memory
deficits (Novelly et al., 1984; Ojemann & Dodrill, 1985;
Saykin et al., 1989). Differences between unilateral TLE
groups on visuospatial memory tasks are generally more
difficult to document (Barr, & The Bozeman Epilepsy
this first study had significant differences between groups in
seizure severity (left temporal more severe than right
temporal), the second study had significant differences
between groups in age at time of testing (left temporal
younger than right temporal), and the third study had one
very small group (n = 6) making their results somewhat
questionable. It is conceivable that in the first two studies the
left temporal groups appeared more unpaired on verbal
memory in part due to their greater severity and younger age
at time of testing.
In addition, children with TLE in our study had lower
Information subtest scaled scores than the NCs, although
they were still within the average range. The Information
subtest is thought to be an estimate of general verbal
intelligence and is itself a measure of semantic memory. It
could be argued that performance on this test does not reflect
a deficit in either area as much as it does a side effect of
having a chronic illness, which may cause children to miss
school more than their peers. This phenomenon has been
noted in children with other types of chronic illnesses (Ryan,
1990). However, it is possible that the significant differences
obtained between groups on memory tasks are explained
simply by differences in verbal intellectual level or semantic
memory, or the differences are exaggerated by the high level
of verbal functioning of the NCs rather than reflecting
impaired memory for the epilepsy groups. Several points
addressing this possibility can be made.
First, the NC group was matched to epilepsy participants
on parents' years of education and on gender. Mean parents'
years of education was comparable among all groups. We
did not match participants on intelligence scores due to the
fact that intelligence is considered to be an outcome measure
of seizure disorder. Matching according to outcome variables has been criticized for creating inappropriate control
groups (Meehl, 1970). Second, there were no significant
correlations between Information scaled scores and key
variables within each group. Thus, better performance on a
verbal intelligence test was not associated with better
performance on the spatial memory task for any participant
group.
Conclusion
In conclusion, although the organization of memory
systems within the adult brain has received tremendous
attention in recent decades, the growth and refinement of
these memory systems have been less intensively studied.
The present study addressed the separable nature of shortand long-term memory in a population with early temporal
lobe dysfunction. The results indicated that early-onset TLE
affects short- and long-term memory differently across
certain task variables. Short-term memory performance as
measured by a spatial delayed response task was not affected
in children with TLE, but performance at a longer delay on
62
HERSHEY, CRAFT, GLAUSER, AND HALE
the same task was impaired, consistent with findings in
adults. Further, although children with both left and right
TLE were largely impaired on spatial memory tasks that had
high memory loads or long delays, they were relatively
unimpaired on comparable verbal tasks. This pattern of
impairment differs qualitatively from findings in adults with
early or late medial temporal lobe damage in whom sparing
of immediate recall, impairment in verbal memory, and
some material-specific patterns of impairments are seen.
These differences may be due to an interaction between the
immaturity of the prefrontal cortex and the dysfunction of
the medial temporal region in the mediation of short- and
long-term declarative memory.
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Received February 15, 1996
Revision received April 28, 1997
Accepted May 5, 1997
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