short-term and long-term memory in early temporal...

Neuropsychology1998, Vol. 12, No. 1,52-64

Copyright 1998 by the American Psychological Association, Inc.0894-4105»8/$3.00

Short-Term and Long-Term Memory in EarlyTemporal Lobe Dysfunction

Tamara HersheyWashington University

Tracy A. GlauserChildren's Hospital Medical Center

Cincinnati, Ohio

Suzanne CraftSeattle-American Lake Veterans Affairs Medical Center

and University of Washington

Sandra HaleWashington University

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 inthe brain has often focused on identifying dissociablesubsystems. Many types of memory distinctions have beenproposed on the basis of cognitive, neuropsychological, andneurophysiological evidence, such as semantic-episodicmemory (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 distinc-tion between short- and long-term memory following earlytemporal lobe dysfunction in children.

Short-term memory, the ability to represent information

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 require-

ments for Tamara Hershey's doctoral degree and was supported in

part by a Washington University Dissertation Fellowship. Prelimi-

nary results from this study were presented at the Second AnnualMeeting of the Cognitive Neuroscience Society held in San

Francisco, California, in 1995. We would like to thank the studentsand 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].

internally for brief periods of time, is considered to be afundamental feature of working memory (Baddeley, 1992;Goldman-Rakic, 1987). This ability is commonly not af-fected by medial temporal region damage in adult humansand animals. Long-term memory, the ability to store informa-tion for later recall, is impaired following damage to ordisruption of components of the medial temporal region. Avariety of tasks have been used in both animals and humansto demonstrate this distinction, most notably the delayednonmatch to sample (DNMS), delayed match to sample(DMS), and spatial delayed response (SDR) tasks. Thesetasks involve the brief presentation of a piece of informationfollowed by a delay. For the DNMS and DMS tasks, objectsor colors are generally used; for the SDR task, spatiallocations are used. After the delay has ended, participantsmust recognize or recall the piece of information presentedprior to the delay. On such tasks, adult animals and humanswith medial temporal damage are able to perform accuratelyon trials with short delays yet are impaired on trials withlonger 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; Kowal-ska, 1995; Rains & Milner, 1994; Zola-Morgan & Squire,1985). In general, delays greater than 15-30 s on these tasksare sensitive to medial temporal damage (Alvarez et al.,1994; Rains & Milner, 1994; Squire et al., 1988), althoughthis 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).

52

MEMORY IN EARLY TEMPORAL LOBE DYSFUNCTION 53

Short-term memory, as measured by the SDR task, has

been associated with the dorsolateral prefrontal cortex.

Following dorsolateral prefrontal damage, performance onthe SDR task is impaired on trials with the shortest delay(Bauer & Fuster, 1976; Freedman & Oscar-Berman, 1986;

Funahashi, Bruce, & Goldman-Rakic, 1993; Joyce & Rob-bins, 1991). In addition, studies have demonstrated that cellsin 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 informationon-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 isunimpaired following prefrontal cortex damage (Goldman-

Rakic, 1987). It has been proposed that the dorsolateralprefrontal cortex is highly involved in the short-term memoryof spatial information, whereas the inferior frontal cortex isinvolved in the short-term memory of object information

(Goldman-Rakic, 1987; Wilson et al., 1993). Thus, short-and long-term spatial and object recognition memory as

measured by DMS, but not DNMS, appear to be dissociablefollowing lesions to medial temporal versus dorsolateral orinferior prefrontal cortex (Alvarez et al., 1994; Winocur,

1992).This general pattern has also been reported in adult

humans with temporal lobe epilepsy (TLE), a disorderassociated with medial temporal dysfunction and neuropa-thology. Notably, these studies have focused on unilateralTLE, which may make comparisons somewhat difficult withanimal work, in which bilateral lesions are generally present.Short-term memory measures (immediate recall, span tasks,consonant or pattern trigram tasks) generally have notrevealed consistent differences between left and right tempo-ral lobe epileptics and their normal control groups (Delaney,Prevey & Mattson, 1982; Delaney, Rosen, Mattson, &Novelly, 1980; Lavadas, Umilta, & Provincial!, 1979). Ifdifferences have been found, they have occurred at delays ofgreater 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 themedial temporal region to treat intractable seizures, long-term memory generally becomes more impaired on clinicalmemory tasks (Ojemann & Dodrill, 1985; Wechsler, 1987).One recent study has addressed the impact of medialtemporal excisions in seizure patients on tasks similar tothose used in animal studies, such as DMS and SDR. Amongother interesting results, Owen et al. (Owen, Sahakian,Semple, Polkey, & Robbins, 1995) found that patients withamygdala-hippocampal excision were impaired on the long-est delay of the DMS task (12 s), with relatively normalperformance on shorter delays and a simultaneous matchingcondition. On a spatial recognition task, participants wereshown a list of spatial locations and then given two-choicerecognition trials 3-72 s later. Patients with amygdala-hippocampal excisions performed significantly worse thancontrols on this task. However, the data were not analyzed

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- andlong-term memory in developing animals and humans has

been less extensively reported. Bachevalier (1990) andMahut and Moss (1984) found that damage to the medial

temporal region in young monkeys produces long-termmemory impairment as measured by the DNMS task, similar

to results in adult monkeys. There have also been severalreports 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 evaluationsof these children have been limited at best, and no careful

analyses of short- and long-term memory have been con-ducted. In contrast, case studies of unilateral or bilateraltemporal 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 develop-mental 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 documentedthat unilateral TLE patients with early-onset seizures or anearly insult, such as febrile seizures, have more severememory 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 wereimpaired on both immediate and delayed recall conditions oftraditional memory tasks. However, tasks such as DMS andSDR have not been used to examine the effects of early-versus late-onset TLE on short- and long-term memory.Further, only one study (Fedio & Mirsky, 1969) has exam-hied short- and long-term memory in children with TLE.They found no difference between left temporal, righttemporal, and normal control children on span measures.However, on supraspan tasks (a presumed long-term memorytask), the left temporal group performed worse on the verbaltask and the right temporal group performed worse on thevisual-spatial task. Unfortunately, there was a significantdifference in severity of disease between the two TLEgroups.

Thus, it is somewhat unclear whether disruption of themedial temporal system during development impairs orspares short-term memory performance in immature animalsor humans as measured by delayed response or delayedrecognition tasks. Given that memory systems and theirneural mechanisms undergo profound changes in bothcapacity and organization during all stages of development(Chugani, Phelps, & Mazziotta, 1987; Flavell, 1977; Hutten-locher, 1990; Janowsky, 1992; Kail, 1979), it is possible thatthe representation of short- and long-term memory changesacross development. Medial temporal damage early in life

54 HERSHEY, CRAFT, GLAUSER, AND HALE

has been reported to produce deficits traditionally associatedwith prefrontal dysfunction, whereas the same damage laterin life does not. Bachevalier (1994) has reported that early,bilateral medial temporal damage in monkeys producesemotional and social dysfunction as well as deficits inlearning and memory. She attributes this pattern to thepossibility that early medial temporal damage stimulatesreorganization of closely associated areas, such as theprefrontal cortex. Another study on humans with TLEreported that early-onset left TLE (LTLE) is associated withsignificantly more perseverative responses on the WisconsinCard Sorting Test (generally sensitive to prefrontal dysfunc-tion) than late-onset TLE. Right TLE (RTLE) was associatedwith mild impairment regardless of age of onset (Strauss,Hunter, & Wada, 1993). Further, Bilder et al. (1995) havefound strong correlations between anterior hippocampalvolumes and executive functions, such as planning skills andresponse inhibition, in schizophrenics. They speculate thatearly damage to the anterior hippocampus disrupts connec-tions to the prefrontal cortex, affecting the entire fronto-limbic system. The short-term memory system, anotherprefrontally mediated skill, may also be affected by earlymedial temporal damage.

Short-term spatial memory appears to rely heavily ondorsolateral prefrontal cortex in adulthood and across devel-opment. The dorsolateral prefrontal cortex is reciprocallyconnected to the medial temporal region and the inferiorparietal cortex, and the medial temporal region receivesprojections from the inferior parietal cortex. All three areasare activated during spatial delayed response tasks (Fried-man & Goldman-Rakic, 1991; Goldman-Rakic, 1987; Gold-man-Rakic, Selemon, & Schwartz, 1984). The medial tempo-ral region and prefrontal cortex appear to be responsible forthe mnemonic aspects of the SDR task, whereas the inferiorparietal region appears to be responsible for initial nonmne-monic spatial processing (Goldman-Rakic, 1987). Goldman-Rakic (1987) has hypothesized that the hippocampal andprefrontal regions coordinate the management of memorydemands, with the prefrontal cortex responsible for short-delay memory processing and the hippocampal regionresponsible for longer term or larger capacity memoryprocessing. Short-term object recognition memory, as mea-sured by die DMS task, is also supported by the reciprocallyconnected areas of medial temporal and inferior frontalcortex (Fuster, 1990; Mishkin & Murray, 1994).

It is possible that the relationship between medial tempo-ral and prefrontal regions and their mnemonic responsibili-ties may change across development. Because the medialtemporal region develops relatively earlier than prefrontalcortex, it may be responsible for short-term memory early indevelopment. As the prefrontal cortex develops, it may beable to take over shorter term and less demanding memorytasks, leaving more difficult and demanding tasks for medialtemporal processing. Early damage to the medial temporalsystem could interrupt this transfer of functional specificityand could thus affect short-term memory functioning. There-fore, we predict that children with early-onset TLE wouldshow 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 difficultto compare to SDR and DMS. However, based on the idea ofreduced short-term memory following early medial tempo-ral damage, we also predicted that children with early-onsetTLE would perform poorly on immediate recall trials andspan 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 seizureswithin 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 epilep-

tic 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 emanat-

ing 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 Deviationsof Demographic Variables by Group

Variable

Normalcontrol

(n = 19)

M SD

Lefttemporal(n = IS)

M SD

Righttemporal(n = 13)

M SD

Age 11.53 2.7 11.24 2.6 11.16 2.4Grade 5.32 2.4 5.00 2.5 5.17 2.2Parents' average years

ofeducation 13.71 2.2 13.93 2.4 13.27 2.0Information 12.68 2.6 10.00* 3.2 8.62* 2.1Block Design 10.79 3.6 8.73 4.1 8.77 2.5

*p < .05, a significant difference from the normal control group.


Table 2Means and Standard Deviations of Clinical Variablesby Epilepsy Group

Left temporal Right temporal

Variable M SD M SD

Age of onset 5.6 2.9 5.7 3.7Age at first risk factor 2.7 3.0 3.5 2.9Duration of seizure dis-

order 5.8 3.9 5.5 4.9Months since last seizure 11.3 9.9 18.4 25.9Hours since last medica-

tion dose 2.7" 1.2 3.8b 1.8Number of medications 1.1 0.6 0.9 0.5Number of seizures in last

month 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, orepilepsy, 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, amean 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'sHospital 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 twoversions were counterbalanced across groups.

Measures

Wechsler Intelligence Scale for Children—3rd Edition

(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 atthe 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 remem-

bered 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 eachtype 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

lrThis 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, sheachieved excellent seizure control and had no seizures in the fewmonths preceding her testing session.


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 partici-

pants 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 infor-

mational bits each. They were then asked to recall as much of each

story as possible immediately after hearing each paragraph (imme-

diate 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; New-

comer, 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, partici-

pants 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' verbalresponses 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 inblack 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 colorof the small block (the block in the middle). Sixty trials were given.


On half of the trials, both blocks were the same color (congruentcondition); on the other half of the trials, the blocks were differentcolors (discongruent condition), requiring the children to inhibittheir response to the larger, more prominent color. Reaction timeand 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 ob-

tained, 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 con-

ducted 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

Table 3

Means and Standard Deviations ofDMS Error

Rates by Group

60 -,

50 -

40-

30 -

20 -

10 -

• Normal Control

• Left Temporal

A Right Temporal

Cue-present 2 30 60

Delays (seconds)

Figure 1. Spatial delayed response: Mean error scores andstandard errors for each group at each delay. Asterisks denote asignificant difference from the normal control group.

Normalcontrol

(« = 19)

Delay

2s30s60s

M

.07

.05

.01

SD

.11

.06

.04

Lefttemporal(n = 14)

M

.14

.09

.11

SD

.16

.12

.11

Righttemporal(« = 13)

M

.09

.09

.07

SD

.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 cue-

present condition. In addition, age of onset was not associ-

ated with performance at any delay for the two epilepsy

groups.

DMS


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.


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

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.


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 -

5 -

Normal Control

Left Temporal

Right Temporal

11 -

E 10

5

1 9

* 8 -

y 7 -

.E

Z

6 - Normal Control

Left Temporal

Right Temporal

Immediate Recall Delayed Recall

Figure 2. Story recall: Mean bits recalled and standard errors foreach group at immediate and delayed recall conditions.

Immediate Recall Delayed Recall

Figure 3. Pattern recall: Mean number of correctly recalledpattern elements and standard errors for each group at immediateand delayed recall conditions. Asterisks denote a significantdifference from the normal control group.

other. Finally, general linear models analyses were con-

ducted 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 cor-

rected 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


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 interfer-

ence), 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; seeTable 4).

Spatial Span


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


Table 4

Means and Standard Deviations of Span Task Performance by Group

Normal control(n = 19)

Task

Verbal spanNo interferenceInterference

Spatial spanNo interferenceInterference

M

10.89.4

10.36.6

SD

2.32.5

3.24.1

Left temporal

(" = 15)

M

10.17.8**

7.7**4.3**

SD

2.12.3

2.72.7

Right temporal(n = 13)

M

9.36.3*

8.5***4.9***

SD

2.73.3

3.53.5

*p < .05, a significant difference from the normal control group. **p < .07, different from normalcontrol group, trend level. ***/> < .09, different from normal control group when outlier isremoved, trend level.

effects in the verbal span task, and the apparently lowerperformance of the epilepsy groups compared to controls inthis task, exploratory comparisons were performed betweeneach epilepsy group and the control group. For the lefttemporal group, performance on both conditions was differ-ent from controls at a trend level (ps < .07). Although theright temporal group's mean scores were generally equiva-lent to the left temporal group, their standard deviationswere higher. When the data were inspected on a participant-by-participant basis, an outlier was discovered. When thisparticipant's data were removed, there was a trend leveldifference between this revised group and the control groupfor both conditions (ps < .09).

Response Inhibition Task

Two participants (1 in the LTLE group and 1 in the RTLEgroup) had missing data on this task due to technicalproblems. A repeated measures general linear models analy-sis was conducted on response inhibition median reactiontimes with group (NC, LTLE, RTLE) as the independentvariable and condition (alone, congruent, discongruent) asthe repeated measure. This analysis revealed a significanteffect of condition, F(2, 42) = 78.32, p < .01, but no maineffect of group and no interaction between group andcondition. All conditions were significantly different fromeach other, with average reaction time increasing acrossconditions (alone, congruent, discongruent; see Figure 4).

A repeated measures general linear models analysis wasconducted on accuracy rates with group (NC, LTLE, RTLE)as the independent variable and condition (alone, concor-dant, discordant) as the repeated measure. This analysisrevealed 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 accuratein the alone condition as compared to the discongruentcondition, and in the congruent condition as compared to thediscongruent condition. The difference between the aloneand congruent conditions was not significant. The interac-tion between group and condition was not significant.

General Cognitive Measures

A general linear models analysis was conducted onInformation scaled scores with group (NC, LTLE, and

RTLE) as the independent variable. This analysis revealed asignificant effect of group, F(2, 44) = 9.56, p < .01. Post

hoc Bonferroni corrected comparisons revealed that the twoepilepsy groups scored significantly lower than the NCgroup but were not significantly different from each other,although the RTLE group had relatively lower scores thanthe LTLE group (see Table 1).

A general linear models analysis was also conducted onBlock Design scaled scores with group (NC, LTLE, RTLE)as the independent variable. The main effect of group wasnot significant (see Table 1).

To understand the possible relationship between IQ andperformance on memory tasks, we conducted Pearsoncorrelations between Information scaled scores and perfor-mance on the conditions of the SDR and pattern recall tasksthat demonstrated significant group differences. For all threegroups, these correlations were nonsignificant.

Clinical Variables

Age of onset was also correlated with all task perfor-mance variables to determine its effect. None of these

900 -,

800 -

700 -

600 -

500 -

400 -

300

0

• Normal Control• Left TemporalA Right Temporal

Alone Congruent Discongruent

Figure 4. Response inhibition: Median reaction times and stan-

dard errors for each group by condition.


correlations were significant for either epilepsy group or forboth groups combined. Age at first risk factor was alsocorrelated with task performance variables. These correla-tions were conducted in an effort to determine if the timingof the first insult to the brain is associated with performancein children with epilepsy. These correlations were notsignificant. Thus, in this sample, neither age at first insult norage at first seizure was associated with cognitive function-ing. The nonsignificance of these correlations could beaffected by our relatively small sample sizes and the wideage ranges. Because age has a strong effect on cognitivefunctioning, it may overpower any more subtle effects ofthese clinical variables.

Finally, to determine the effect of medication dosage onperformance, we correlated total daily dose with selectperformance variables (SDR, pattern recall, and story recall)for children only on Tegretol (n = 18). None of thesecorrelations was significant. Thus, it is unlikely that medica-tion dosage alone can account for any group differences.

Discussion

The present study examined the pattern of short- andlong-term memory function in children with early-onset

TLE with two tasks used extensively in animal work (SDRand DMS) as well as with a supporting battery of clinicaland experimental measures. When the data from all tasks areconsidered (see Table 5), the results can be grouped intothree major findings: (a) Children with focal TLE were notimpaired on short-delay memory tasks associated with theprefrontal cortex working memory system; their perfor-mance was variable on short-term memory tasks withheavier working memory demands, (b) Children with focalTLE were impaired on spatial tasks with high memory loadsor long delays, demand characteristics that have beenpreviously associated with the medial temporal memorysystem (Gabrieli, Keane, & Stebbins, 1993; Squire, 1992).(c) Children with focal TLE were less impaired on compa-rable verbal medial temporal-related memory tasks.

Variably Spared Short-Term Memory

The primary hypothesis of this study was that childrenwith early-onset TLE would show short- and long-term

memory deficits due to developmental disruption of themedial temporal-prefrontal memory system. On the tasksmost closely linked to prefrontal cortex and short-termmemory in animals and humans (short-delay conditions onSDR and DMS), this hypothesis was not supported. Child-hood 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 monkeysand humans with medial temporal damage on spatial de-layed response tasks (Backer Cave & Squire, 1992; Kowal-ska, 1995; Rains & Milner, 1994; Zola-Morgan & Squire,1985). Ceiling effects on our version of the DMS impededour ability to detect any effects using this paradigm. Thus, itis unlikely that early temporal lobe dysfunction affects thedevelopment of prefrontally mediated short-term memory asmeasured by these two tasks.

However, on the span tasks, a more complex pattern wasevident. Children with TLE were unimpaired on simple

verbal span (no interference condition) relative to controls,but they were impaired on simple spatial span (trend levelsignificance). All three groups performed better on theverbal span task than on the spatial span task, indicating thatmanipulating the spatial material was inherently moredemanding than manipulating the verbal material. When a

dual task (interference condition) was added to the spantasks, the children with TLE performed poorly with bothtypes of material compared to controls. It is possible that themore demanding nature of the spatial span task overloadedthe prefrontally mediated short-term memory system, evenwithout an added interference condition. This possibly isconsistent with the following discussion of other high-loador long-delay spatial tasks.

Spatial Medial Temporal-Related Memory Deficits

The SDR task, long-delay condition only, pattern recalltask, and spatial span with interference all have heavydemands on the declarative memory system. It is notsurprising that participants who have difficulty holding onelocation on-line for 60 s (as in the SDR task) also havedifficulty holding 12 locations on-line for 10-15 s (as in thepattern recall task) or 4 to 5 locations under dual taskconditions (spatial span with interference). Gabrieli and

Table 5Summary of Task Performance by Seizure Groups Relative to Controls

Task

SDRDMSStory recallPattern recall

Verbal span

Spatial spanResponse inhibitionInformationBlock design

Left temporal(n = 15)

Impaired at 60-s delay

—• —

Impaired — immediaterecall

Impaired — interfer-ence condition2

Impaired"—

Lower—

Right temporal(n = 13)

Impaired at 60-s delay—

—Impaired — immediate

recallImpaired — interfer-

ence conditionImpaired3

—Lower

—

Note. SDR = spatial delayed response; DMS = delayed match to sample."Trend level effect.


colleagues (1993) reported that patients with amnesia due to

medial temporal damage performed adequately on a low-

load short-term memory task, but they were impaired on a

high-load short-term memory task. The researchers specu-

lated 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

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 re-

gions. 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 MedialTemporal-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 lateraliza-

tion 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 moredifficult to document (Barr, & The Bozeman Epilepsy

Consortium, 1995; Novelly et al., 1984). Of the three

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,

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 vari-

ables 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 short-

and 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


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, 1996Revision received April 28, 1997

Accepted May 5, 1997

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