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The Story Learning and Memory (SLAM) test: Equivalence of three forms and sensitivity to left temporal lobe dysfunction Jelena Djordjevic a, , Mary Lou Smith b , Viviane Sziklas a , Dominique Piper a , Sidonie Pénicaud a , Marilyn Jones-Gotman a a McGill University, Montreal, Quebec, Canada b University of Toronto, Toronto, Ontario, Canada abstract article info Article history: Received 1 December 2010 Revised 31 December 2010 Accepted 4 January 2011 Available online 26 February 2011 Keywords: Verbal learning Memory Story recall Temporal lobe epilepsy Neuropsychology Remembering meaningful information is an important component of verbal memory. However, ndings from existing story memory tests have been mixed in patients with temporal lobe epilepsy (TLE). We developed a test, the Story Learning and Memory (SLAM) test, in which a story is presented repeatedly until a performance criterion is reached, and verbatim recall is obtained only once, after a delay. In Study 1 we demonstrated a signicant learning decit in patients with left, but not right, TLE, and they were further impaired in retention of the story despite having learned it to the same criterion as subjects with right TLE and healthy subjects. These decits remained conned to patients with left TLE after surgery. For clinical use we developed the SLAM in three versions in two languages; in studies 2 and 3 we tested and proved their equivalence. © 2011 Elsevier Inc. All rights reserved. 1. Introduction It has been known for many years that damage in the dominant temporal lobe results in verbal memory decits [e.g., 17]. Conse- quently, tests of verbal learning and memory are important components of neuropsychological test batteries that are used for determination of the site of seizure focus in patients who are candidates for surgical treatment of epilepsy. List learning tests are commonly used for this purpose, with a high degree of success in differentiating left from right temporal lobe dysfunction [e.g., 812]. However, to approximate more closely the demands of everyday life, we believe that memory for meaningful prose should also be tested. A number of tasks exist that test memory for stories, the most commonly used being the Logical Memory subtest (LM) of the Wechsler Memory Scale (WMS). The rst version of the WMS was published in 1945 [13], and it was followed by WMS-Revised [14], WMS-III [15], and WMS-IV [16]. The content of the LM test has undergone some changes over the course of the revisions of the WMS, but the format has changed very little: two stories are read aloud to the person being tested, who must repeat back each story immedi- ately after hearing it and again after a delay interval. One innovation was that in the WMS-III, the second story was read twice. In the most recent version, WMS-IV, the WMS-III stories were unchanged for ages 1669, but the second reading was dropped for consistency with previous editions, and a new, simpler story was introduced for the age range 6590. Although some authors have reported that the LM is sensitive to preoperative [17,18] and postoperative [1921] memory decits associated with left temporal lobe damage, many more have testied to the poor ability of the LM subtest to lateralize temporal lobe dysfunction in unoperated [2129] and operated [30,31] patients. Lacritz and colleagues [18] analyzed the effect of the additional presentation of the second story in the WMS-III battery. They found that healthy subjects and patients with either left or right temporal lobe epilepsy (TLE) all remembered the second story better than the rst, but the ability of this task to classify patients with left TLE correctly was modest (58%). We believe that an important reason why the WMS LM task is not able to differentiate better between left and right temporal lobe dysfunction is that the stories are presented only once or, exception- ally in the case of WMS-III, twice. Factors other than poor memory can play a role in failure to recall them well, such as being temporarily distracted by something (e.g., a sound, a thought) or misunderstand- ing some words or part of the story. Additional presentations should overcome this type of problem, allowing people who do not have a true memory decit to learn and remember the stories. Very few of the existing tests of memory for meaningful prose incorporate a learning component. The Adult Memory and Informa- tion Processing Battery [32] uses a trials-to-criterion paradigm and a delayed recall test. Blake and colleagues [23] compared patients with a left or right temporal lobe seizure focus and healthy control subjects Epilepsy & Behavior 20 (2011) 518523 Corresponding author at: Montreal Neurological Institute, 3801 University Street, Montreal, Quebec H3A 2B4, Canada. Fax: +1 514 398 1338. E-mail address: [email protected] (J. Djordjevic). 1525-5050/$ see front matter © 2011 Elsevier Inc. All rights reserved. doi:10.1016/j.yebeh.2011.01.002 Contents lists available at ScienceDirect Epilepsy & Behavior journal homepage: www.elsevier.com/locate/yebeh

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Epilepsy & Behavior 20 (2011) 518–523

Contents lists available at ScienceDirect

Epilepsy & Behavior

j ourna l homepage: www.e lsev ie r.com/ locate /yebeh

The Story Learning and Memory (SLAM) test: Equivalence of three forms andsensitivity to left temporal lobe dysfunction

Jelena Djordjevic a,⁎, Mary Lou Smith b, Viviane Sziklas a, Dominique Piper a,Sidonie Pénicaud a, Marilyn Jones-Gotman a

a McGill University, Montreal, Quebec, Canadab University of Toronto, Toronto, Ontario, Canada

⁎ Corresponding author at: Montreal Neurological InMontreal, Quebec H3A 2B4, Canada. Fax: +1 514 398 1

E-mail address: [email protected] (J. Djord

1525-5050/$ – see front matter © 2011 Elsevier Inc. Aldoi:10.1016/j.yebeh.2011.01.002

a b s t r a c t

a r t i c l e i n f o

Article history:Received 1 December 2010Revised 31 December 2010Accepted 4 January 2011Available online 26 February 2011

Keywords:Verbal learningMemoryStory recallTemporal lobe epilepsyNeuropsychology

Remembering meaningful information is an important component of verbal memory. However, findings fromexisting story memory tests have been mixed in patients with temporal lobe epilepsy (TLE). We developed atest, the Story Learning andMemory (SLAM) test, in which a story is presented repeatedly until a performancecriterion is reached, and verbatim recall is obtained only once, after a delay. In Study 1 we demonstrated asignificant learning deficit in patients with left, but not right, TLE, and they were further impaired in retentionof the story despite having learned it to the same criterion as subjects with right TLE and healthy subjects.These deficits remained confined to patients with left TLE after surgery. For clinical use we developed theSLAM in three versions in two languages; in studies 2 and 3 we tested and proved their equivalence.

stitute, 3801 University Street,338.jevic).

l rights reserved.

© 2011 Elsevier Inc. All rights reserved.

1. Introduction

It has been known for many years that damage in the dominanttemporal lobe results in verbal memory deficits [e.g., 1–7]. Conse-quently, tests of verbal learning and memory are importantcomponents of neuropsychological test batteries that are used fordetermination of the site of seizure focus in patients who arecandidates for surgical treatment of epilepsy. List learning tests arecommonly used for this purpose, with a high degree of success indifferentiating left from right temporal lobe dysfunction [e.g., 8–12].However, to approximate more closely the demands of everydaylife, we believe that memory for meaningful prose should also betested. A number of tasks exist that test memory for stories, the mostcommonly used being the Logical Memory subtest (LM) of theWechsler Memory Scale (WMS). The first version of the WMS waspublished in 1945 [13], and it was followed by WMS-Revised [14],WMS-III [15], and WMS-IV [16]. The content of the LM test hasundergone some changes over the course of the revisions of theWMS,but the format has changed very little: two stories are read aloud tothe person being tested, who must repeat back each story immedi-ately after hearing it and again after a delay interval. One innovationwas that in the WMS-III, the second story was read twice. In the mostrecent version, WMS-IV, theWMS-III stories were unchanged for ages

16–69, but the second reading was dropped for consistency withprevious editions, and a new, simpler story was introduced for the agerange 65–90.

Although some authors have reported that the LM is sensitive topreoperative [17,18] and postoperative [19–21] memory deficitsassociated with left temporal lobe damage, many more have testifiedto the poor ability of the LM subtest to lateralize temporal lobedysfunction in unoperated [21–29] and operated [30,31] patients.Lacritz and colleagues [18] analyzed the effect of the additionalpresentation of the second story in the WMS-III battery. They foundthat healthy subjects and patients with either left or right temporallobe epilepsy (TLE) all remembered the second story better than thefirst, but the ability of this task to classify patients with left TLEcorrectly was modest (58%).

We believe that an important reason why the WMS LM task is notable to differentiate better between left and right temporal lobedysfunction is that the stories are presented only once or, exception-ally in the case ofWMS-III, twice. Factors other than poor memory canplay a role in failure to recall them well, such as being temporarilydistracted by something (e.g., a sound, a thought) or misunderstand-ing some words or part of the story. Additional presentations shouldovercome this type of problem, allowing people who do not have atrue memory deficit to learn and remember the stories.

Very few of the existing tests of memory for meaningful proseincorporate a learning component. The Adult Memory and Informa-tion Processing Battery [32] uses a trials-to-criterion paradigm and adelayed recall test. Blake and colleagues [23] compared patients witha left or right temporal lobe seizure focus and healthy control subjects

519J. Djordjevic et al. / Epilepsy & Behavior 20 (2011) 518–523

on this task, using short and long delay intervals of 30 minutes and8 weeks. They found no difference between the groups on learning oron recall after 30 minutes, but the left temporal lobe group differedfrom the control group in recall after 8 weeks. The lack of any lefttemporal deficit except after an 8-week delay makes this test a poorchoice as a diagnostic tool in epilepsy.

A second story task that uses a learning paradigm is the HeatonMemory Test [33], in which a story is also read until a criterion isreached (or a maximum of five readings), and a delayed recall isobtained after 4 hours. The usefulness of this task in patients withepilepsy has not been evaluated.

A third storymemory task that tests learning as well as retention isa story learning test that was devised by Frisk and Milner [34]. It is alearning-to-criterion task using a selective reminding format [35]. Aninteresting aspect of this test is that learning is judged not by recall,but by responses to a set of questions about the story; recall isobtained only once, 20 minutes after the learning phase. Frisk andMilner tested healthy control subjects and patients who hadundergone surgical resection from the left or the right temporallobe and found that patients with resection from the left temporallobe were impaired in learning and in retention compared with thecontrol group.

We thought that the learning paradigm of Frisk and Milner's taskand its sensitivity to damage in the left temporal lobe made itpotentially a good clinical tool to be used for testing patients withepilepsy. However, it existed only in English and in only one form, andtheir results were obtained in operated patients. Two of us (M.L.S. andM.J.G.) devised an additional two stories patterned after the original,to be used when retesting is needed, and we translated all three intoFrench because the majority of our patients are francophones. Weextended the delay interval to 30 minutes and administered the testto unoperated patients with TLE to investigate its sensitivity to thesubtler dysfunction of an epileptic focus in the dominant temporallobe (Study 1).

In that initial studywe found that the task did indeed show specificsensitivity to left TLE and, furthermore, that surgical resectionexacerbated the deficit. However, we observed that the patientswith right TLE and healthy control subjects “improved” on retest,leading us to suspect that the different forms of the test were notequivalent. We carried out a second study (Study 2) to testequivalence of the three forms and found that they did differ onseveral measures. We followed that finding by making progressivechanges through a number of pilot studies, keeping structuralcomponents constant across versions, until equivalence was reachedamong the three forms in English and in French. In Study 3 weadministered the resulting tests to 126 healthy subjects (63anglophones and 63 francophones) to verify equivalence acrossforms and languages.

Table 1Summary information on subjects tested in Study 1.

Unoperated patientswith left temporallobe epilepsy

Unoperated patientswith right temporallobe epilepsy

Healthy controlsubjects

Number of subjects 46 (23)a 44 (23) 19 (16)Age (years) 33.5 36.8 30.2Education (years) 12.1 12.9 13.3Full Scale IQ 92.2 96.1 -Anglophones 37.8% 51.2% 100%Women 35.1% 67.6% 42.1%

a Numbers in subsets who had surgery (patients) or test–retest (HC) are given inparentheses.

2. Story Learning and Memory test: Task paradigm

The task paradigm was identical in all three studies except thatafter the first 38 patients, the length of the delay interval wasextended from 30 minutes to 24 hours to make the memory demandsmore comparable to those of everyday life. In the learning phase, thestory is read aloud to the subject, after which 10 questions are askedabout story content. The story is then read repeatedly, using aselective reminding technique, until all 10 questions have beenanswered correctly on two consecutive trials or until it has beenpresented for a maximum of 10 readings. A verbatim recall is obtainedjust once, after a delay. The measures analyzed are the number ofcorrect answers to the 10 questions on the first trial (T1); the numberof readings required, or Trials to Criterion (TTC); and a Delayed Recall(DR) score, which is a percentage of the number of units recalled outof the total number of units.

3. Study 1

3.1. Methods

3.1.1. SubjectsIn Study 1, the SLAM was used to examine verbal memory in

unoperated TLE patients with a left (LTLE, N=46)- or right (RTLE,N=44)-sided temporal-lobe focus, and their results were comparedwith those of a matched group of healthy control subjects (HC,N=19). The three groups did not differ with respect to age oreducation, and the two patient groups did not differ in Full Scale IQ(Table 1); pN0.05 in all three cases. A subset of patients underwentunilateral anterior resection from a temporal lobe (23 left and 23right) and were retested on an alternate form of the SLAM. A subset ofthe HC group (N=16) was also tested twice, using two differentforms of the test.

3.1.2. ProcedureBefore surgery, all patients were tested with Form 1 of the SLAM,

as were the healthy volunteers at first test. All retested subjects weregiven Form 2: patients were retested after surgery and controlsubjects were retested a minimum of 1 week after the first test. Test–retest intervals were not comparable between the patients andcontrol subjects for practical reasons: it is very difficult to bring backhealthy volunteers for retest after long intervals, and the testing ofpatients is tied to clinical constraints with respect to how long afterpreoperative evaluation the surgery takes place. Postoperative testingvaried between 3 months and 4 years and this was the case in bothgroups of patients. The learning phase of the test was administered tothe whole sample in the same way, and therefore, the results for thetwo learning measures are shown for the whole sample together.However, delayed recall was given in two ways: an earlier set of 38patients (19 LTLE and 19 RTLE) and all control subjects (N=19) weregiven the delayed recall test after an interval of 30 minutes, and theremaining 52 subjects (27 LTLE and 25 RTLE) had a 24-hour delayedrecall test. For that reason, we show the results for delayed recall bothcollapsing together results obtained with two delay intervals and foreach interval separately. Each subject was tested in their firstlanguage, which was either English or French.

3.2. Results

3.2.1. Effect of temporal lobe focus: Unoperated patientsTo examine verbal learning and memory in unoperated patients

with focal TLE, we conducted three one-way ANOVAs comparing theeffects of group (LTLE, RTLE, and HC) on the three test measures: twomeasures of learning, that is, performance on Trial 1 (T1) and numberof trials to reach criterion (TTC), and one measure of delayed recall(DR). The two measures of learning yielded comparable results: thegroup effect was significant for T1: F(2,106)=9.5, Pb0.001, and forTTC, F(2,106)=7.4, Pb0.01. Pairwise comparisons (LSD) revealedthat patients with LTLE had fewer correct answers on the first learning

520 J. Djordjevic et al. / Epilepsy & Behavior 20 (2011) 518–523

trial than did those with RTLE (Pb0.05) and healthy control subjects(Pb0.001), and they needed more learning trials to reach criterionthan did the RTLE (Pb0.01) and HC (Pb0.001) groups. Furthermore,the performance of patients with a right temporal focus was notdifferent from that of the healthy volunteers on either measure(PN0.05).

When the patients who had short- and long-delay intervals werecollapsed together, the group effect was significant for the delayedrecall measure (DR), F(2,106)=8.3, Pb0.001 (Fig. 1A). Post hoccomparisons revealed that the LTLE group had poorer delayed recallthan did the RTLE (Pb0.01) and HC (Pb0.001) groups. As with the twolearning measures, recall of the RTLE group was not different fromthat of the HC group (PN0.05). When only subjects who had a shortdelay (i.e., 30 minutes) were entered into the analysis, the effect ofgroup was marginally significant, F(2, 54)=2.6, P=0.08 (Fig. 1B).Importantly, patients with LTLE performed worse than healthycontrols (P=0.05) and those with RTLE (P=0.055), whereas recallof patients with RTLE did not differ at all from that of healthy controls(P=0.97) following a 30-minute interval. A similar pattern was seenwhen recall of the two patient groups who recalled the story after along delay (i.e., 24 hours) was analyzed: recall of the story wassignificantly lower in patients with LTLE than RTLE, t(50)=0.02(Fig. 1C).

3.2.2. Effect of temporal lobe surgery: Operated patientsWe next conducted three two-way repeated-measures ANOVAs to

examine the effects of group (LTLE, RTLE, and HC) and session (1 vs 2,which referred to before vs after surgery for patients, and to test vsretest for healthy volunteers) on the three measures (T1, TTC, andDR). For the number of correct answers on Trial 1, only the groupeffect was significant, F(2,59)=15.5, Pb0.001. Post hoc testsindicated that patients with LTLE were impaired before and after

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Fig. 1. Percentage delayed recall (DR) as a function of group (LTLE: patients with lefttemporal lobe epilepsy, RTLE: patients with right temporal lobe epilepsy, HC: healthycontrol group). Error bars show standard errors. Pb0.01. (A) Mean delayed recall scorefor the whole sample regardless of the delay interval. (B) Mean delayed recall score forsubjects who recalled the story after a short (30-minute) delay interval. (C) Meandelayed recall score for subjects who recalled the story after a long (24-hour) delayinterval.

surgery, compared with the RTLE (Pb0.001) and the HC (Pb0.001)groups. The effect of session was not significant, and neither was theinteraction between session and group, both PN0.05. Although theinteraction effect was not significant, we had predicted that the LTLEgroup's performance would deteriorate after surgery. We thusconducted planned comparisons, which showed a statistical tendencyfor the LTLE group to performworse after surgery (P=0.09), whereascomparisons for the two other groups across sessions did notapproach significance (P=0.55 for the RTLE and P=0.81 for the HCgroup).

The second learning measure, the number of trials to criterion(TTC), also showed only a significant group effect, F(2,59)=9.47,Pb0.001. Post hoc comparisons revealed that the LTLE group requiredmore trials to reach criterion than did the RTLE (Pb0.01) and HC(Pb0.001) groups. Again, the interaction effect was not significant, butplanned comparisons confirmed that performance on TTC wassignificantlyworse after surgery for the LTLE group (Pb0.05), whereascomparisons for the two other groups across sessions did notapproach significance.

The delayed recall measure (DR) showed a somewhat differentpattern of results (Fig. 2). All three effects were significant: group, F(2,59)=11.3, Pb0.001; session, F(1,59)=7.93, Pb0.01; and theinteraction between group and session, F(2,59)=3.63, Pb0.01. Posthoc tests conducted on the interaction effect revealed that the RTLE(Pb0.01) and HC (Pb0.01) groups both improved on retest, whereasthe LTLE group did not change (PN0.05).

4. Study 2

The results of Study 1 were very promising, as they showed theSLAM to be sensitive to LTLE as well as to the effects of resection fromthe left temporal lobe. The unexpected finding was that the patientswith RTLE and healthy control subjects had better recall on the secondadministration of the SLAM. Because Form 1 was given to all subjectsat first test and Form 2 at second test, we suspected that the differentforms may not be equivalent in difficulty. To test this hypothesis, weadministered the three forms of the SLAM to three groups ofuniversity students (one form per group), whose performance wasexpected not to differ if the three test forms were equivalent.

4.1. Methods

4.1.1. SubjectsWe recruited 72 university students and assigned them at random

to one of three groups according to the form of the test administered:Form 1 (N=28, 11 women, mean age=21.2 years), Form 2 (N=24,

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Fig. 2. Percentage delayed recall (DR) as a function of session [(1) before surgery forpatients and first test for the HC group, (2) after surgery for patients and retest for theHC group)] and group (LTLE: patients with left temporal lobe epilepsy, RTLE: patientswith right temporal lobe epilepsy, HC: healthy control group). Error bars represent SE.

521J. Djordjevic et al. / Epilepsy & Behavior 20 (2011) 518–523

12 women, mean age=22.6 years), and Form 3 (N=20, 12 women,mean age=20.3 years). Mean age did not differ among these threegroups, F(2,69)=1.97, PN0.05. All subjects were anglophones.

4.1.2. ProcedureThe SLAM was administered in the same way as described above

and used a 30-minute interval for delayed recall.

4.2. Results

Three one-way ANOVAs were conducted to examine the effect ofform (1, 2, and 3) on the two learning and one retention measures.The form effect was significant for the number of correct answers onT1: F(2,69)=4.795, Pb0.05. Post-hoc tests indicated that perfor-mance on T1 was inferior in the groups tested on Forms 1 and 2 incomparison with that of the group tested on Form 3 (both Pb0.05),suggesting that Forms 1 and 2 were more difficult than Form 3 on thismeasure.

The effect of the test form was also significant when trials to reachcriterion (TTC) was analyzed: F(2,69)=3.682, Pb0.05. Post-hoc testsrevealed that Form 1 was more difficult than Form 3, Pb0.05.

The effect of test form was also significant for delayed recall (DR):F(2,69)=7.14, Pb .01, Fig. 3; Form 1 was more difficult than Forms 2and 3, both Pb0.05.

5. Test modifications

Study Two confirmed that the three forms of the SLAM notequivalent in difficulty. For that reason, we decided to revise the teststo match the three forms to one another in difficulty, and toaccomplish equivalence also in the English and French versions. Tothis end, we conducted several pilot studies. First we analyzed,retrospectively, the details of data from 60 healthy volunteers and 62patients (28 left temporal and 34 right temporal) on the three originalforms of the SLAM. To estimate the level of difficulty of each scoreditem, we ordered the scoring units recalled by the healthy volunteersaccording to frequency of recall. We then modified the stories suchthat the proportions of easier, average and difficult items were keptconstant across the three forms and two languages. In addition, weanalyzed the frequency of recall of individual scoring units in the datafrom patients. Items that were less sensitive to left temporal damagewere replaced. The content of Form 3, shown to be easier than theother two forms on all three measures, was completely changed andmodelledmore closely to Forms 1 and 2. Finally, an effort wasmade tokeep parts of speech (e.g., numbers of verbs, adjectives, nouns andadverbs) and the total number of words constant across the threeforms and two languages.

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Fig. 3. Percentage delayed recall (DR) as a function of story form (1, 2, and 3) in healthyvolunteers. Error bars represent SE. *Pb0.05.

6. Study 3

In Study Three, the revised test was administered to 126 healthyvolunteers with the aim to examine the difficulty level of the threerevised forms and to compare the English to the French versions.

6.1. Methods

6.1.1. SubjectsThe subjects were 126 healthy volunteers (86 women), all

undergraduate students: one half of the sample was anglophoneand the other half was francophone, Table 2. Within each language,subjects were assigned randomly to one of the three forms of the test.Their nonverbal reasoning, measured with the Matrix Reasoning test,did not differ: the effects of language, test form, and their interactionwere not significant on the Matrix Reasoning scores (in all casesPN0.05).

6.1.2. ProcedureAdministration of the SLAM was the same as described above.

6.2. Results

A two-way ANOVA comparing the mean number of correctresponses on thefirst trial (T1) across the three forms and two languagesshowed no significant effects of language, F(1,120)=0.9, PN0.05, orform, F(2, 120)=2.2, PN0.05, or their interaction, F(2, 120)=0.5,PN0.05.

Similarly, a two-way ANOVA comparing the mean number of trialsrequired to learn the story to criterion (TTC) across forms and languagesshowed no significant effects of language, F(1, 120)=0.1, PN0.05,or form, F(2,120)=1.9, PN0.05, or their interaction, F(2,120)=1.1,PN0.05.

Finally, a two-way ANOVA comparing the mean percentagescores for delayed recall (DR) across forms and languages showed asignificant effect of language, F(1,120)=8.6, Pb0.01, the Frenchscores being slightly lower than English scores, and no effect of form,F(2,120)=1.9, PN0.05 or interaction, F(2,120)=0.1, PN0.05, Fig. 4.

7. Discussion

Study 1 showed the SLAM test to be an excellent neuropsycho-logical instrument for use in pre- and post-operative evaluation ofpatients with epilepsy. We showed that it has the potential tolateralize temporal lobe dysfunction in patients with unilateraltemporal lobe epilepsy: not only was it able to capture verbalmemory deficits that occur after resection from a left temporal lobe,but it was also able to discriminate between a left- and a right-sidedfocus in unoperated patients. The performance of patients with a lefttemporal lobe focus was significantly worse than that of patients witha right temporal lobe focus on both of the two learning measures andon retention. This was the case both when the interval betweenlearning and delayed recall was short (30 minutes) and when it waslong (24 hours). Further, the right temporal lobe group did not differfrom the healthy control subjects on any measure. This finding speaksagain to the specificity of the deficit elicited by the SLAM test.

Table 2Summary information on subjects tested in Study 3.

Study 1 Study 2 Study 3

Number of subjects 42 42 42Age (years) 23.3 23 22Matrix Reasoning Score 107.2 110.1 109.1Anglophones 50% 50% 50%Women 69% 64.3% 66.7%

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Fig. 4. Percentage delayed recall (DR) as a function of story form (1, 2, and 3) andlanguage (English, French) in healthy volunteers. Error bars represent SE.

522 J. Djordjevic et al. / Epilepsy & Behavior 20 (2011) 518–523

The results using the SLAM are even more encouraging in thecontext of other existing story memory tests, which in most casesinclude one or at best two presentations followed by immediate anddelayed recall. Among these, the logical memory subtest of theWechsler Memory Scales is by far most often used in generalneuropsychological practice and also in specialized evaluation ofpatients with epilepsy. Although findings on the logical memorysubtest have been mixed, a majority of studies have clearly shownthat it cannot discriminate reliably among patients with epilepsy whounderwent excisions from a left versus right temporal lobe [30,31],and particularly not in unoperated patients [21–23,25–27,29,36,37].Specifically with respect to the WMS-III, mixed findings have alsobeen reported in that some studies found the logical memory subtestto discriminate between left and right temporal lobe damage [17,19],whereas others reported that this subtest was not clinically useful insuch discriminations [26,27].

The SLAM test described in this article has two main advantagesover other existing tests that measure memory for prose passages.First, the SLAM uses a learning paradigm. Consequently, in addition toproviding a measure of retention/recall, it provides two measures oflearning: number of correct answers on the first trial and number oftrials needed to learn the story to criterion. We showed that both ofthese measures were sensitive to left-sided temporal lobe damage inunoperated and operated patients. In contrast to our findings, oneother study using a story learning paradigm [23] failed to show adifference between unoperated patients with left temporal lobedamage and those with right temporal lobe damage on their learningmeasures, which were the first three learning trials and trials tocriterion. An important difference existed in task paradigm. Blake etal. tested recall on every learning trial (free recall), whereas in theSLAM, recall was tested only once, after a delay, and instead, subjectswere asked questions about the story during learning (selectivereminding procedure). It could be that the selective remindingprocedure, unlike verbatim free recall, promotes acquisition of therequired amount of information in a uniform way, thus helpingsubjects to attain a definable level of acquisition. This facilitateslearning in those able to benefit from cuing, whereas free recall doesnot provide any support and might not distinguish those with truelearning difficulties from those with learning difficulties resultingfrom other problems. Finally, another possible reason for thisdiscrepancy may be sample size: the study by Blake et al. had asmall sample size compared with our sample of 90 unoperatedpatients (46 with LTLE vs 44 with RTLE).

A second advantage of the SLAM over most existing story memorytests is that the learning paradigm and the requirement that subjectsreach a specific criterion level of learning allow a better estimate ofretention because all subjects reach a similar level of initial acquisitionbefore retention is measured. In SLAM, if criterion has not been

achieved the material will have been presented 10 times. Such aprocedure ensures sufficient exposure to the material and reduces thelikelihood that fluctuating attention, temporary distraction, orreduced comprehension can confound the retention outcome.Therefore, the delayed recall measure is more likely to reveal a trueretention deficit than will a similar measure on a test where the storyhas been presented only once. Lacritz et al. [18] found that thevariability of story retention scores was greater for a story presentedjust once (A) than for a story read twice (B). Furthermore, whereas onStory A some proportion of all three of their groups (LTLE, RTLE, andhealthy volunteers) had suboptimal recall, defined as less than 50%retention [18], only the LTLE group displayed suboptimal recall onStory B. These qualitative aspects of performance on the logicalmemory subtest of WMS-III are consistent with our claim that alearning paradigm permits better capture of retention deficits inpatients with LTLE.

In the early phase of the SLAM test, we used a short (30-minute)delay interval to obtain recall of the story. Later we changed to alonger (24-hour) delay interval for clinical purposes. Although weprefer longer delay intervals in our clinical practice, our results showthat the SLAM test is clinically useful alsowith the short delay interval.

We had expected the preexisting impairments in patients with aleft temporal lobe focus to be exacerbated after surgery, and this wasthe case for the two learning measures, whereas performance of theother two groups remained unchanged—after surgery in the case ofthe RTLE group and at retest in the case of healthy volunteers. Incontrast, the retention measure showed that patients with a lefttemporal lobe focus earned similar scores after surgery as before,whereas the HC group and patients with a right temporal lobe focusearned significantly higher scores in second testing. We did notanticipate this improvement, as significant practice effects should beunlikely given that different stories were used in retest. In fact,Benedict and Zgaljardic [38] showed that verbal memory wasresistant to practice effects when alternate test forms were usedover four sessions. The failure of the LTLE group to show apostoperative decrement on verbatim delayed recall was alsosurprising given that their results on the learning measures were inkeeping with postoperative memory loss. As all subjects had beengiven Form 1 of the story first and Form 2 second, we hypothesizedthat insufficiently matched story formsmay have caused the observedpattern in the recall scores on second testing. However, it is importantto note that the LTLE group was not able to benefit from thedifferences between stories as had the RTLE and HC groups, againconfirming the sensitivity of the story learning procedure to the verbalmemory deficits associated with dysfunction in the left temporal lobe.

To examine the possibility that the story forms were indeed notequal in difficulty, we conducted the second study, in which the threedifferent forms of the SLAMwere tested in university students, so thatperformance differences should be unlikely unless the three forms ofthe test differed in difficulty level. We found differences on all threeperformance measures, leading us to conclude that our existing formsof the SLAMwere not equivalent and, in particular, that Forms 2 and 3were easier than Form 1.

On the basis of this finding, we made important revisions to Forms2 and 3 in the texts, the questions, and the scoring rules for verbatimrecall. Very few changes were made to Form 1 as it was used as themodel to which we attempted to match Forms 2 and 3. The results ofStudy 3 showed that the three forms of the stories yielded comparableresults in healthy volunteers on all three performance measures. Oneimplication of these findings is that the three forms can be used inrepeated evaluations of patients without the concern of memorysavings from one evaluation to another. Importantly, results obtainedon the different forms can be compared directly, as we showed thatthey do not differ in difficulty: losses or gains in scores on retestshould reflect changes within the patient and not in the test formsused. However, we did not succeed in matching the English and

523J. Djordjevic et al. / Epilepsy & Behavior 20 (2011) 518–523

French versions to each other completely, as we found slight butsignificantly lower delayed recall scores for the French tests. This wasdespite the fact that the groups of anglophone and francophonesubjects were matched for age, education, and nonverbal reasoning.This finding of a French translation yielding lower scores than itsEnglish counterpart is consistent with some of our previous findings.We showed lower scores in francophones than in anglophones on twodifferent naming tests: the Boston Naming Test and the AuditoryNaming Test [39]. Similarly, we showed that francophone studentsperform slightly but significantly less well on the French version of alist learning test, the Rey Auditory Learning Test, than do anglophonestudents on the English version [40]. These two groups of subjects didnot differ on a figure learning test, showing that the difference lay inimperfect correspondence between the English and French versions ofthe verbal memory tests and not in differences between the subjectgroups.

In summary, we have shown the SLAM to be a potentially valuabletool in neuropsychological evaluation of patients with focal epilepsy,as it revealed deficits on three measures in patients with left temporallobe dysfunction, whether owing to an epileptic focus alone or tosurgical resection of the focus, while patients with right temporal lobedysfunction were unimpaired. We have also demonstrated equiva-lence of our revised three forms of the SLAM in English and of therevised three forms in French, with near equivalence of the Englishand French versions. The SLAM is thus suitable for the repeatedevaluations so frequently needed in postoperative follow-up ofpatients with epilepsy and also in other clinical applications [e.g.,41] where repeated testing may be indicated.

Acknowledgments

We are grateful to Dr. Virginia Frisk for her assistance indeveloping the stories used in Studies 1 and 2, and to NathalieRouthier and Maria Fraraccio for help in testing subjects. This workwas funded by Operating GrantMOP 53274 awarded toM.J.G. and V.S.by the Canadian Institutes of Health Research.

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