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Brain and Language 102 (2007) 13–21

Verbal memory compensation: Application to left and righttemporal lobe epileptic patients

Christel Bresson a,*, Veronique Lespinet-Najib a, Alain Rougier b,Bernard Claverie a, Bernard N’Kaoua a

a Laboratoire de Sciences Cognitives (UPRES – EA-487), Institut de Cognitique, Universite Victor Segalen Bordeaux 2,

Domaine Universitaire de Carreire, Zone Nord, Bat. 2A 146 Rue Leo Saignat, 33076 Bordeaux cedex, Franceb Laboratoire d’Epileptologie Experimentale et Clinique (EA 2967), Universite Victor Segalen Bordeaux 2, Domaine Universitaire de Carreire,

Boıte 78 146 Rue Leo Saignat, 33076 Bordeaux cedex, France

Accepted 2 June 2006Available online 12 July 2006

Abstract

This study investigates the compensatory impact of cognitive aids on left and right temporal lobe epileptic patients suffering fromverbal memory disorders, who were candidates for surgery. Cognitive aids are defined in the levels-of-processing framework and dealwith the depth of encoding, the elaboration of information, and the use of retrieval cues. Results indicate differential compensatoryimpact for left and right epileptic patients and are discussed according to the HERA model and the compensation framework.� 2006 Elsevier Inc. All rights reserved.

Keywords: Cognitive compensation; Verbal memory; Temporal lobe epilepsy; Hemispheric specialization; Levels-of-processing

1. Introduction

Temporal lobe epilepsy is the most important focal epi-lepsy due to its high prevalence, drug resistance, and com-monly disabling effects on memory functions (Engel, 1996).Seizures concern hippocampal and parahippocampal struc-tures, which mediate declarative memory (Cohen & Squire,1980; Eichenbaum, 2001; Nadel & Moscovitch, 2001).Thus, poor memory is a primary complaint of patients withtemporal lobe epilepsy (TLE). Indeed, a large body of liter-ature is devoted to memory impairment in TLE and studieshave frequently focused on the potential differences thatoccur when seizures are generated from left versus righttemporal lobe (Andersson-Roswall, Engman, Samuelsson,Sjoberg-Larsson, & Malmgren, 2004; Griffith, Pyzalski,Seidenberg, & Hermann, 2004; Helmstaedter, 2002;Reminger et al., 2004; Schwarcz & Witter, 2002).

0093-934X/$ - see front matter � 2006 Elsevier Inc. All rights reserved.

doi:10.1016/j.bandl.2006.06.005

* Corresponding author. Fax: +33 0 5 57 57 46 07.E-mail address: [email protected] (C. Bresson).

One way of approaching memory deficits is the levels-of-processing framework (LOP) developed by Craik &Lockhart in 1972. In this framework, the durability anddistinctiveness of memory traces are direct functions ofthe nature and quality of the encoding operations. Depthof processing is seen as a processing continuum from shal-low (sensory) to deep (semantic) processes, with some typesof processing (typically sensory analyses) preceding others(typically conceptual analyses). So, the deeper the initialprocessing, the better subsequent memory performance isexpected to be. To complete this theoretical approach(Lockhart & Craik, 1990), two other main concepts havebeen added: elaboration and encoding specificity. There-fore, memory performance depends upon three dimen-sions, depth of processing, elaboration, and encodingspecificity (kind of retrieval) of the information operativeat the two memory stages, encoding and retrieval.

The first dimension in the LOP theory, ‘‘depth of pro-cessing’’, states that deeper processing is associated withhigher levels of subsequent remembering. Encoding infor-mation at a shallow level (e.g., phonetic) leads to worse

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14 C. Bresson et al. / Brain and Language 102 (2007) 13–21

performance than encoding information at a deeper level(e.g., semantic). For example, memorizing ‘‘brain, train,rain’’ leads to worse performances than memorizing ‘‘bear,horse, dog.’’ These results have been obtained in numerousexperiments with healthy subjects (e.g., Bentin, Moscov-itch, & Nirhod, 1998; Craik & Tulving, 1975; Fujii et al.,2002) and are explained by the fact that encoding semanticinformation activates semantic associates in memory thatare more efficient for the retrieval of information than lessmeaningful phonetic associates.

The second dimension, ‘‘elaboration,’’ demonstrated byCraik and Tulving (1975), states that an elaborated memo-ry trace is remembered more readily. Information is ‘‘elab-orated’’ by paying attention to the specific meaning i.e., thesemantic aspect of associated information (Symons &Johnson, 1997). The richness or extensiveness of processing(Lockhart, Craik, & Jacoby, 1976) makes it possible toretrieve elaborated information via several pathways (Ein-stein & Hunt, 1980; Lockhart et al., 1976). Among theways to handle elaboration, the self-reference effect (Kuiper& Rogers, 1979; Maki & McCaul, 1985; Rogers, Kuiper, &Kirker, 1977) describes the fact that asking the subject ifthe word describes him/her produces a better memorytrace. In addition, the ‘‘self-generated cuing’’ paradigm,introduced by Mantyla and Nilsson (1983), involves thesubject in elaborating the information to be memorizedby making him/her producing the cue to be matched withthe information.

Finally, the third dimension concerns the retrieval stageand refers to encoding specificity (Tulving & Thomson,1973). Given a specific type of encoding, retrieval is opti-mized when the retrieval test is designed to utilize the sametype of information (Fisher & Craik, 1977; Marmurek,1995). So, cued recall or recognition provides better retriev-al performance than free recall, with no context.

These three dimensions derived from the levels-of-pro-cessing theory can be studied together to determine theimpact of their interaction on memory performance.Interaction between depth of processing and encodingspecificity shows that retrieval (cued recall) is more effec-tive for a deep encoding than for a shallow encoding(Fisher & Craik, 1977). Secondly, interaction betweenelaboration and encoding specificity has been observed.Mantyla and Nilsson (1988) demonstrated that self-gener-ated cueing is much more effective in cued than free recall.This indicates that elaboration improves the efficiency ofencoding specificity. Thus, interaction between depth ofprocessing and elaboration demonstrated that depth wasboosted by elaboration. The superiority of semantic overphonetic encoding is enhanced by elaboration. Finally,the triple interaction has been obtained. Indeed a contex-tualized recall of an elaborated and deeply processedinformation results in better performance (Mantyla &Nilsson, 1988).

In the levels-of-processing theory, the three dimensionscould be seen as aids that enhance performance and socould be proposed to compensate cognitive deficits.

As TLE patients’ main complaint concerns their mem-ory deficits, the mismatch between their memory skillsand the demands of everyday life (Fisher et al., 2000;Guerreiro, Jones-Gotman, Andermann, Bastos, & Cen-des, 2001; Smith, 1989), these patients are candidatesfor compensation studies to assess the positive impactof the three LOP dimensions (seen as compensation aids)on performance.

In the epileptic research field, some studies have shownthat a deficit in memorizing information at a shallow leveldisappears when patients are helped by deep processing ofinformation, although authors do not agree on the rela-tionship between deficits and laterality of the foci (Helms-taedter & Kurthen, 2001). For some, this compensatoryimpact of depth of processing is observed only in left tem-poral lobe epileptic (L-TLE) (Helmstaedter, Gleissner, DiPerna, & Elger, 1997; Jokeit, Okujava, & Woermann,2001) or right temporal lobe epileptic (R-TLE) patients(Christianson, Nilsson, Saisa, & Silfvenius, 1992; Mungas,Ehlers, Walton, & McCutchen, 1985). Finally, some worksdo not find any impact of depth of processing, irrespectiveof the laterality of the epileptic foci (Gleissner & Elger,2001; N’Kaoua, Lespinet, Barsse, Rougier, & Claverie,2001; Troster et al., 1995). Furthermore, it could be notedthat in patients who suffer from a Korsakoff syndrome,authors have not found benefits from deep processingwhereas patients’ performance levels after shallow process-ing were nearly normal (Cermak, 1979; Cermak, Reale, &Baker, 1978).

Few studies have investigated elaboration. In a memori-zation task using self-generated cueing, Lespinet-Najibet al. (2004) demonstrated that elaboration did not helpL-TLE patients in phonetic (shallow) or semantic (deep)processing. On the contrary, the R-TLE group benefitedfrom elaboration in phonetic processing, as well as insemantic processing.

The third dimension, ‘‘retrieval’’, was tested by compar-ing free and cued, or coping recall. Numerous authors haveused this paradigm (Christianson, Silfvenius, & Nilsson,1987, 1989; Savage, Saling, Davis, & Berkovic, 2002).Mungas et al. (1985) found that cued recall only had animpact in L-TLE patients after deep processing. Accordingto Lespinet-Najib and collaborators (2004) L-TLE patientsdid not benefit from cued recall in deep processing, whereasR-TLE patients did. These findings indicate that the inter-action between depth of processing and retrieval does notprovide cognitive aid in left TLE, whereas it does in rightTLE.

Although verbal memory deficits have been widely stud-ied, there is no consensus as to the profile of left and righttemporal lobe epileptic patients’ memory disorders or thecompensatory power of cognitive aids, which is crucialfrom a rehabilitation perspective. While individual cogni-tive aids may be useful, the impact of their interaction isof real interest. We therefore studied the impact of eachdimension of the LOP theory and examined how theirinteractions potentiated performance. In our approach,

C. Bresson et al. / Brain and Language 102 (2007) 13–21 15

three compensation outcomes were identified by comparingperformance of left- and right-TLE patients to healthy sub-jects. In a ‘‘no compensation outcome,’’ healthy subjectsimproved their performance when at least one aid wasused, whereas the TLE groups did not. In a ‘‘partial com-pensation outcome,’’ the TLE groups improved their per-formance using the aid, but did not achieve the sameperformance as healthy subjects. Finally, in a ‘‘full com-pensation outcome,’’ the TLE groups achieved the sameperformance level as healthy subjects when the aid wasprovided.

The aim of our study is to investigate the compensationeffect of the three cognitive aids, separately and in interac-tion, on L- and R-TLE patients.

2. Materials and methods

2.1. Participants

Thirty patients with intractable partial epilepsy due totemporal lobe epilepsy, who had been referred for evalua-tion for epilepsy surgery, were included in this study. Four-teen patients suffered from left temporal lobe epilepsy and16 from right temporal lobe epilepsy. Seizure origin in allpatients retained for analysis was assessed by standard pre-operative diagnostic procedures, including videotape/elec-troencephalographic monitoring and MRI. Both groupswere right handed and matched for gender, current age,age at seizure onset, seizure frequency, seizure duration,number of antiepileptic drugs (AEDs), and educationallevel. A normal control group (NC) consisted of sixteenpersons matched with the TLE groups for age, educationallevel, and gender.

As medication and epilepsy can reduce processing speed(Shulman & Barr, 2002), patients completed standard pre-

Table 1Group characteristics

Parameters L-TLE (n = 14)

Age, in years M (SD) 31 (13)Number of male/female 4/10Educational level, in years M (SD) 11 (3)Age of seizure onset, in years M (SD) 13 (12)Epilepsy duration, in years M (SD) 18 (12)

Seizure frequency per monthUnder 5 55–10 5Over 10 4

No. of AEDsa, M (SD) 2.6 (0.9)‘‘Coding’’ subtestbM (SD) 53.1 (15.4)TMT AcM (SD) 32.3 (18.4)TMT BcM (SD) 75.7 (40.5)Logical Memory IdM (SD) 39.1 (14.7)Logical Memory IIdM (SD) 23.8 (16.6)

a Antiepileptic drug.b Scores.c Times in seconds.d Percent of recall.

operative neuropsychological testing: the ‘‘Coding’’(WAIS-R subtest, Wechsler, 2000) and Trail Making Test(TMT), A and B (Reitan & Wolfson, 1985). Finally, theWechsler memory Scale-III (WMS-III) verbal subtests‘‘Logical Memory I’’ (short-term verbal memory) and‘‘Logical Memory II’’ (long-term verbal memory) (Wechs-ler, 1997, 2001) were performed by the three groups inorder to determine the verbal memory deficits of the L-and R-TLE patients in comparison to normal controlgroup. (Demographic and clinical and neuropsychologicalcharacteristics of the groups are summarized in Table 1).

2.1.1. Demographic characteristics

There was no difference between the three groups interms of ‘‘age’’ [F(2, 43) = 0.4; p > .05] and ‘‘educationallevel’’ [F(2, 43) = 1.1; p > .05].

2.1.2. Clinical characteristics

L-TLE and R-TLE groups did not differ in terms of‘‘seizure frequency’’ [v2 = 0.4; p > .05], ‘‘age at seizureonset’’ [t = �0.5; p > .05], ‘‘seizure duration’’ [t = �0.2;p > .05], or number of AEDs [t = �0.3; p > .05] (Table 1).

2.1.3. Neuropsychological characteristics

There was no difference between the two groups ofpatients in terms of processing speed: ‘‘Coding’’ [t = 0.8p > .05], TMT A [t = �0.8; p > .05], or TMT B [t = �1.1;p > .05]. Concerning the Wechsler memory Scale, a two-way (Groups * Logical Memory) analysis of variance(ANOVA), with repeated measures for the last factor,was used to assess verbal memory deficits in the two groupsof patients. The ANOVA revealed single effects. Groups

effect [F(2,43) = 20.7; p 6 .0001]: patients are impaired incomparison to NC group as revealed by the Fisher posthoc analysis [p 6 .0001]. Logical Memory effect

R-TLE (n = 16) NC (n = 16)

35 (10) 32 (10)9/7 10/612 (2) 12 (2)15 (11)19 (14)

745

2.7 (0.8)48.2 (17.1)37.7 (16.9)95.8 (56.1)44.5 (16.8) 67.5 (13.4)36.8 (17.6) 63.6 (13.1)


[F(1,43) = 86.5; p 6 .0001]: Logical Memory I (short termmemory) is better performed than Logical Memory II (longterm memory). Finally interaction between Groups and

Logical Memory is shown [F(2,43) = 11.8; p 6 .0001]. ForLogical Memory I, L-, and R-TLE patients performedworth than NC group. For Logical Memory II, L-TLEperformed worth than R-TLE patients who performedworth than NC group.

2.2. Apparatus

Four lists were developed. Two lists required shallowprocessing (phonetic lists) and the two other, deep pro-cessing (semantic lists). For each level of processingone list is constituted of word pairs and the other listof single words. The word pairs list (target–cue) corre-sponds to the experimenter provided cue condition(named E-provided condition) that enables low elabora-tion, the cue is given to the subject by the experimenter.The single words list corresponds to the subject pro-duced cue condition (named S-produced condition) thatenables deep elaboration because the subject produceshis cue.

For phonetic processing:

• One list consisted of 16 isolated words (self-generatedcueing condition) to enable the subject to produce therhyme cue (e.g., Brain–subject produced cue);

• One list consisted of 16 ‘‘target–cue’’ rhyming-pairs,ending with 16 different phonemes (e.g., Brain–Train).

For semantic processing:

• One list consisted of 16 isolated words (self-generatedcueing condition) to enable the subject to produce thesemantic cue (e.g., Brain–subject produced cue);

• One list is of 16 ‘‘target–cue’’ pairs representing exam-ples of different categories coupled with the categoryper se. (e.g., Brain–Head).

The presentation order of each list was counterbalancedby subject.

The verbal stimuli were drawn from the Brulex database(Content, Mousty, & Radeau, 1990), their lexical frequencymean was 1885 occurrences per 100,000,000. Stimuli con-creteness was evaluated in a preliminary study, in whichstudents had to score 96 words on a seven-point scale(mean = 5.8 ± 0.8).

2.3. Procedure

Each subject had to memorize the four word-lists, one ata time. At the encoding stage, words were presented orallyat the rate of one word every 5 s. For each word, either theexperimenter (E-provided condition) or the subject (S-pro-duced condition) gave the cue. At the retrieval stage a freerecall was followed by a cued recall, where the experiment-

er gave the imposed or produced cue to enable the subjectto retrieve the target.

3. Results

A four-way (Groups * Depth of processing * Elabora-tion * Retrieval) analysis of variance (ANOVA), withrepeated measures for all factors except Groups, was usedto compare the total scores.

The single effects, partial interactions, and four-wayinteraction revealed by the ANOVA are presented below.

The data showed the single effect of each of the threedimensions: Depth of processing [F(1,43) = 288.9;p 6 .0001]; Elaboration [F(1,43) = 20.2; p 6 .0001]; andRetrieval [F(1,43) = 152.4; p 6 .0001]. These results indi-cated respectively enhanced performances for semanticprocessing (48.7 ± 23.9) in comparison to phonetic one(25.3 ± 17.1), for elaborated information (41.5 ± 25.8) incomparison to non elaborated one (32.5 ± 20.9), and forcued recall (45.2 ± 28.1) in comparison to free recall(28.8 ± 14.7). These results are irrespective of the group.The ANOVA also revealed a Groups effect[F(2,43) = 11.3; p 6 .001], where left (31.1 ± 21.7) andright (33.1 ± 22.4) epileptic patients had lower perfor-mance scores than normal control subjects (46 ± 24.6), asrevealed by the Fisher post hoc analysis [p 6 .005].

Results also showed two-by-two interactions betweenthe aids: Depth of processing and Elaboration: [F(1,43) =6.7; p 6 .01]; Depth of processing and Retrieval:[F(1,43) = 107.8; p < .0001]; Elaboration and Retrieval:[F(1,43) = 22.5; p 6 .0001]. Adding an aid in a situationwhere another aid was already present enhanced perfor-mance. Elaboration had much more effect on deep process-ing than on shallow one. Cued recall enhancedperformance for deep processing in comparison to shallowprocessing and also for elaborated processing relative toless elaborated. In addition, the triple interaction betweenthe aids is observed. Each group benefited from the interac-tions of all three aids: Depth of processing, Elaboration and

Retrieval: [F(1,43) = 5.2; p 6 .05]. Cued recall of semantic(deep processing) and elaborated information induced thebest performance.

Concerning Groups, first an interaction Groups byRetrieval and second the four-way interaction betweenthe three aids and groups were observed.

The two-way interaction Groups by Retrieval[F(2,43) = 9.4; p 6 .001] revealed that the NC and R-TLE groups’ enhanced cued recall performance (conditionwith an aid) in comparison to free recall, although bothgroups of patients were still impaired in comparison tothe NC group.

The four-way interaction Groups, Depth of processing,Elaboration and Retrieval [F(2,43) = 3.3; p 6 .05] showedthat the interaction between the three aids was differentin the three groups and could be interpreted as below.Graph 1 presents means of performance for the four-way interaction which are enumerated in Table 2. Finally,

0

20

40

60

80

100

E-provided

S-produced

E-provided

S-produced

E-provided

S-produced

E-provided

S-produced

Shallow Deep Shallow Deep

Free recall Cued recall

NC

L-TLE

R-TLE

% of recall

Graph 1. Means of performance for the three groups.


we collapse the results and the differences of the threevariables between their two modalities in Table 3. Todo so, mean of the four conditions that implicate eachvariable (two conditions by modality) have beencalculated.

For the phonetic processing the L-TLE patients did notenhance performance whatever the aid whereas R-TLEpatients improved performance when information iselaborated.

For a semantic processing in an E-provided conditionand free recall task, the L-TLE patients were better thanR-TLE. Moreover, all the groups achieved better perfor-mance when the three aids were given, but the two groupsof patients did not match NC performance (compensationwas partial).

Finally, Table 3 shows that L-TLE patients benefit glob-ally from deep processing whereas R-TLE patients enhanceperformance in cued recall conditions.

Table 2Means and standard deviations for the four-way interaction

Shallow processing (phonetic)

E-provided S-produced

Free recall Cued recall Free recall Cued reca

L-TLE 18.7 21 19.2 15.6M (SD) (16) (14) (8.3) (14.2)R-TLE 18 17.2 24.2 27.7M (SD) (11) (11.9) (12) (20.5)NC 29.7 32 29.7 46.8M (SD) (15.7) (15.4) (14) (23.3)

Table 3Differences between means of performances for the three LOP dimensions

Depth Elaboration

Shallow Deep Difference E-provided S-pro

NC 35 58 23 40 52L-TLE 19 44 25 29 34R-TLE 22 45 23 28 38

4. Discussion

When somebody suffers from a disease, the first step isto define and quantify the disorder and, second, to deter-mine how to cure the disease or minimize its effects. Anal-ysis of the literature on temporal lobe epilepsy and memoryshowed that many experiments had investigated the extentof verbal memory deficits but very few had explored waysof reducing them (Engelberts et al., 2002). The aim of ourstudy was to introduce a compensatory approach by pre-senting cognitive aids to epileptic patients, in order toinvestigate a possible alleviation of their memory disorders.

The term ‘‘compensation’’ is used in a wide range ofstudies concerning neuronal plasticity and/or agingresearch (e.g., Becker et al., 1996; Helmstaedter & Elger,1998). In our work, ‘‘compensation’’ refers to a psycholog-ical framework developed by Backman and Dixon (Back-man, 1985; Backman & Dixon, 1992), and is defined as a

Deep processing (semantic)

E-provided S-produced

ll Free recall Cued recall Free recall Cued recall

32.1 42.4 35.3 64.3(15.4) (24) (7.9) (19.6)26.6 51.5 33.2 66.8

(15.5) (22.8) (9.6) (17.6)34.4 64.1 43.7 87.9

(10.9) (15.2) (16.1) (12.3)

Retrieval

vided Difference Free recall Cued recall Difference

12 34 58 235 26 36 10

10 26 41 15


process that makes it possible to overcome or reduce verbalmemory deficits. These processes were explored via theLOP theory (Craik & Lockhart, 1972) by manipulatingthe depth of processing of information, elaboration, andkind of retrieval.

4.1. Healthy subjects and cognitive aids

In the healthy subjects, each cognitive aid was effective,alone and in interaction with another aid, as shown by thefact that their performance improved consistently from thecondition with no aid to the one with three aids.

Deep (semantic) processing led to better subsequentmemory performance than ‘‘shallow’’ perceptual or physi-cal processing (Craik & Lockhart, 1972; Craik & Tulving,1975). An elaborated processing enhanced performance(Mantyla & Nilsson, 1983). Finally, encoding specificityalso had an effect (Tulving & Thomson, 1973). Given a spe-cific type of encoding, retrieval was optimized when the testwas designed to use the same type of information. Forexample, to benefit from phonetic encoding, a rhyme-cuedrecall is effective (Fisher & Craik, 1977; Morris, Bransford,& Franks, 1977).

By combining depth of processing and retrieval aids, wefound that semantic processing was enhanced by semantic-cued recall. Giving these two aids together boosts memoryperformances. This result is in agreement with previousstudies, which showed that rhyme encoding coupled witha rhyme retrieval task resulted in poorer performance thana combination of semantic encoding and semantic retrieval(Fisher & Craik, 1977; Lespinet-Najib et al., 2004; Morriset al., 1977) The second interaction in our study concernedelaboration and depth of processing. We demonstratedthat elaboration aid coupled with depth of processing aidin a memorization task improved performance (Kuiper &Rogers, 1979; Maki & McCaul, 1985; Rogers et al.,1977). Finally, the interaction between all three dimensionsconfirmed that each individual effect was enhanced by thepresence of the others, as previously shown by Mantylaand Nilsson (1983) or Lespinet-Najib et al. (2004).

Our results confirmed that LOP dimensions facilitatedmemorization and could be used as cognitive aids in thefield of compensation.

4.2. Epileptic patients and cognitive compensation

The two groups of patients’ present verbal memory def-icits revealed by the Wechsler memory test. Our resultsshow that both groups benefited from cognitive aids suchas deep processing, elaboration, or cued recall. TheANOVA revealed the global effect of each of these factors.Furthermore, the Retrieval-Groups interaction revealedthat the effect of the retrieval aid differed from one groupto another. L-TLE benefited relatively little from cuedrecall; whereas R-TLE and NC performance wereenhanced, even if R-TLE do not achieve NC performances(compensation for R-TLE was only partial). Furthermore,

the interaction data indicate that the combined effects ofthe three aids differed from group to group with the follow-ing findings:

• For phonetic processing: L-TLE did not enhance perfor-mance whatever the aid whereas R-TLE improved per-formances when information is elaborated. So, L-TLEpatients suffer from a memory deficit in encoding pho-netic information. When both of the other aids were giv-en, the performance of this group did not improve.These results reflect those of N’Kaoua et al. (2001)and Rains (1987), who reported on deficits in anL-TLE group, and support the fact that phonetic pro-cessing selectively engages the left cortex (Berman,Mandelkern, Phan, & Zaidel, 2003; Coney, 2002; Dem-onet et al., 1992, Demonet, Price, Wise, & Frackowiak,1994). The R-TLE group, however, did benefit fromcognitive aids at the phonetic processing stage, particu-larly from elaboration. These results are in agreementwith those of Lespinet-Najib et al. (2004) and Mungaset al. (1985), who showed verbal memory deficits forshallow levels of processing in an L-TLE group but few-er (Mungas et al., 1985) or none (Lespinet-Najib et al.,2004) in an R-TLE group.

• For semantic processing: L-TLE patients presentedbetter performance than R-TLE. So, when asked tomemorize semantic information, L-TLE patients didimprove their performance. This result may be interpret-ed as reflecting the fact that their difficulty in engagingsemantic processing spontaneously is attenuated by anappropriate semantic aid. The memory performance ofR-TLE patients was improved by cued recall, whichfindings may also be interpreted as reflecting theirdifficulty in engaging retrieval processing, which isovercome by providing a retrieval aid.

• Finally, all the groups achieved better performancewhen the three aids were given, but the two groups ofpatients did not match NC performance (compensationwas partial). At this stage, the two groups of patientspresented their most important deficit in comparisonto healthy subjects but at the same time they presentedtheir better performance. So, they did not benefit ashealthy subjects of the conjunction of the three aids,as a function of the cognitive load of the task. Indeed,L-TLE patients performed as healthy subjects whenonly one aid (deep processing) was proposed but didnot reach their performance when the three aids weregiven.

Another main result of our study is that L-TLE patientshad difficulty engaging spontaneously in encoding process-es (deep processing as to be proposed to enable theimprovement of their performance), whereas R-TLEpatients had retrieval process impairments (a cue is neces-sary to enable memory performance improvement). Thisfinding may be interpreted in the light of functional imag-ing studies. It has often been found that left lateralization


of cerebral activity is correlated with the encoding stage,whereas activity on the right is correlated with the retrievalstage (Golby et al., 2001), as in the HERA (HemisphericEncoding Retrieval Asymmetry) model developed by Tul-ving, Kapur, Craik, Moscovitch, and Houle (1994). In theirarticle, Tulving and collaborators (1994) reviewed numer-ous publications and demonstrated that frontal lobes areimplicated in encoding and retrieval. But when we examinethose publications we can observe that temporal lobes arealso implicated (e.g., Squire et al., 1992; Wise et al.,1991). So, the HERA model could also be used in temporallobe pathology like epilepsy. The asymmetry reported bythe HERA model in processing verbal material has beenalso demonstrated to be independent of material modality(Habib, Nyberg, & Tulving, 2003; Nyberg, Cabeza, &Tulving, 1996) as it has been observed for verbal andnon-verbal material. However, these results are not consen-sual (Blanchet et al., 2001). Campo et al. (2005), usingMEG, found right as well as left medial temporal lobe acti-vation during verbal encoding. Finally, Greicius et al.(2003) tested the HIPER (Hippocampus Encoding Retriev-al) model of Lepage, Habib, and Tulving (1998), developedusing PET studies, which states that the anterior hippo-campus is activated by encoding and the posterior hippo-campus by retrieval. These authors refuted the HIPERmodel by finding left and right activation of the entire hip-pocampus for encoding and retrieval stages using fMRIand a visual word recognition task. However, the resultsof our study are clearly aligned with the HERA findings,as patients suffering from a left hemisphere injury developan encoding deficit, whereas patients with a right hemi-sphere epileptic focus develop a retrieval deficit.

Therefore, the fact that the ability of the L-TLE to com-pensate depends mainly on the deep processing aid which isgiven at the encoding stage (they achieved healthy subjectsperformance), while the R-TLE need retrieval aid given bythe cue at the retrieval stage (R-TLE patients alwaysenhanced performance when a cue is provided), may beexplained by the use of the residual ability of their damagedhemisphere. Indeed, the left hemisphere is largely implicat-ed at encoding stage and the right hemisphere at retrievalstage (HERA model). So, our findings that L-TLE patientsbenefit from the encoding aid and R-TLE patients from theretrieval aid are in favor of the hypothesis that they useresidual hippocampal ability. This assumption is in agree-ment with the hippocampal functional adequacy model ofthe damaged hippocampus described by Chelune (1995),where functional adequacy is defined as the residual capac-ity of the epileptic hippocampus to perform memoryfunctions.

When the three aids are given, they are proposed atencoding and retrieval stages so our results suggest thatpatients rely on the residual ability of their damaged hippo-campus and on their contralateral hemisphere reserves:encoding aids solicit the damaged hippocampus ofL-TLE patients and retrieval aids involve their undamagedhemisphere, and conversely for R-TLE patients.

To conclude, from a perspective of rehabilitation, thisstudy is a first step in understanding the type of cognitivetool to use in neuropsychological sessions. To improveL-TLE memory performance, patients would be helpedto use depth of processing more effectively, e.g., byself-reference or self-generated cues. The performance ofR-TLE patients is enhanced by all the cognitive aids,provided that a retrieval aid is presented. A cognitive tooldealing with retrieval cues is likely to be effective. Furtherresearch is required to observe the impact of differentcognitive aids on compensation, in order to developcognitive tools specially adapted to each type of epilepticpatient’s deficit, depending on several factors, includinglaterality, seizure frequency, number of antiepilepticdrugs, and age of onset.

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