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This article appeared in a journal published by Elsevier. The attachedcopy is furnished to the author for internal non-commercial researchand education use, including for instruction at the authors institution
and sharing with colleagues.
Other uses, including reproduction and distribution, or selling orlicensing copies, or posting to personal, institutional or third party
websites are prohibited.
In most cases authors are permitted to post their version of thearticle (e.g. in Word or Tex form) to their personal website orinstitutional repository. Authors requiring further information
regarding Elsevier’s archiving and manuscript policies areencouraged to visit:
Children with refractory epilepsy often display academicdifficulties and behavioral problems. Recent research in theneuropsychology of childhood epilepsy has provided evidenceof specific cognitive profiles according to the localization ofthe epileptic process (Elger, Helmstaedter, & Kurthen, 2004;Jambaque, Lassonde, & Dulac, 2001). Temporal lobe epilepsy(TLE) has been associated with language and memory impair-
∗ Corresponding author at: Universite Paris Descartes, Laboratoire de Psy-chologie et Neurosciences Cognitives, CNRS FRE 2987, 71 avenue EdouardVaillant 92 774 Boulogne Billancourt Cedex, France. Tel.: +33 1 55 20 59 51;fax: +33 1 55 20 59 85.
ments in adults (Helmstaedter, Lehnertz, Grunwald, Gleissner,& Elger, 1997; Jones-Gotman, 1986; Saykin, Gur, Sussman,O’Conner, & Gur, 1989), and more recently in children as well,both before and after surgery (Gleissner, Sassen, Schramm,Elger, & Helmstaedter, 2005; Jambaque et al., 2007; Lendt,Helmstaedter, & Elger, 1999). Some children studies reportedan effect of the side of epilepsy, with impairment of ver-bal functions in left temporal lobe epilepsy (LTLE) and ofnonverbal functions in right temporal lobe epilepsy (RTLE)(Beardsworth & Zaidel, 1994; Fedio & Mirsky, 1969; Gadianet al., 1996; Jambaque, Dellatolas, Dulac, Ponsot, & Signoret,1993; Jambaque et al., 2007; Szabo et al., 1998). Other stud-ies failed to find this effect or found it to be less pronouncedthan in adults, which suggests that the effect of lateraliza-tion of the epileptic focus on specific cognitive functions
1416 N. Golouboff et al. / Neuropsychologia 46 (2008) 1415–1428
is less relevant in children than in adults, particularly aftertemporal lobe surgery (Gonzalez, Anderson, Wood, Mitchell,& Harvey, 2007; Lendt et al., 1999; Mabbott & Smith,2003).
On the other hand, children with TLE have high ratesof psychopathology, such as mood and personality disorders,hyperactivity, conduct disorders and social difficulties or autism-like behaviors (Besag, 2004; Caplan et al., 2004; Carracedo etal., 1995; Deonna, Ziegler, Moura-Serra, & Innocenti, 1993;Kaminer, Apter, Aviv, Lerman, & Tyano, 1988; Neville et al.,1997; SBarra, Rimm-Kaufman, & Pianta, 2002). An importantfactor in determining the severity of the effect of epilepsy oncognitive and behavioral disorders is age of onset (Caplan et al.,2004; Cavazzuti & Nalin, 1990; Nolan et al., 2003; Saykin et al.,1989). Improvement of cognitive abilities, behavior, and qualityof life has been reported after temporal lobe resection in chil-dren which argues in favor of early surgical intervention (Costada Costa, 2002; Danielsson, Rydenhag, Uvebrant, Nordborg,& Olsson, 2002; Gleissner et al., 2005; Lendt, Helmstaedter,Kuczaty, Schramm, & Elger, 2000; Lendt et al., 1999; Lewiset al., 1996; Sinclair et al., 2003; Smith, Elliott, & Lach,2004).
Since children with TLE display cognitive and psychoso-cial difficulties, neuropsychological investigations should assessboth cognitive functions and socio-emotional abilities as well.Facial expressions are nonverbal cues that allow us to expressand communicate our own emotions. They also allow us to rec-ognize the emotions of others, which helps us to gauge theeffects of our behavior on others and to adjust it accordingly.Recognizing emotions in the faces of others is an importantsocial skill that facilitates appropriate interpersonal interactions(Harrigan, 1984) and, thus, justifies using facial photographsin research studies of emotion processing in children, adoles-cents, and adults (Ekman & Friesen, 1976; Herba & Phillips,2004; McClure, 2000). Deficits of emotion processing are usu-ally detected in brain-damaged and emotionally disturbed adultsusing Pictures of Facial Affect (Ekman & Friesen, 1976); a setof pictures of adult faces expressing six innate, universal emo-tions (happiness, sadness, anger, disgust, fear, and surprise), theso-called ‘basic’ emotions (Ekman, 1992; Ekman & Friesen,1971).
Neural networks underlying facial emotion recognitioninvolve a distributed set of structures that include the visualcortices, the amygdala, the orbitofrontal cortex, and addi-tional cerebral regions, such as the insula, the basal ganglia,and the prefrontal cortex (Adolphs, 2002). The amygdala,which is often damaged with the hippocampus in patientswith TLE (Miller, McLachlan, Bouwer, Hudson, & Munoz,1994; Pitkanen, Tuunanen, Kalviainen, Partanen, & Salmenpera,1998), has been identified as an important structure for eval-uating emotional stimuli, particularly potentially threateningand dangerous stimuli, and for regulating social and emotionalbehavior (Aggleton, 1992; LeDoux, 1992, 2000). In the maturemonkey, bilateral damage of the amygdala produces an inabilityto evaluate the social and emotional meaning of visual stim-uli and generates a lack of fear responses to inanimate objectsand a “socially uninhibited” pattern of behavior (Amaral et al.,
2003; Kluver & Bucy, 1939; Meunier, Bachevalier, Murray,Malkova, & Mishikin, 1999; Weiskrantz, 1956). In humans,there is evidence that bilateral lesions to the amygdala impairthe recognition of emotions in facial expressions, fear particu-larly (Adolphs, Tranel, Damasio, & Damasio, 1994; Adolphs,Tranel, Damasio, & Damasio, 1995; Broks et al., 1998; Calderet al., 1996; Sprenglenmeyer et al., 1999). Severe impairmentin recognizing fear can be included into a larger impairmentin recognizing emotions of negative valence (Adolphs et al.,1999; Broks et al., 1998; Calder et al., 1996; Sato et al., 2002;Schmolck & Squire, 2001; Sprenglenmeyer et al., 1999). Sim-ilar or more subtle deficits in recognizing fear were reported inadults with TLE after right temporal lobe resection (Adolphs,Tranel, & Damasio, 2001; Adolphs, Baron-Cohen, & Tranel,2002; Anderson, Spencer, Fulbright, & Phelps, 2000; Brierley,Medford, Shaw, & David, 2004; McClelland et al., 2006). How-ever, these deficits are not related to the surgery exclusively,but also to the pre-existing epileptogenic lesion. A recent facialemotion recognition study of patients with RTLE indicatedthat their impairment in fear recognition existed before surgery(Melleti et al., 2003) and a functional magnetic resonance imag-ing study indicated that patients with RTLE, but not those withLTLE, failed to activate right temporal lobe structures dur-ing implicit processing of fearful expressions (Benuzzi et al.,2004).
Nevertheless, some adult patients with RTLE or bilateralamygdala damage perform normally in face-emotion recogni-tion tasks (Adolphs et al., 1995; Adolphs et al., 2001; Andersonet al., 2000; Brierley et al., 2004; Hamann & Adolphs, 1999). Theeffect of a damaged amygdala on fear recognition may depend onthe state of maturation of the amygdala when the damage occurs.Indeed, impaired fear recognition is observed in patients suffer-ing from congenital disease or early-acquired bilateral amygdaladamage (Calder et al., 1996; Hamann et al., 1996; Hamann &Adolphs, 1999) and in adults with RTLE whose seizures beganearly in childhood, especially before the age of 5–7 (Anderson etal., 2000; Adolphs et al., 2001; Benuzzi et al., 2004; McClellandet al., 2006; Melleti et al., 2003). These findings suggest that anearly epileptic focus situated in the right mesial temporal loberegions might delay or disturb or preclude the functional mat-uration of the neural networks mediating the processing andthe interpretation of fear conveyed by facial expressions. Thissuggestion is consistent with the hypothesis that the right hemi-sphere is dominant for the perception of emotions both in adults(Adolphs, Damasio, Tranel, & Damasio, 1996; Borod et al.,1998; Bowers, Bauer, & Heiman, 1993) and children (Saxby& Bryden, 1985).
In normal development, neural networks for the processingof facial emotions mature progressively from early childhooduntil the end of adolescence (Batty & Taylor, 2006; Taylor,McCarthy, Saliba, & Degiovanni, 1999). Functional imagingstudies indicate a functional maturation of the amygdala occursduring adolescence (Monk et al., 2003; Nelson et al., 2004) andthat amygdala responses occur during the processing of fear-ful expressions in children and adolescents (Baird et al., 1999;Killgore, Oki, & Yurgelun-Todd, 2001; Lobaugh, Bibson, &Taylor, 2006; McClure et al., 2004; Thomas, Drevets, Whalen
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et al., 2001). Developmental studies of children’s ability todetect and label emotions in pictures of facial expressions havedescribed progressive improvement of performance betweenthe ages of 5 and 15–16, except for happiness, which is accu-rately recognized from the youngest age (Gosselin, 1995; Lenti,Lenti-Boero, & Giacobbe, 1999; Tracy, Robins, & Lagattuta,2005; Vicari, Reilly, Pasqualetti, Vizzotto, & Caltagirone, 2000).However, methodological differences between studies make itdifficult to describe the trajectories of the development of therecognition of negative emotions (Herba & Phillips, 2004).We recently developed a new task in which children labelpictures of children miming five basic emotions (fear, anger,disgust, sadness, happiness) and a neutral expression, Test deReconnaissance des Emotions Faciales pour Enfants (TREFE,Golouboff, Jambaque, & Fiori, unpublished). With the TREFE,typically developing children are nearly perfect in recogniz-ing happiness (99%), neutrality (98%) and fear (97%) andsomewhat lower for anger (90%), disgust (85%) and sadness(80%).
In the present study, we used the TREFE to assess recognitionof children’s facial emotions in 37 children and adolescents withfocal drug-resistant epilepsy. The impact of TLE on recognitionof children’s facial emotions was assessed by comparing the per-formances of 29 children and adolescents with TLE (13 right,16 left), eight with extra-temporal frontocentral epilepsy (FCE),and 37 matched healthy children. Children with FCE consti-tute an epileptic control group, as epiletogenic focus does notinvolve orbitofrontal cortex or prefrontal cortex, which are thecortical areas implicated in recognition of facial affect (Hornak,Rolls, & Wade, 1996). The performance of children with TLEwas also compared to that of the large sample of typically devel-oping children that was used to standardize the TREFE. Wehypothesized that (1) the children suffering from an epilepticfocus in the mesial temporal lobe regions would be impaired inemotion recognition, particularly fear; (2) emotion recognitionimpairments would be more pronounced in the children whoseseizure activity began early in infancy than in the children whoseseizures began later in childhood; and (3) the lateralization ofthe epilepsy would have an impact on emotion recognition per-formances, with the poorest recognition expected in childrenwith RTLE. Finally, prior research has emphasized a relationshipbetween psychopathology and face-emotion recognition. Manystudies in children and adolescents note associations betweenreduced face-emotion recognition skill and anxiety/depression(Easter et al., 2005; Lenti, Giacobbe, & Pegna, 2000; McClure,Pope, Hoberman, Pine, & Leibenluft, 2003), social problems(Simonian, Beidel, Turner, Berkes, & Long, 2001) and conductdisorders (Blair & Coles, 2000; Stevens, Charman, & Blair,2001). Therefore, we also tested the hypothesis that TREFEscores of subjects with TLE will be related to their psychoso-cial adjustment. For psychopathology, behavioral profiles wereassessed with the Achenbach Child Behavior Checklist (CBCL)(Achenbach, 1991), a widely used parental-report question-naire to assess psychosocial disorders in children, especiallyin children with epilepsy (Dorenbaum, Cappelli, Keene, &McGrath, 1985; Hermann, Whitman, Hughes, Melyn, & Dell,1988). Ta
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1418 N. Golouboff et al. / Neuropsychologia 46 (2008) 1415–1428
2. Methods
2.1. Participants
Thirty-seven children with epilepsy (21 girls), 8–16 years old, were evaluatedbetween September 2004 and December 2006 at the Paediatric Epilepsy Neuro-surgery Department of the Fondation Rothschild (Paris, France). The followingselection criteria were used to select the children: (1) right-hand dominance,(2) mesial TLE or fronto-central epilepsy (FCE) involving motor, pre-motor oropercular regions, (3) enrolment in a normal school and (4) full-scale IQ scoreabove 70 on the Weschler Intelligence Scale for Children – III (Weschler, 1991).Twenty-nine of the children had TLE – 13 with right temporal lobe epilepsy(six treated surgically) and 16 with left temporal lobe epilepsy (nine treatedsurgically) and eight children had FCE (six were treated surgically). Anatom-ical MRI data were available for all the children. Children with surgery hadundergone either a unilateral anteromesial temporal lobe resection (includingthe amygdala, the hippocampus and temporal pole) or a unilateral resectionof the motor, pre-motor or opercular regions (but not of the orbito-frontalcortex). Demographical, neuropsychological and medical profiles of childrenwith epilepsy are shown in Table 1. There was no significant difference in theprofiles of the TLE and FCE groups. The number of boys and girls and themean age of children in RTLE and LTLE groups were equivalent. However,the LTLE group had an earlier age of seizure onset and poorer verbal perfor-mances (IQ and naming) than subjects with RTLE. Finally, each subject withepilepsy was matched on age and gender to a healthy subject without epilepsy(n = 37).
2.2. Materials and procedures
A face recognition battery was used to investigate socio-emotional skillsof the children with epilepsy. All of them were administered (1) a preliminaryFace Matching Task to insure that performance on the TREFE could not berelated to perceptual deficits, (2) a Face Memory Task to assess their ability torecognize unfamiliar faces and finally, (3) the TREFE. Their parents filled theCBCL questionnaire. One girl with LTLE did not complete the Face MemoryTask and the CBCL for one girl with LTLE was not returned.
2.2.1. Preliminary tests2.2.1.1. Face Matching Task. We constructed a face identity matching task toassess visuo-perceptual ability to identify faces. Black and white photographs ofchildren’s neutral faces were extracted from the face memory test of the NEPSY(Korkman, Kirk, & Kemp, 2003). Each trial was composed of a stimulus face onthe top of a sheet of paper and four stimulus faces below it (the target stimulusand three distractors). Distractors were photographs of faces of different childrenmatched to the target on sex, age and appearance. On each trial the subject hadto point to one of the four faces on the bottom of the paper that they thoughtmatched the target on the top of the paper. There were 16 trials. The score wasthe number of correct answers.
2.2.1.2. Face Memory Task. The Face Memory Task of the CMS (Cohen, 2000)was used to assess the subjects’ ability to remember faces. The subject wasinstructed to remember the color photographs of unfamiliar faces of children and
adults. The photographs were presented one at a time for 2 s each. There were12 faces to remember for children 5–8 years old and 16 faces for children 9–16years old. Face memory was assessed immediately after presentation (immediaterecognition) and 30 min later (delayed recognition). In each recognition phase,the stimuli were presented one at a time and the target stimuli were mixed withdistractors (16 distractors for the youngest, 24 distractors for the oldest). Thesubject had to show the already seen faces. The number of correct answersand a standardized score were calculated (max = 20) by referring to normativedata.
2.2.2. Facial recognition of emotions (TREFE)The Test de Reconnaissance des Emotions Faciales pour Enfants (TREFE,
Golouboff, Jambaque, & Fiori, unpublished) is a computerized test for childrenand adolescents that evaluates their recognition of facial emotions expressedin the photographs of children and adolescents. The test includes 72 colorpictures of 5–15 year-old children’s faces miming five basic emotions (fear,anger, disgust, sadness, happiness) and neutrality (no emotion). The test con-tains 12 items (six photographs of boys and six photographs of girls) of eachfacial expression (Fig. 1). Facial expressions of surprise, which share a numberfeatures similar to those expressed by fear (i.e., wide eyes, raised eyebrows,opened mouth) were not included to avoid confusion between these two emo-tions (Bullock & Russell, 1985; Ekman & Friesen, 1971; Rapcsak et al., 2000).As in Ekman’s test (Ekman & Friesen, 1976), we retained neutral faces to allowassessment of the ability to recognize positive and negative emotions relative tono emotion.
During their introduction to the TREFE, subjects had to read the printednames of the emotions and to give synonyms or examples of situations in whichthey might feel these emotions to prove that they knew their meaning. If nec-essary, the investigator explained the emotions in order to verify that the childunderstood the instructions.
Then, six practice stimuli (one for each facial expression) were used tofamiliarize the subjects with the task while receiving feedback from the exper-imenter: a picture of a child’s face expressing an emotion was presented ona computer screen until the subject labeled it or until 30 s passed without asubject response, at which time the subject was forced to supply a label. Thesubject had a list of the six possible labels (fear, anger, disgust, sadness, happi-ness, and neutrality) and was free to consult it. After the subject responded, theexperimenter corrected its response if necessary and pressed a computer key,which recorded the first response and initiated the next picture: a cross on ablack background appeared for 1000 ms, then, the next picture appeared on thescreen.
The same procedures were used during administration of the TREFE, but nofeedback was provided. Seventy-two pictures occurred in a sequence determinedby an E-Prime software program, with the constraint of the same mean rank ofpresentation for each expression category. The total number of correct answers(out of 72) and correct answers for each facial expression (out of 12) werecomputed.
2.2.3. Behavioral profileThe CBCL (Achenbach, 1991) is an internationally used instrument for
the assessment of behavioral disorders in children between 4 and 18 yearsof age. The questionnaire consists of 113 items to which parents respondwith a number, 0 – not true at all, 1 – somewhat or sometimes true or 2
Fig. 1. Stimuli used in the TREFE. Girls’ and boys’ faces expressing fear, anger, disgust, sadness and happiness, as well as faces with neutral expression, were used.
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N. Golouboff et al. / Neuropsychologia 46 (2008) 1415–1428 1419
– very true or often true. The CBCL contains Behavior Scales (withdrawn,somatic problems, anxious/depressed, thought problems, social problems, atten-tion problems, aggression problems, and delinquency). The results for eachscale are expressed as T-scores, with T-scores of 67–70 representing a ‘border-line clinical’ range, and T-scores above 70 indicating ‘pathological’ range. Italso provides a general behavioral problem index (total score); an InternalizingProblems index that represents over-controlled behavioral problems (social with-drawal, somatic complaints, anxiety/depression) and an Externalizing Problemsindex that represents under-controlled behavior problems (aggression, delin-quent behavior). Results for these three scales are also expressed as T-scores,with T-scores of 60–63 representing a ‘borderline clinical’ range, and T-scoresabove 63 indicating a ‘pathological’ range.
2.3. Data analysis
Statistical analyses were performed with Statistica 6.0 and SAS softwareversion 6.0. Unresected and resected patients were grouped together because nosignificant effect of resection was found either for the face memory tasks or forthe facial expression recognition task (all P-values >.05). We used the GeneralLinear Model (GLM) procedure to examine age and group effects (comparingthe mean accuracy of RTLE, LTLE, FCE and control subjects) on the immediateand delayed face memory tests and on the TREFE, total score and scores for eachfacial expression. When the group effect was significant, a two by two post-hoccomparison of the means was performed using Duncan’s test. To examine thetype of emotion effect and the emotion by group interaction a repeated measureMANOVA was performed (using the repeated measures option of GLM). TheMANOVA examines if some emotions are better recognized than others (i.e.the type of emotion effect) and if this effect is the same in all groups (i.e. theemotion by group interaction).
Additional analyses were performed within the TLE group. Age at acquiredbrain insult has been proposed as a possible source for inconsistent findingsin recognition of facial emotions in adults with TLE (Anderson et al., 2000;Adolphs et al., 2001; Melleti et al., 2003; Benuzzi et al., 2004; McClellandet al., 2006). We explored the impact of the febrile convulsions and of theage at onset of epilepsy on the ability to recognize emotions by regressionsanalyses, partialling out the effect of the age of the child at examination. Forthis purpose, raw scores of the TREFE were transformed to Z-scores, accord-ing to normative references established for boys and girls of five age ranges(7–8, 9–10, 11–12, 13–15, 16–25 years) (Golouboff, Jambaque, & Fiori, unpub-lished).
The relation between emotion recognition (Z-scores) and scores on eachbehavioral scale of the CBCL was assessed using Pearson correlations. Totest whether these correlations were significantly different in RTLE and LTLEsubjects, the General Linear Model (GLM) procedure of SAS software wasused.
3. Results
3.1. Preliminary tasks
3.1.1. Face matchingAll children with epilepsy performed successfully in the
face matching task which indicates that none of them hadvisuo-perceptual difficulties that would compromise face dis-crimination (Table 2).
3.1.2. Face memoryThe RTLE group obtained the poorest performances in this
task, and the RTLE and LTLE groups tended to recognize fewerfaces than the FCE group, however these tendencies were notsignificant: F(2, 33) = 1.69, P = .20, for the immediate, and F(2,33) = 1.07, P = .36 for the delayed recognition phases (Table 2).The correlation between face recognition memory and the ageat onset of epilepsy was not statistically significant. Face recog-nition scores were negatively correlated with T-scores on theinternalizing problems scale (immediate recognition, r = −.48,P = .012, and delayed recognition, r = −.41, P = .036), includ-ing the withdrawal scale (immediate recognition, r = −.39,P = .05 and delayed recognition, r = −.40, P = .044) and the anx-iety/depression scale (immediate recognition, r = −.46, P = .02and delayed recognition, r = −.46, P = .02). These correlationsindicate that the memory for faces of introverted, anxious ordepressed children with TLE was lower than that of childrenwith TLE without internalizing problems.
3.2. Facial recognition of emotions (TREFE)
3.2.1. Impact of presence and localization of theepileptogenic zone3.2.1.1. Mean accuracy. Age was significant on the mean over-all accuracy at the TREFE, F(1, 69) = 4.95, P = .003, howevermean age was similar in all groups. The effect of the group onoverall performance was significant, F(1, 69) = 4.92, P = .004.All groups of children with epilepsy (RTLE, LTLE and FCE
Table 2Mean recognition scores of the controls and of the children with frontal lobe epilepsy (FCE), right temporal lobe epilepsy (RTLE) and left temporal lobe epilepsy(LTLE) on the face matching, face memory and TREFE tests
Controls (n = 37) FCE (n = 8) RTLE (n = 13) LTLE (n = 16)M (S.D.) M (S.D.) M (S.D.) M (S.D.)
a Group-values performance significantly lower than controls (P < .05).
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1420 N. Golouboff et al. / Neuropsychologia 46 (2008) 1415–1428
groups) performed lower relative to controls (Table 2), how-ever, post-hoc analyses of the means revealed that the LTLEgroup only obtained a mean overall performance significantlylower than controls. Analyses by emotion showed significantgroup differences for fear, F(1, 69) = 4.08, P = .01, disgust,F(1, 69) = 3.11, P = .03, neutrality, F(1, 69) = 5.32, P = .002,and marginally for happiness, F(1, 69) = 2.64, P = .056. Post-hoc comparison of the means revealed that (1) the LTLE groupwas significantly impaired for the recognition of fear relative toall the other groups, and for neutrality relative to controls andFCE groups; (2) the RTLE was significantly impaired relativeto controls for the recognition of disgust, and (3) the FCE groupwas significantly impaired relative to controls and RTLE groupsfor the recognition of happiness. No significant difference wasfound for anger and sadness (P-values >.05).
3.2.1.2. Emotion effect and emotion by group interaction onaccuracy. There was a main effect of emotional category, F(5,66) = 23.8, P < .001. The interaction group by emotion was sig-nificant, F(15, 182.6) = 2.00, P = .02. Performance of controlswas better for happiness, neutrality and fear than for recogni-tion of anger, disgust and sadness (in a decreasing order) (allP-values <.05, except between happiness, neutrality and fear).This indicates that, in typically developing children, fear is thethird best recognized emotion, easier to recognize than the threeother negative emotions (anger, disgust and sadness). It has beennoted that surprise, which is often confused with fear, was notincluded in our task. The children with epilepsy showed a some-what different emotional ordering pattern relative to controls,with different places of fear or disgust according to the topog-raphy of the epilepsy. Fear was less well recognized than angerby the children with LTLE (fear in fourth position) whereas fearwas better recognized than happiness by the children with FCE(fear in first position). Disgust was less well recognized thansadness by the children with RTLE and by the children withFCE (disgust in last position).
Like typically developing children, LTLE patients often mis-interpreted fearful expressions as disgust (61% of the errors forfear recognition), and RTLE patients misinterpreted disgustedexpressions as anger (73% of the errors for disgust recognition).In contrast, for neutral faces, LTLE children made atypical errorsby misinterpreting them as anger (43% of the errors for neutralfaces recognition) whereas typically developing children rathermisinterpreted them as sadness (39% of the errors for neutralfaces recognition). FCE children made atypical errors for therecognition of happy faces by misinterpreting them as fear (57%of the errors for neutral faces recognition) whereas typicallydeveloping children rather misinterpreted them as neutral faces(53% of the errors for neutral faces recognition). This suggests abias toward negativity in the recognition of emotions in childrenwith FCE.
3.2.2. Influence of the age at epilepsy onset and of febrileconvulsions
For children with TLE, age-adjusted total score (Z-score) onthe TREFE were positively correlated with the age at onset ofthe first temporal lobe seizure (r = .51, P = .006) which indicates
that earlier onset of temporal lobe seizures led to worse perfor-mances for the recognition of facial expressions. We observedpositive correlations between Z-scores for each facial expres-sion and the age at onset of the first temporal lobe seizure, butthese correlations did not reach a significant threshold (all P-values >.05). With regard to the impact of febrile convulsions onemotion recognition, we found that children with TLE who hadexperienced febrile convulsions during infancy obtained a meanrecognition Z-score for fear (M = −3.0, S.D. = 3.7) significantlylower than children with TLE without history of febrile convul-sions (M = .1, S.D. = 9.9), t(27) = 3.36, P = .002). In contrast, theimpact of febrile convulsions was not statistically significant forthe other emotional expressions. There was no significant asso-ciation between presence or absence of febrile convulsions andage at onset of the first temporal lobe seizure, t(27) = .36, P = .73.
3.2.3. Correlations with CBCL scoresRTLE group obtained higher CBCL scores, particularly for
internalizing problems, than FCE and LTLE groups, but thistendency was not significant (P-values >.5 for all scales of theCBCL) (Table 3). RTLE patients showed the highest CBCLscores for internalizing (anxiety/depression, withdrawal) andsocial problems, followed by attention deficit, conduct problemsand thought disorders. LTLE patients often showed social andinternalizing problems and, in a less extend, attention deficitand conduct disorders. There was no significant correlationbetween CBCL scores and age at onset of temporal lobe epilepsy.FCE patients showed the highest CBCL scores for internalizing(anxiety/depression, withdrawal), social problems and attentiondeficit, followed by thought disorders. None of the children withFCE showed conduct disorders.
Correlations between age-adjusted TREFE scores (Z-scores)and CBCL scores were statistically significant in the group ofchildren with RTLE, but only for the emotion of fear. In con-trast, the correlations in children with LTLE were not statisticallysignificant, for any expression. For fear recognition, Z-scoresof the children with RTLE were negatively correlated with T-scores on almost all the CBCL scales, which indicates that, inthe RTLE group, the poorest performances for fear recogni-tion were obtained by the children who had the highest rates of
Table 3Percent of behavioral problems in children fronto-central lobe epilepsy (FCE),right temporal lobe epilepsy (RTLE) and left temporal lobe epilepsy (LTLE),after pooling ‘borderline’ and ‘pathological’ ranges in the CBCL
N. Golouboff et al. / Neuropsychologia 46 (2008) 1415–1428 1421
Table 4Correlations between fear recognition Z-scores and T-scores for each scale of the CBCL in the children with right temporal lobe epilepsy (RTLE) and left temporallobe epilepsy (LTLE)
Hemisphere × Fear indicates if the correlations are significantly different between RTLE and LTLE patients.* P < .05.
** P < .01.*** P < .001.
psychopathological disorders. In contrast, correlations betweenemotion recognition Z-scores and behavioral disorders in thegroup of children with LTLE were positive and not significant,which indicates that, contrary to the children with RTLE, impair-ments in emotion recognition were not related to behavioraldisorders. The interaction between fear recognition performanceand the side of the TLE was significant for all the scales ofthe CBCL (except somatic complaints), which confirms that therelationship between fear recognition and psychopathologicaldisorders was not the same for the group of children with RTLEand the group of children with LTLE (Table 4). No significantcorrelation was found between happiness recognition Z-scoresand behavioral disorders in the group of children with FCE.
3.2.4. Analysis of individual differences3.2.4.1. Proportion of children with deficient recognition offacial emotions. The large individual differences in TREFE per-formances of the children with epilepsy suggest that some ofthem were impaired in emotion recognition whereas others werenot. In order to establish the extent of impairments in TLE andFCE samples and then, in RTLE and LTLE samples, we assessedhow many individuals in each sample obtained a recognitionscore that was significantly lower than the scores of typicallydeveloping children: we considered subjects whose recognitionZ-scores fell below −2 S.D. to be impaired. We made this assess-ment for the total score and for each of the six expressions.Given because of the not normal distribution of the scores, weverified that all children with −2 S.D. obtained a score lowerthan the 5th percentile of the normative data. Table 5 indicatesthe total proportion of impaired subjects for each emotion foreach group of children with epilepsy. Three of the 13 RTLEsubjects, four of the 16 LTLE subjects and two of eight FCEsubjects were considered to be impaired for overall performanceat the TREFE. Considering scores per expression category, weobserved that some individuals (three RTLE, four LTLE and twoFCE) showed impaired recognition of several expressions butother children with epilepsy (six RTLE, four LTLE, two FCE)
showed impaired recognition of only one expression. Impair-ment of fear was observed in six TLE children (four left, tworight). In contrast, none of the children with FCE was impairedfor fear recognition. Impaired fear recognition tended to be morefrequent in LTLE group (4 of 16) than in the RTLE group (2 of13), and impaired recognition of disgust more frequent in theRLTE group (4 of 13) than in the LTLE group (2 of 16), how-ever these differences were not statistically significant, given thesmall number of subjects in each group.
3.2.4.2. Children with deficient recognition of fear. Here wefocus on the medical history and the neuropsychological pro-files of the six individuals with fear recognition deficit (seeTable 6). These six children had TLE (four left, two right).Five of them showed additional deficiency for the recognition ofone or two other emotions, and one child showed fear-specificimpairment. All of them experienced febrile convulsions duringinfancy whereas only 26% of the children with TLE who per-formed successfully did. The difference was significant (t Fisherexact, P = .002) (Fig. 2). In addition, five of them (four left, oneright) began temporal lobe seizures before the age of 5. Their
Table 5Proportion of children with epilepsy who were impaired at the TREFE per emo-tion type (recognition Z-scores below −2 S.D. of typically developing children’sratings)
Number of patients FCE (n = 8) RTLE (n = 13) LTLE (n = 16)
Impaired total score 25% 23% 31%Impaired at least for one
Note: FCE, fronto-central lobe epilepsy; RTLE, right temporal lobe epilepsy;LTLE, left temporal lobe epilepsy.
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1422 N. Golouboff et al. / Neuropsychologia 46 (2008) 1415–1428
Tabl
e6
Det
aile
dpr
ofile
sof
the
child
ren
with
tem
pora
llob
eep
ileps
y(T
LE
)im
pair
edin
reco
gniz
ing
fear
Subj
ect
Surg
ery
Age
(yea
rs)
FCA
geat
first
TL
EL
esio
nB
ehav
iora
lpro
blem
sV
IQ/P
IQN
amin
g(Z
-sco
re)
Dig
itsp
an(f
orw
ard)
Face
mem
ory
imm
edia
te/
dela
yed/
20Fe
ar(s
core
/12)
Fear
(Z-s
core
)A
dditi
onal
defic
it
R1
(boy
)N
o14
.5Y
es22
mon
ths
HS
Inte
rnal
izin
g,ex
tern
aliz
ing,
soci
al,t
houg
ht,a
ttent
ion
103/
88−.
85
8/7
9−3
.7D
isgu
st
R2
(gir
l)N
o16
.7Y
es13
year
sH
S+
DN
ET
ofth
eam
ygda
laIn
tern
aliz
ing,
exte
rnal
izin
g,so
cial
,tho
ught
,atte
ntio
n92
/91
1.8
75/
710
−4.5
Hap
pine
ss,n
eutr
al
L1
(boy
)Y
es16
.7Y
es4
year
sC
DIn
tern
aliz
ing
86/9
9−2
.46
6/6
10−4
.5Sa
dnes
sL
2(g
irl)
Yes
8.10
Yes
2ye
ars
HS
–86
/90
−3.7
410
/13
5−6
.8D
isgu
st,h
appi
ness
L3
(gir
l)Y
es10
.2Y
es11
mon
ths
HS
+C
D–
88/1
07−5
.65
12/1
02
−8.0
–L
4(g
irl)
No
15.9
Yes
5m
onth
sH
AD
epre
ssio
n,th
ough
t10
6/76
−.3
511
/76
−9.3
Ang
er,h
appi
ness
Not
e:FC
,feb
rile
conv
ulsi
ons;
DN
ET,
dyse
mbr
yopl
asic
neur
oepi
thel
ialt
umor
;HS,
hipp
ocam
pals
cler
osis
;CD
,cor
tical
dysp
lasi
a;H
A,h
ippo
cam
pala
trop
hy.
MRI or pathologic diagnosis indicated hippocampal sclerosis oratrophy. Among these children, three had undergone temporallobe resection including the left amygdala. For the two otherchildren (presurgical patients), the MRI did not reveal amyg-dala damage but only the pathological diagnosis of the resectedtissue can give definite information regarding the nature and theextend of lesion. The other individual was a 16-year-old girl(R2) who began temporal lobe seizure later in childhood. HerMRI revealed right amygdala damage (Fig. 3).
The two adolescents with RTLE (R1 and R2) who wereimpaired in recognizing fear were not surgically treated. Theyhad a relatively low PIQ and exhibited the highest rates of psy-chopathology (‘borderline’ or ‘pathological’ T-scores on all thescales of the CBCL, except somatic complaints). They had a poorvisual contact and, in spite of preserved verbal skills, they rarelyspoke spontaneously and had trouble expressing their feelings.They had poor self-esteem and were anxious and nervous (inter-nalizing problems). They were lonely; they did not approachothers and had few or no friends (social problems). They weredreamy and could not concentrate (attention problems). Theydisplayed mannerisms, obsessions and compulsive behaviors orrepetitive acts (thought problems). They also exhibited verbaland physical aggressive behaviors such as insults, unprovokedscreaming fits, episodic attacks of rage and violence against oth-ers (externalizing problems). R2, who had an amygdala lesion,was also severely depressed: she made multiple auto-mutilationsand suicide attempts. Her case is strongly suggestive of thelink between amygdala damage, impaired fear recognition anddepression.
Among the four children with LTLE that were impaired inrecognizing fear (L1–L4), three had resections (L1, L2, and L3).All four had a relatively low VIQ. These children had trou-ble expressing their thoughts (naming problems) and feelings ineveryday life. They had also a poor visual contact and poor self-esteem. They were anxious and nervous. However, in contrast tothe two children with RTLE, none of them exhibited conduct dis-orders or aggressive behavior, which strongly suggests that thelink between fear recognition impairments and psychopathol-ogy (e.g. externalizing problems) is not the same in the RTLEgroup and in the LTLE group (Fig. 4). The case L4 appeared tobe unique among the children with LTLE. In contrast to the othercases (L1, L2, L3), she had an intellectual efficiency character-ized by a visuo-verbal dissociation in favor of verbal functions,which strongly suggests that she had an atypical hemisphericspecialization, and a behavioral profile that looked like to thatof the case R1 (depression, thought problems).
4. Discussion
The aim of this study was to assess the ability of childrenand adolescents with partial epilepsy to recognize facial expres-sions of emotion using an original paradigm adapted for youths,the TREFE. In spite of their average intellectual level and fullsuccess on a face recognition task, some children with RTLE,LTLE and FCE were impaired in recognizing facial expressionsof emotion relative to controls and showed differential patternsof deficits according to the localization of the epileptogenic zone.
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N. Golouboff et al. / Neuropsychologia 46 (2008) 1415–1428 1423
Fig. 2. Fear recognition Z-scores of the children with TLE who experienced febrile convulsions and of the children with TLE who did not.
Fig. 3. Sagittal (1a) and coronal (1b) MRI shows the damage of the right amygdala in case R2.
Fig. 4. Relationship between T-scores for externalizing problems and Z-scores for fear recognition in the children with right temporal lobe epilepsy (RTLE) and lefttemporal lobe epilepsy (LTLE).
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1424 N. Golouboff et al. / Neuropsychologia 46 (2008) 1415–1428
Relative to controls, LTLE group was impaired in recognizingfear and neutrality, RTLE group was impaired in recognizingdisgust and children with FCE were impaired in recognizinghappiness. Individual analyses showed fear recognition impair-ments in some children with TLE, not in the FCE group. Thisis in agreement with findings from previous studies that provideevidence for fear recognition impairments in adults with TLE,“surprise” being included (Adolphs et al., 2001, 2002; Andersonet al., 2000) or not (Melleti et al., 2003) as one of the basicemotions in the paradigm. This confirms our hypothesis andclearly implicates temporal lobe structures in the developmentof fear recognition. However, we did not find a specific asso-ciation between RTLE and errors on the TREFE task. Rather,we observed more frequent fear recognition deficits in childrenwith LTLE than in children with RTLE. An earlier age at onsetof epilepsy in the LTLE group than in the RTLE group, couldcontribute to this observation. In addition, although previousstudies in children with TLE reported material-specific mem-ory deficits (Jambaque et al., 1993; Nolan et al., 2004) andimpaired face memory in children with RTLE (Beardsworth& Zaildel, 1994; Mabbott & Smith, 2003), the RTLE and theLTLE group did not differ significantly on the face memorytask. However, there is evidence of atypical language lateraliza-tion in early-onset LTLE adults (Liegeois et al., 2004; Pataraiaet al., 2004; Weber et al., 2006) and children (Yuan et al., 2006).Thus, although our children with TLE were all right-handed,one cannot exclude the possibility that several individuals haveatypical language lateralization, e.g. case L4. Nevertheless, onthe cognitive level, the recognition and the labeling of emotionin faces requires both the capture of the perceptual properties ofthe facial expression its link to knowledge of the concept andname of the emotion category. According to this view, the righthemisphere would be especially involved for encoding percep-tual information about the facial emotion (preverbal ability) andthe left hemisphere would be especially involved for the lexicalretrieval of the knowledge and the name of the emotion (verbalability) (Adolphs, 2002). Our analysis of the neuropsycholog-ical profiles of the children with TLE who were impaired infear recognition (except L4 who appears to be a special case)revealed that the children with LTLE but not in children withRTLE had naming problems (Jambaque & Dellatolas, 2000),which has been reported in previous studies (Davies et al., 1994;Hermann, Wyler, & Somes, 1991; Jambaque et al., 2007). Thus,although subjects were free to consult the list of names of theemotions, it can be hypothesized that LTLE group-values pooroverall performance in our facial expression recognition testwas due to an inability to retrieve semantic verbal knowledgeabout emotion, thus, preventing the link between the perceptof the facial expression (that may be intact) and the name ofthe emotion. In contrast, impairments in some of the childrenwith RTLE may not be due to verbal or categorizing disabilitybut rather to a more profound deficit at the perceptual stage ofemotion processing. It would be interesting to compare emotionrecognition performances of the children with RTLE and LTLEusing different tasks, e.g., implicit recognition via a pointingtask vs. explicit recognition via a labeling task, to verify thishypothesis.
4.1. Impact of early seizure activity on the development offear recognition
We observed a great inter-individual variability in fear recog-nition performances of the children with TLE; some showedimpairments whereas others performed similarly to controls.The fact that not all the children with TLE were impaired in rec-ognizing facial expressions is consistent with previous evidencethat unilateral mesiotemporal lobe damage does not invariablyimpair recognition of fearful expressions (Adolphs et al., 1995).Our study provided evidence that an early age of epilepsy onsetmay be crucial in causing facial emotion recognition deficits inchildren with TLE. In particular, the present data suggest thatfebrile convulsions, which generally occur early in life (i.e., 6–18months of age, much earlier than the mean age at onset of TLE)can affect the ability of the children with TLE to recognize fear.This observation is in agreement with findings from adult stud-ies in which it was the age of the first seizure (febrile or afebrile)that was found to be critical for emotion recognition (Adolphset al., 2001; Benuzzi et al., 2004; Melleti et al., 2003). Thissupports the existence of a crucial period, possibly before theage of 5 years, for establishing the neural network that underliesemotion recognition. Chronic TLE is often associated with hip-pocampal and amygdala damage in adults and children (Milleret al., 1994; Pitkanen et al., 1998) and more pronounced volumereductions to the mesial temporal lobe structures were found inpatients who had experienced prolonged febrile seizures earlyin life (Cendes et al., 1993; Wu et al., 2005). Our finding thatof all the TLE children who had experienced febrile convul-sions were impaired in recognizing fear supports the hypothesisthat developmentally early seizure onsets and damage of themesiotemporal lobe structures (rather than the duration of theepilepsy) can generate impairments in fear recognition in thechildren with TLE.
Our data showed for the first time that early-onset TLE cancompromise the ability to recognize facial emotions in child-hood. Furthermore, impaired recognition of facial expressionoccurred both before and after surgery, which suggests that fearrecognition deficits in adults with early-onset TLE (surgicalcases or not) is a developmental disorder and that their deficitmay have been detected earlier if they had been assessed duringchildhood.
The present study confirms the high prevalence of behav-ior problems in children and adolescents with TLE. Behavioralproblems were found in multiple domains – internalizingproblems (anxiety/depression, social withdrawal), externalizingproblems, thought disorders and attention deficits, consistentwith reports of previous studies (Besag, 2004; Caplan et al.,2004; Kaminer et al., 1988; Lendt et al., 2000; SBarra et al.,2002). Children with RTLE tend to have the highest rates ofpsychopathology and we demonstrate that deficits in recogniz-ing fear are related to psychosocial adjustment difficulties inthe RTLE group only, not in the LTLE group. This suggests
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N. Golouboff et al. / Neuropsychologia 46 (2008) 1415–1428 1425
an effect of the laterality of the epileptogenic focus on thebehavioral profiles of these children. In children with RTLE,reduced fear sensitivity may reflect a more general disturbancein emotional behavior related to right hemisphere damage thatis dominant for emotion processing. In agreement with previ-ous psychopathological studies in children and adolescents, wefound a relationship between reduced responsiveness to fear andexternalizing (Blair & Coles, 2000; Stevens et al., 2001) andinternalizing problems (Easter et al., 2005; Lenti et al., 2000;McClure et al., 2003; Simonian et al., 2001). Recent functionalMRI studies have emphasized abnormal amygdala activation inchildren with antisocial behaviors during the passive viewingof emotional scenes (Sterzer, Stadler, Krebs, Kleinschmidt, &Poustka, 2005) and in children with anxiety/depression duringthe passive viewing of fearful faces (Pine et al., 2004; Thomas,Drevets, Dahl et al., 2001). In addition, volumetric studies havedemonstrated an association between volumes of the amygdalaand hippocampus and psychopathological disorders in adultswith TLE (Tebartz van Elst, Woermann, Lemieux, Thompson,& Trimble, 2000; Tebartz van Elst et al., 2003). These data sug-gest that by combining neuropsychological and MRI data in thechildren with TLE it is possible to specify structure–functionassociations within the temporal lobe regions and hemisphericspecialization during the explicit or implicit processing of facialemotions.
4.3. Differential impairment of emotions
Some of the children with TLE who were impaired for therecognition of emotional expressions showed emotion-specificdeficits whereas others showed deficits for the recognition ofseveral emotions, often including the negative emotions. Thesedata indicate that the medial temporal lobe may participate inthe recognition of several emotions, not only in the recogni-tion of fear. Such a view is corroborated by data from adultswith TLE, who have been found to be impaired in the recog-nition of various emotions (Adolphs et al., 2001; Anderson etal., 2000; Melleti et al., 2003). The involvement of the tempo-ral lobe structures in disgust processing remains controversial.Some neuropsychological and functional imaging studies arguein favor of a specific involvement of the anterior insula andbasal ganglia, but not the amygdala, in processing expressionsof disgust (Calder, Keane, Manes, Antoun, & Young, 2000;Phillips et al., 1997; Sprengelmeyer et al., 1996). However,recent functional imaging studies demonstrated that the amyg-dala is involved in the processing of both fear and disgust inhealthy adults and children. Amygdala responses were observedin adults during the processing of disgust-inducing films or pic-tures (Schienle, Schafer, Walter, Stark, & Vaitl, 2005; Stark etal., 2005). Using an implicit face-emotion processing task inhealthy children aged 10–12 years, Lobaugh et al. (2006) pro-vided evidence of insula, basal ganglia and bilateral amygdalaresponses to disgust, with a larger differentiation between fearand disgust in the amygdala. This suggests that the mesial tem-poral lobe structures may have a general role in the processing ofemotions that belong to the category of ‘negative affect’ ratherthan fear alone.
We did not expect children with FCE to be impaired inemotion recognition. Indeed, we selected them because theepileptogenic zone was not localizated in an area that has beenimplicated in emotion recognition (the orbitofrontal cortex).However, there is evidence of connections between the lateraland caudal areas of the orbitofrontal cortex and the premotorareas or frontal opercular areas (Kringelbach & Rolls, 2004). Itcan also be hypothesized that the diffusion ‘at distance’ of theepileptogenic discharges may have a deleterious impact on thematuration and the functioning of the prefrontal cortex, whichmay generate impairments in emotion recognition in some ofthe children with FCE. Interestingly, impairments in recognizingfacial expressions of the FCE group concerned happiness.
4.4. Limitations of the study and perspectives
The present results, and especially the differential impact offear recognition impairment on psychopathology in right andleft TLE, need to be confirmed with larger samples of patientswith TLE. Diminished processing speed is acknowledged to bea primary cognitive morbidity in chronic TLE subjects (Dow,Seidenberg, & Hermann, 2004) and it would be interesting toanalyze response times of children with epilepsy during facialemotion assessment. In addition, our study has focused on therecognition of emotion in static stimuli but it would particu-larly interesting to explore emotion recognition in children withepilepsy using dynamic stimuli since there is evidence that suchstimuli can improve the recognition and discrimination of emo-tions compared to static displays (Werhle, Kaiser, Schmidt, &Scherer, 2000). Finally, it would also be interesting to assessfacial emotion recognition in children with TLE both before andafter surgery to explore the impact of temporal lobe resection onthe development of this socio-emotional skill.
5. Conclusion
Our study is the first to demonstrate emotional dysfunctionin children with TLE. Early-onset TLE can lead to selectiveimpairments in the explicit recognition of fear in children whichsuggests that the integrity of the mesial temporal lobe structuresduring infancy is essential for the development of the process-ing and the appropriate interpretation of threatening signalsconveyed by faces. If our findings of impairments for fear recog-nition in children with TLE only, but not in children with FCE,are confirmed on a larger sample of patients, then the evaluationof facial affect recognition abilities in youth with drug-resistantepilepsy can yield information on the localization of the seizurefocus and the testing of facial affect recognition competenciesmight become a useful part of the neuropsychological evalua-tion of children with epilepsy. In all cases, emotional disordersshould be considered when evaluating the quality of life andsocial adjustment in children with epilepsy. In this context, reha-bilitation projects would include programs that train children tounderstand emotion and that teach them the specific emotiondepicted by a facial expression. It is tempting to hypothesizethat such programs would be useful to improve social commu-nication skills of children with epilepsy.
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Acknowledgments
We thank all the children and their families who so generouslyparticipated in this study. We also thank Georges Dorfmullerand Christine Bulteau of the Unit of Neuropediatric EpilepsySurgery of the Fondation Rothschild and Philippe Bonnet andHenri Coulaud of the Laboratoire de Psychologie et Neuro-sciences Cognitives for advice. This work was supported by agrant from the French Foundation for the Research on Epilepsy(FFRE) to Isabelle Jambaque and by bursaries from the FrenchLeague Against Epilepsy (LFCE) and the French Foundation forthe Research on Epilepsy (FFRE) to Nathalie Golouboff.
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