Cognitive outcome of parietooccipital resection in children with epilepsy

Epilepsia, 51(10):2047–2057, 2010doi: 10.1111/j.1528-1167.2010.02651.x Cognitive outcome of parietooccipital resection in children *yzxSarah Lippe´, *y{Christine Bulteau, *y{Georg Dorfmuller, **Franc¸ois Audren, {Olivier Delalande, and *y{yyIsabelle Jambaque´ *Inserm, U663, Paris, France, University Paris Descartes, Faculty of Medicine, Paris, France; APHP, Necker Hospital, Paris, France; yFaculty of Medicine, Necker Hospital, University Paris Descartes, APHP, Paris, France; zCentre de Recherche CHU Ste, University of Montreal, Montreal, Quebec, Canada; xDe´partement de Psychologie, Centre de Recherche en Neuropsychologie et Cognition, Universite´ de Montre´al, Montreal, Quebec, Canada; {Unite´ de Neurochirurgie Pe´diatrique, Fondation Ophtalmologique A. de Rothschild, Paris, France; **Service d’Ophtalmologie Pe´diatrique Fondation Ophtalmologique A. de Rothschild, Paris, France; and yyLaboratoire de Psychologie et Neurosciences Cognitives (UMR CNRS 8189), Institut de Psychologie, Universite´ Paris Descartes, Paris, France ited deficits related to visual attention, object recognition, and praxis. Nevertheless, our results suggest that brain Purpose: We followed the neuropsychological develop- plasticity after parietooccipital epilepsy surgery in young ment of five children who underwent unilateral neurosur- children allows for a schooling level of cognitive skills such gery of the occipitoparietal lobes as a treatment for epilepsy caused by a developmental lesion (cortical dys- Discussion: Although recovery for visual perceptual cog- nition was more limited than for verbal functions, long- Methods: The follow-up period ranged from 3–7 years term neuropsychological outcomes showed that early surgery for epilepsy offers the possibility of optimizing Results: Two participants had a verbal intelligence quo- cognitive outcomes in children with posterior intractable tient (IQ) >100 and three had a verbal IQ between 65 and 80. All five children had abnormal nonverbal IQ and exhib- KEY WORDS: Visuospatial, Plasticity, Neurosurgery.
Neurosurgery is an accepted treatment for intractable (Bayard & Lassonde, 2001; Helmstaedter, 2004). Scores on partial epilepsy in pediatric and adult populations. It has attention and working memory, episodic memory tasks, and been proven effective, particularly for intractable temporal naming tests have been shown to improve (Gleissner et al., lobe epilepsy (Olivier, 1992; Wiebe et al., 2001; JambaquØ 2005; JambaquØ et al., 2007), allowing for higher scholastic et al., 2007; Kim et al., 2008). In children, surgery for extra- temporal lobe epilepsy represents approximately 50% of However, very few studies have measured the neuropsy- procedures and has been shown successful in one-half to chological outcomes for surgery in parietal and occipital two-thirds of the cases (Wyllie et al., 1998; Cossu et al., epilepsies (Smith & Billingsley, 2001). JambaquØ et al.
2008). The most frequent cause of surgically treated extra- (1998) reported visual apperceptive agnosia with severe temporal intractable epilepsy is cortical dysplasia, an early face recognition impairment, executive function deficits, developmental malformation of the cortex (Wyllie et al., and autistic symptoms in a 13-year-old girl who had under- 1998; Janszky et al., 2000; Lortie et al., 2002; Lerner et al., gone a right occipital lobectomy for cortical dysplasia at age 7 years. Remarkably, her academic abilities in spelling, A number of studies have reported that surgical treatment reading, and arithmetic were higher than her functional can improve cognitive prognosis in children with epilepsy intelligence level, perhaps as a result of special abilitiesoften encountered in patients with autism. Cohen et al.
(2004) demonstrated brain reorganization of the visual word Accepted April 29, 2010; Early View publication June 18, 2010.
form area (VWFA) toward the right hemisphere in a young Address correspondence to Sarah LippØ, PhD, Professeure Adjointe/ Assistant Professor, DØpartement de psychologie/Department of Psychol- epileptic child operated at the age of 4 years for a Sturge- ogy, UniversitØ de MontrØal/University of Montreal, C.P. 6128, Succursale Weber syndrome in the left occipitotemporal lobe. Sinclair Centre-Ville, MontrØal, QC, H3C 3J7 Canada. E-mail: sarah.lippe@ et al. (2005) reviewed the epileptic outcomes of nine children with parietal resections and six with occipital resections. Although cognitive outcome was not addressed, ª 2010 International League Against Epilepsy occipital lobe patients showed visual field losses. Focusing The project was approved by the Paediatric Neuro- on the possibility of generalized impairments, Gleissner surgery Committee of the Fondation Ophtalmologique de et al. (2008) assessed 15 children with parietal lobe epi- Rothschild. Both parents and children gave informed con- lepsy. One year after surgery, these children were seizure- sent. We reviewed preoperative and postoperative clinical free with postoperative improvements in attention and investigations, which included intracranial video-electroen- behavior, but they showed a decrease in performance intelli- cephalography (video-EEG), magnetic resonance imaging (MRI), and IQ findings from Wechsler or developmental In the present study, we assessed the long-term cognitive scales. Clinical information for each patient is detailed in outcome—from 3–7 years postsurgery—of occipitoparietal Table 1 and in the individual case descriptions.
epilepsy in five children who showed early onset due toTaylor-type focal cortical dysplasia. Neurosurgical resec- tion involved the occipital lobe and temporal or parietal lobe The follow-up period ranged from 3–7 years. All children junctions. Neuropsychological assessment specifically tar- underwent a neuroophthalmologic and comprehensive neu- geted the cognitive functions of the posterior regions of the ropsychological evaluation, designed to assess cognitive brain. Although the occipital lobe is mainly responsible for functions related to the posterior region of the brain. Verbal visual perception and discrimination, the parietal lobe is and nonverbal intellectual functions were evaluated preop- important for visuospatial orientation, attention, saccades, eratively and postoperatively on Wechsler or developmental numerical cognition, grapheme–phoneme transcoding, esti- scales (Table 2). Postoperatively, more extensive neuropsy- mating time and quantities, and praxis (Leff et al., 2001; chological and ophthalmologic evaluations were performed.
Hubbard et al., 2005; Pouthas et al., 2005; Cavanna & The neuroophthalmologic evaluation included visual acuity Trimble, 2006). Occipitotemporal areas are involved in and the Goldmann visual field examination. We used stan- color, object, and face recognition; reading; and other func- dardized tests to assess the following five subdomains of tions (Dehaene et al., 2001; Casarotto et al., 2008). In both nonverbal cognition: basic visual discrimination, visual children and adults, the impact of a lesion in the occipital attention, visual recognition, spatial perception, and praxis.
and parietal lobes can result in visual agnosia, neglect, vi- In addition, we evaluated working memory, executive func- suospatial disorientation, alexia, sensorial extinction, and tions, and academic skills such as reading and numerical Gerstmann syndrome (Laurent-Vannier et al., 2003). Given the early maturation of the posterior areas of the brain, we Screening tests from the Visual Object and Space Percep- predicted reduced recovery of visuospatial abilities as com- tion (VOSP) battery (Warrington & James, 1991) were used pared to language development. Within the posterior to assess the basic visual discrimination level of each child.
regions, we also hypothesized that lesion type and location We measured visual attention with cancellation tasks: the (right- or left-sided resection) would differentially impact NEPSY Visual Attention Task (Korkman et al., 1998) and cognitive function, given that the right and left hemispheres the Bell test from the Batterie d’Øvaluation de la nØgligence show distinct preferences for Gestalt versus analytical pro- unilatØrale du Geren (BEN) (Rousseaux et al., 2001). Sub- cessing (Van Kleeck & Kosslyn, 1989). We posited that tests for eye and head deviation, extinction, and line bisec- neurodevelopmental lesions, such as cortical dysplasia and tion were used from the Batterie to assess symptoms of early onset epilepsy, would entail reduced recovery of neglect. Visual recognition was tested through naming and visuoperceptual cognition compared to verbal function.
designation of objects (JambaquØ & Dellatolas, 2000), dis- Because the literature reports of long-term follow-up in crimination of overlapping and embedded figures (Ghent, children with postoperative occipitoparietal epilepsy are 1956), and recognition of degraded figures (Gestalt closure) scarce, our neuropsychological case descriptions from 3– (Kaufman & Kaufman, 1983). For facial recognition, we 7 years postsurgery focused on visuospatial abilities and used the short form of the Benton Facial Recognition Test scholastic skills such as reading and arithmetic.
We evaluated spatial perception using the NEPSY Arrows subtest (Korkman et al., 1998) and the Benton Judgement of Line Orientation Test (JLOT) (Benton, 1983a; Benton et al., 1983b), with children’s norms Eleven children with medically refractory epilepsy (Lindgren & Benton, 1980). To measure visuoconstructive underwent surgical resection of the posterior region of the abilities and praxis, we used the Rey Complex Figure Test brain at the Fondation Ophtalmologique Rothschild de Paris (Rey, 1959) and NEPSY Hand Movements and Visuomotor (France) between 1999 and 2007 (Figs S1 and S2). Children were selected based on age at surgery (£7 years of age), cur- Reading was assessed by subtests from two batteries: the rent age (between 8 and 12 years), and postoperative status Test de l'Alouette (Lefavrais, 1967) and the Outil de DØpi- (seizure-free or greatly improved). Five children fulfilled stage des Dyslexies (ODEDYS) (Neurocognition, 2002).
the inclusion criteria and agreed to participate in the study.
In both cases, accuracy and speed were measured.
Epilepsia, 51(10):2047–2057, 2010doi: 10.1111/j.1528-1167.2010.02651.x Outcome of Posterior Resection in Children ND, not done; VIQ, Verbal Intelligence Quotient; PIQ, Performance Intelligence Quotient.
aGlobal Developmental Quotient (French Gesell scale adaptation).
Numerical cognition was evaluated by the Zareki-R bat- a right hemisphere lesion. In four children, between 20 tery of scores (2006), which includes assessment of visual and more than 100 seizures were recorded during the counting, mental counting, number writing, number read- period of intracranial video-EEG monitoring, whereas ing, oral mental calculation, visual quantity estimation, and one patient, Patient 2, presented with only two seizures.
The preoperative IQ scores revealed a range from mild Visual span and working memory were tested with the deficit (Patient 1) to mental delay (Patients 3 and 5), and Wechsler Intelligence Scale for Children – Fourth Edition autistic features in one patient (Patient 4). All children (WISC-IV) Integrated Spatial Span subtest. Auditory atten- exhibited poor visual perception and recognition in every- tion and working memory were tested further by compari- day life. The posterior part of the occipitotemporal gyrus son to visual tasks, using the NEPSY Auditory Attention was included in the occipital and posterior parietal lobe and the WISC-IV Integrated Digit Span tests. Executive resections (Figs S1 and S2) in all participants but one function was assessed through the NEPSY Tower subtest, and behavior was evaluated on the Child Behaviour CheckList (CBCL) questionnaire (Achenbach, 1991) filled out by Postoperatively, all children improved their intellectual Standardized neuropsychological test scores were classi- abilities, but with significant differences between verbal fied into two categories, according to the mean and standard and nonverbal components (see Table 2 and detailed deviation (SD) of each test: 1.5 SD below the mean was description). Although all nonverbal IQs were abnormal qualified as a ‘‘deficit,’’ whereas 1.0 SD above or below the and three children had a verbal IQ below 80, two had verbal mean were qualified as ‘‘average.’’ With some exceptions, a IQs above 100. Parental rating of behavior (on the CBCL pathological threshold was used: for the Benton Facial Rec- questionnaire) was average for four of the five children.
ognition Test, this was more than two points from the mean Nevertheless, behavioral difficulties were observed during (Benton), and for the embedded figures task, two omissions our evaluations and are reported in the case descriptions.
(Ghent, 1956). For the scoring of the BEN subtests (Bell All participants displayed normal visual discrimination test, Eye and Head Deviation, Extinction and Line Bisec- (VOSP). However, all performed at least 1.5 SD below the tion), young adult norms were used as a guideline (Rous- mean on object naming (DEN-48), visuomotor praxis (hand seaux et al., 2001). Finally, T scores above 60 on the CBCL movements), and regular word reading (ODEDYS-time) questionnaire (Achenbach, 1991) were rated pathological.
tasks (Table 3). Four of the five children performed at least1.5 SD below the mean on visual attention tests (Bell andNEPSY), visual perceptual integration skills (degraded forms Kaufman Assessment Battery for Children [K-ABC]), embedded figure discrimination (Ghent), face recognition All five children experienced seizure onset in the early (Benton), visuospatial orientation (Benton JLOT and months of life, characterized by various types of clinical NEPSY Arrows), visuoconstructive praxis (Rey figure), ocular manifestations. The seizures were stereotypic par- visuomotor precision (NEPSY), and irregular word reading tial seizures beginning with a conjugate gaze deviation or and pseudo-word reading time (ODEDYS) (Table 1).
a strabismus followed by ocular clonus; one child (Patient On the other hand, only Patient 4 did not show normal 2) presented infantile spasms, which were well controlled auditory attention and planning abilities (NEPSY Auditory by Vigabatrin. MRI lesions were visible in the occipital Attention and NEPSY Tower, SD < )1.5). The two chil- lobe in all children (Patients 1–5) as well as in the parietal dren with normal verbal IQ (Patients 1 and 2) performed lobe in three (Patients 1–3) and in the temporoparietal above the mean on the planning task. Numerical abilities junction in one (Patient 4). Only one child, Patient 1, had such as number reading and writing, counting, and verbal Epilepsia, 51(10):2047–2057, 2010doi: 10.1111/j.1528-1167.2010.02651.x Outcome of Posterior Resection in Children showed visual attention deficits. On the line-bisection task, Table 3. Patients showing deficit or average score she exhibited left visual neglect, and was also impaired on object recognition, with poor visual perceptual integration performance on object naming and Gestalt closure tests.
The patient was highly impaired when face recognition involved lighting and angle variation between the target and responder, contrasting her perfect performance on identical Spatial perception was markedly impaired (Benton JLOT and the NEPSY Arrows task). On the copy of the Rey figure, she could not easily estimate shape dimensions or distance between elements. She showed also dyspraxia, with marked difficulty in imitating hand movement positions, and poor This patient was significantly slow at reading single words and text, and made more mistakes reading pseudo- words and regular words than irregular words. On the other hand, she was not significantly impaired on numerical cog- nition. She could count items, count backwards mentally, read and write numbers, do oral mental arithmetic (addition, subtraction, multiplication), and estimate visually and ver- Patient 2. Seizures were characterized by left eye and head deviations and ocular clonus, associated with infantile spasms and psychomotor regression one month after the ini- tial presentation. The preoperative neurologic examination showed mild axial hypotonia, poor socialization skills with impaired visual contact, if any, and an inability to catch objects. The right eye was affected with strabismus. After neurosurgery and introduction of low-dose carbamazepine, the patient showed amazing development of language andinteraction skills.
and visual estimation were within average range for four ofthe five children (exception, Patient 3).
At 8 years old, this boy showed right inferior quadranop- Case descriptions of participants with normal sia, hypermetropia, astigmatism, and strabismus. On hemi- neglect tasks, he showed extinction signs in the left ear, Patient 1. Experienced seizures at birth with ictal and whereas the line-bisection test was significantly skewed to interictal right occipital EEG activity. Seizures were charac- the right. On the Bell cancellation task, he omitted more terized by upward left elevations of the eye globes and stimuli in the left hemispace than the right. Furthermore, he ocular clonus. After the second neurosurgery, at age exhibited visual inattention with disorganized visual search- 5 years, the child became seizure-free without need for ing abilities. Object recognition was impaired and even medication, although upward left ocular movements were more so when the forms were degraded or embedded. On still present at random instances. The visual field test the Benton Facial Recognition Test, he was slow and made showed left hemianopsia. This girl was 9.7 years old at the mistakes on the matching of identical front-view photo- time of the neuropsychological evaluation.
The patient exhibited left hemianopsia with upward left Spatial perception was relatively preserved but the child was greatly impaired on visuomotor precision, calligraphy, explored her visual field mainly with her right eye and and the imitation of hand positions.
Reading assessment showed that word reading was slower than expected, but error rates were normal or better hypermetropia, and right hemianopsia. On cancellation than average. Furthermore, text reading performance was tasks, the patient omitted a large number of items on the left within normal range. The child showed normal numerical and right fields but was still able to explore the entire visual field. She showed extinction phenomena only in the tactilemodality. This girl is the only child in our sample displaying Case descriptions of participants with abnormal aural–verbal as well as visual attention deficits. Visuospa- tial memory and verbal working memory were both Patient 3. This patient was 19 months old at epilepsy impaired. Object recognition was altered (naming and des- onset. The EEG showed ictal and interictal left occipitopa- ignation), mainly for degraded forms and embedded figures.
rietal abnormal activity. At 5 years of age, this left-handed Object-naming errors were mainly semantic (e.g., gripper boy had permanent deviation of the right eye and tended not named as screwdriver). On the other hand, she could per- to sufficiently use the right side of his body. He exhibited fectly recognize front-view photographs of the face but was language delay but was characterized by evident visual very much impaired when skew and lighting conditions agnosia and dyspraxia. At 8 years 8 months of age, the patient still showed a lack of behavioral control.
The patient showed impaired visuospatial abilities on the Ophthalmologic examination showed a right eye devia- Benton JLOT and the NEPSY Arrows task. The copy of the tion, which was irregularly present. Assessed through can- Rey figure was segmented and she could not estimate the cellation tasks, he exhibited visual attention difficulties with dimensions of shapes or the distances between elements.
a similar number of omissions on each side of the hemi- The child exhibited marked impairment during hand move- space. In addition, he showed significant symptoms of ment and visuomotor precision tasks.
apperceptive agnosia. He could recognize identical figures,but object recognition, especially for degraded and embed- ded figures, was altered. He made mistakes on both semanti- This girl showed the greatest reading deficits of all the colexical (e.g., stairs for ladder) and visual (e.g., caterpillar participants, as she was significantly slow at reading single for snail) levels. On the Benton Facial Recognition Test, the words and text. Furthermore, the number of mistakes was child’s performance was also highly impaired.
similar whether she was reading regular words, irregularwords, or pseudo-words. She made visual, phonologic, and regularization mistakes. On the other hand, she was not sig- Visuospatial orientation abilities as well as constructive nificantly impaired on numerical cognition. She could count items, read and write numbers, and estimate verbally con-textualized quantities. However, the visual quantities esti- mation task was riddled with attention difficulties; in fact, Reading abilities were relatively preserved for text. The this patient showed hyperactivity and lack of behavioral boy showed only a 1-year lag in reading speed for regular, irregular, and pseudo-words. Unlike other children in our Patient 5. Preoperatively, the EEG revealed ictal and inte- sample, he was significantly impaired on numerical cogni- rictal left parietooccipital abnormal activity. Seizures tion, although, especially number reading and writing.
occurred with left upward eye movements and ocular clo- Many mistakes were visuospatial, for example, reading 305 nus. At the age of 2 years, the child had mild psychomotor as 135, but other errors involved a misrepresentation of delay and interacted poorly with his mother. Behavioral dif- numerical knowledge (reading 138 as one thirteen eight; ficulties related to food, with signs of anorexia. Two neuro- reading 6,485 as 74,895). Visual and verbal contextual esti- surgeries were needed to obtain freedom from seizures. The mation abilities, however, were normal.
boy was 10 years and 8 months old at the time of the neuro- Patient 4. The first neurologic examination found psycho- motor delay and abnormal eye movements. Seizuresoccurred with upward right elevations of the eye globes and body, and the EEG showed ictal and interictal left occipital The ophthalmologic examination showed right hemia- activity. Postoperative MRI revealed blurring of the white– nopsia, but the patient compensated well. Although he gray matter junction over the left posterior temporal lobe, showed right visual extinction when stimulated bilaterally, which extended anteriorly to the resection. The patient was he had a lesser level of visual attention deficit than the other 11 years of age at the time of the neuropsychological evalu- children in the sample. Visuospatial working memory was within average. However, this boy could not name objects Epilepsia, 51(10):2047–2057, 2010doi: 10.1111/j.1528-1167.2010.02651.x Outcome of Posterior Resection in Children properly despite preserved visual perceptual integration neglect syndrome, an attention deficit disorder that causes abilities. He could recognize front-view photographs of patients to demonstrate pathologic bias for ipsilesional faces, but was impaired when lighting and skew varied items, neglecting the contralateral ones (Mattingley et al., between the target and the responder.
1997). The one child with a right-sided lesion (Patient 1)was the most impaired on spatial attention and showed signs of neglect. Our observations are consistent with those of The patient showed well-preserved visuospatial orienta- recent studies reporting that the right temporoparietal junc- tion abilities but poor spatial construction abilities. He also tion, part of which had been resected in Patient 1, is related was affected with dyspraxia, poor imitation of hand posi- to the network involved in reorienting behaviors following attentional capture by other stimuli (Corbetta & Shulman,2002; Mitchell, 2008). In addition, neglect has recently been described in children with left and right parietal acquired This patient was one of the most impaired in reading lesions (Laurent-Vannier et al., 2003). In our sample, only skills, being significantly slow at single words and text.
Patient 1 with a right occipitoparietal lesion showed neglect Errors were made while reading pseudo-words, regular of the contralateral hemispace. With regard to developmen- words, and irregular words, making visual mistakes 28% of tal lesions, our results do not confirm the previously prevail- the time. On the other hand, numerical cognition tasks were ing hypothesis of more frequent spatial neglect of the right easily performed. Assessed by NEPSY tests, auditory atten- hemispace in very young children (Laurent-Vannier et al., tion was within average, but digit span and verbal working Most children were impaired on degraded object recogni- tion or object naming. Object recognition is known toinvolve the lateral occipital and the fusiform cortex bilater- ally (Eger et al., 2004, 2007; Pegna et al., 2004) and to be All children experienced seizure onset before 2 years of modulated by top-down processes by the frontoparietal net- age. After surgery, three children were seizure-free and off work. Children were unable to recognize or name an object medication, whereas the remaining two showed infrequent without contextual cues, which suggests that recovered seizure reoccurrence and received one antiepileptic drug.
brain processes related to seizure freedom and/or brain plas- Four of five children attained normal schooling level. Ver- ticity failed to completely compensate for the unilateral pos- bal IQ was improved by up to 35 points after the surgery. As terior lesions. Interestingly, the one child who could in children with Sturge-Weber syndrome with drug-resistant accurately identify degraded objects had the lateral occipital epilepsy, the control of epilepsy and reduction of pharmaco- cortex (LOC) preserved out of his left lesion (Patient 5), therapy may have prevented severe cognitive impairments whereas the analogous LOC-sparing surgery in a right hemi- (Sujansky & Conradi, 1995). Three to seven years postoper- sphere lesion still impaired the child on the same task atively, all children showed significant discrepancies (Patient 1). The right hemisphere is typically associated between verbal and nonverbal IQs. Although two of five with spatial transformation of a mental Gestalt, a process children displayed normal verbal IQ, all were moderately likely to be involved in degraded object recognition tasks impaired on nonverbal IQ. Our observations are in concor- (Warrington & James, 1991; Humphreys et al., 1992). Our dance with the significant postsurgery difference between observations, therefore, confirm the bilateral LOC role in verbal and nonverbal IQ reported in adults with posterior resections, regardless of side of surgery or visual field loss Facial recognition, tested using the Benton Facial Recog- nition Test, was impaired in four of the five children. The Our neuropsychological evaluation suggests that a history task is separated into two parts. Only the first part does not of early severe epilepsy with a focal cortical dysplasia fol- require visuospatial skills, as it shows front-view photo- lowed by surgical resection will have an impact on the cor- graphs; the second part shows the angles and lighting in a responding visual, spatial, and academic cognitive abilities.
different view. The lesions and cognitive difficulties experi- All five children showed cognitive deficits related to visual enced by the subject are reflected in corresponding deficits attention, object recognition, praxis, and reading speed.
on the first or second part of the task. For example, the onlychild showing normal performance on orientation tasks (a patient with a small lateral resection in the left hemisphere), The posterior parietal lobe is considered to have a special made mistakes on the first section but very few on the sec- role in spatial functions (Nachev & Husain, 2006). Indeed, ond. In contrast, the most impaired child on orientation visual spatial attention was impaired in all five children.
tasks, with a median right hemisphere resection, showed a Subregions such as the temporoparietal junctions are perfect performance on the first part, but a worse perfor- involved in the spatial attention network (Mesulam, 1981; mance on the second part of the test. Other reports on facial Vallar et al., 1993). They are strongly associated with perception have revealed limited postlesional plasticity in the pediatric population resulting from both right and left preserved left fusiform gyrus. Cohen et al. (2004) reported lesions (Mancini et al., 1994; de Schonen et al., 2005). Our hemispheric shift for reading but not for language in a child study supports the heterogeneity of the mechanisms related of preschool age at the time of left occipital resection. In to developmental prosopagnosia (Duchaine & Nakayama, Patient 4, the large left hemispheric dysplasia, the early resection (6 years of age), and early seizure freedom andreduction of pharmacotherapy could have resulted in brain reorganization toward the right hemisphere allowing for a All children showed dyspraxia, ranging from movement certain level of reading. In all cases, it is possible that visual imitations to constructions. Movement imitation is thought field loss may have altered the saccade movements, causing to involve a complex network in the frontal and parietal a reduction in reading speed. Inefficient fixation during regions (Iacoboni et al., 1999; Shmuelof & Zohary, 2007).
reading has been described in hemianoptic patients Authors have proposed that the anterior intraparietal area is 6 months after the acquired lesion (McDonald, 2006).
involved in a kinesthetic copy of the movements to be used Although it should be considered for the two least impaired during action execution (Iacoboni et al., 1999), whereas the children, who mainly showed alteration in reading speed inferior parietal lobule is associated with body schema instead of accuracy, this alternative explanation cannot hold knowledge (Berlucchi & Aglioti, 1997). Although the ante- true in the most impaired children because both accuracy rior intraparietal area was not altered in most of our chil- dren, the epilepsy and the resections, with the inferior Although the impact of developmental lesions and neuro- parietal lobe partially resected in most children, must have surgery did not create alexia in any of the children, it did produced a disconnect in the neural network that prevented impair all of them on word reading speed. Parietal regions them from performing accurate gesture imitations. As of the brain are involved in spatial attention processes, ori- expected, visuomotor precision and complex figure copying enting and decoding letters and words, and consequently in were impaired, being associated with a number of brain early learning of lexical functions. Epelbaum et al. (2008) areas in the frontal, parietal, and occipital lobes bilaterally, showed that disconnecting the occipital cortex from the such as the cuneus (Tzagarakis et al., 2009), which had been VWFA (by altering the inferior longitudinal fasciculus) was resected in most children in our sample.
sufficient to provoke reading deficits. Therefore, it wouldseem that up to 7 years postsurgery, a right or left posteriorlesion of the extent seen in our subjects prevents the child from performing at normal reading capacity at school age, but does not prevent the individual from learning how to All children were impaired with regard to reading speed.
Reading is a complex task involving an extended network.
Word recognition has recently been strongly associated with the ventral stream, where a functional specialization for Numerical cognition refers to processes such as subitiz- recurrent spelling patterns was found in the left occipitotem- ing (estimation for quantities lower than four), estimating, poral sulcus, named the visual word form area (VWFA) counting, calculating, and comparing quantities or numbers.
(Cohen et al., 2003; Marinkovic et al., 2003; McCandliss Studies have demonstrated the role of a frontoparietal net- et al., 2003; Binder et al., 2006; Gaillard et al., 2006). The work for numerical cognition (Roland & Friberg, 1985; dorsal stream is thought to be involved in word recognition, Dehaene et al., 1996). Within this network, the intraparietal when serial reading ensues from degraded special properties sulcus regions, bilaterally, are specifically involved in most of words or spatial rearrangement of letters (Gitelman et al., numerical cognition processes. In children, comparison 2005; Vinckier et al., 2006; Cohen et al., 2008). Graph- tasks of Arabic numerals and color nonnumerical symbols eme–phoneme conversion and semantic processing of induced bilateral intraparietal sulcus activity in normal chil- words involve left temporal and frontal regions of the brain dren but not in children showing developmental dyscalculia (Simos et al., 2002; Mechelli et al., 2005).
(Mussolin et al., 2010). Only one child in our sample was The two most impaired children had lesions spread over impaired on numerical cognition, the one in whom the the left ventral stream (Patients 3 and 5). Patient 3 had an largest part of the superior parietal lobule was resected extensive left dysplasia and Patient 5 had a resection of the (Patient 3). The child showed deficits in number reading, left fusiform gyrus (including the VWFA) at 7 years of age.
number writing, and dot counting. He did not show deficits Indeed, plasticity may have been limited in Patient 5 by vir- on visual estimation, whereas the one child demonstrating tue of age and the fact that he had acquired a level of reading difficulties on the estimation tasks had an occipitotemporal expertise before the surgery. The two children with the least lesion (Patient 4). A plausible explanation is that the estima- impaired reading speed had very distinct lesions. Patient 4 tion task was modulated by spatial working memory had extensive left dysplasia combined with a resected fusi- (Culham & Kanwisher, 2001), which was altered in the form gyrus, whereas Patient 2 had a small neurosurgery with latter (Patient 4) but not the former (Patient 3).
Epilepsia, 51(10):2047–2057, 2010doi: 10.1111/j.1528-1167.2010.02651.x Outcome of Posterior Resection in Children Patient 1, the only child with a right occipitoparietalresection, was the most impaired as concerns visual atten- tion, visuospatial orientation, simultagnosia, and visuospa- Our sample allowed us to directly compare two chil- tial construction abilities. In contrast, Patient 5, with a dren with very early epilepsy onset and lesions of the very similar resection of the left occipitoparietal region, occipital-temporoparietal region, one in the left hemi- showed the least visual attention and visuospatial working sphere (Patient 5) and one in the right (Patient 1). Both memory difficulties, but was the most impaired on read- children were impaired as to reading, but showed a double ing. Finally, the only patient in whom the resection dissociation in two aspects. First, although Patient 5 was involved the left occipital-temporoparietal region (Patient significantly impaired on irregular word reading, Patient 1 3), including the superior parietal lobe, was the only one showed normal performance. The lexicosemantic path to show numerical cognition impairments and had rela- necessary for irregular word reading is thought to involve the anterior part of the inferior frontal gyrus and of the From our small series, we can only convey that a number fusiform gyrus (Mechelli et al., 2005), which had been of variables including dysplasia size, resection size, and resected in Patient 5 but not in Patient 1. Lesioned in the location are important in predicting verbal and nonverbal left hemisphere, Patient 5 was greatly impaired in lexical cognitive outcomes. However, given that verbal IQ knowledge. In contrast, Patient 1 was able to directly read improvements occurred after surgery, we can ascertain a with the left hemisphere, where lexical knowledge is well beneficial role for seizure freedom and antiepileptic drug developed. Second, although Patient 1 showed significant reduction in verbal brain processing. The mechanisms pseudo-word reading errors, Patient 5 had normal perfor- responsible for the visuospatial outcomes remain unclear.
mance. Words are first processed within each hemisphere Whereas performance IQ did not significantly change after in the V4 area and then transferred through the corpus the surgery, the level of competence of each child is still callosum to the left hemisphere, in the VWFA, around the striking when one considers the lesion sizes in some of the temporooccipital sulcus (Cohen et al., 2000). Pseudo-word children. Possible recovery factors in visuospatial tasks may reading may further involve the dorsal premotor cortex include distinct cognitive strategies, brain reorganization, (Mechelli et al., 2005). Our results suggest that pseudo- and normalized brain activity resulting from seizure free- word reading may in fact involve other networks, including the right hemisphere. Both the right and left One limitation of this study includes the fact that the more hemisphere fusiform gyri process newly presented words extensive neuropsychological evaluation was conducted (Dehaene et al., 2001), and the posterior fusiform area has only postoperatively. This limitation comes from the young been shown to correlate with the frontal region involved age of the patients included in this study. For future work, in pseudo-word reading (dorsal premotor cortex) (Mechelli more comprehensive preoperative assessment could help in et al., 2005). We posit a right hemisphere contribution in better characterizing their improvements or worsening after the early detection of pseudo-words that could mimic serial reading processes known to activate biparietal In conclusion, early surgical intervention in children with regions (Vinckier et al., 2006; Cohen et al., 2008).
posterior intractable epilepsies offers the possibility of opti- In summary, our sample was too small to quantify cog- mizing cognitive outcome and quality of life. We believe nitive outcome with respect to dysplastic tissue, localiza- that, in future, more attention should be paid to neuropsy- tion, resection size, time of surgery, seizure freedom, and chological assessment of these patients to better understand pharmacotherapy reduction. However, the visuospatial their visual perceptive deficiencies and provide better clini- impairment profile of our sample can be related to the neuroanatomic framework. We observed that the one child(Patient 2) showing the highest nonverbal IQ score wasalso the one with the smallest dysplastic tissue as visual- ized on MRI, had the least amount of resection, and was This work was supported by the Canadian Institutes of Health operated on at the youngest age. Indeed, this patient Research (Lippe S) and UnitØ de Neurochirurgie PØdiatrique, Fondation showed a very good outcome considering the classic long- Ophtalmologique A. de Rothschild, Paris, France Inserm UMR663. Epi- term prognosis of infantile spasms (JambaquØ et al., lepsies de l’enfant et plasticitØ cØrØbrale, UniversitØ Paris Descartes,Paris, France.
1993). Furthermore, the child showing the worst overallresults (Patient 4), including deficits in oral–verbal atten-tion, also showed the most extended dysplasia, involving the left temporal lobe. The other four patients may also We confirm that we have read the journal’s position on issues show residual nonepileptogenic dysplastic tissue not obvi- involved in ethical publication and affirm that this report is consistent ous on MRI. In these cases, the dysplastic tissue may or with those guidelines. None of the authors has any conflict of interest to may not be cognitively functional (Janszky et al., 2000).
Ghent L. (1956) Perception of overlapping and embedded figures by chil- dren of different ages. Am J Psychol 69:575–587.
Gitelman DR, Nobre AC, Sonty S, Parrish TB, Mesulam MM. (2005) Lan- Achenbach T. (1991) Manual for the child behavior checklist/4–18 guage network specializations: an analysis with parallel task designs and 1991 profile. Department of Psychiatry, University of Vermont, and functional magnetic resonance imaging. Neuroimage 26:975–985.
Gleissner U, Sassen R, Schramm J, Elger CE, Helmstaedter C. (2005) Bayard S, Lassonde M. (2001) Cognitive, sensory and motor adjustment to Greater functional recovery after temporal lobe epilepsy surgery in chil- hemispherectomy. In JambaquØ I, Lassonde M, Dulac O (Eds) Neuro- psychology of childhood epilepsy. Kluwer Academic/Plenum Publish- Gleissner U, Kuczaty S, Clusmann H, Elger CE, Helmstaedter C. (2008) Neuropsychological results in pediatric patients with epilepsy surgery Benton A. (1983a) Facial recognition. Les Editions du Centre de Psycholo- in the parietal cortex. Epilepsia 49:700–704.
Helmstaedter C. (2004) Neuropsychological aspects of epilepsy surgery.
Benton A, Hamsher K, Varney NR, Spreen O. (1983b) Judgment line orien- Epilepsy Behav 5(suppl 1):S45–S55.
tation form H. Contribution to neuropsychological assessment. Oxford Hubbard EM, Piazza M, Pinel P, Dehaene S. (2005) Interactions between number and space in parietal cortex. Nat Rev Neurosci 6:435–448.
Berlucchi G, Aglioti S. (1997) The body in the brain: neural bases of corpo- Humphreys GW, Riddoch MJ, Quinlan PT, Price CJ, Donnelly N. (1992) real awareness. Trends Neurosci 20:560–564.
Parallel pattern processing and visual agnosia. Can J Psychol 46:377– Binder JR, Medler DA, Westbury CF, Liebenthal E, Buchanan L. (2006) Tuning of the human left fusiform gyrus to sublexical orthographic Iacoboni M, Woods RP, Brass M, Bekkering H, Mazziotta JC, Rizzolatti G.
(1999) Cortical mechanisms of human imitation. Science 286:2526– Casarotto S, Bianchi AM, Ricciardi E, Gentili C, Vanello N, Guazzelli M, Pietrini P, Chiarenza GA, Cerutti S. (2008) Spatiotemporal dynamics of JambaquØ I, Chiron C, Dulac O, Raynaud C, Syrota P. (1993) Visual inat- single-letter reading: a combined ERP-FMRI study. Arch Ital Biol tention in West syndrome: a neuropsychological and neurofunctional imaging study. Epilepsia 34:692–700.
Cavanna AE, Trimble MR. (2006) The precuneus: a review of its functional JambaquØ I, Mottron L, Ponsot G, Chiron C. (1998) Autism and visual anatomy and behavioural correlates. Brain 129:564–583.
agnosia in a child with right occipital lobectomy. J Neurol Neurosurg Cohen L, Dehaene S, Naccache L, Lehericy S, Dehaene-Lambertz G, Henaff MA, Michel F. (2000) The visual word form area: spatial and JambaquØ I, Dellatolas G. (2000) Epreuves de fluence verbale et de dØnom- temporal characterization of an initial stage of reading in normal ination chez l’enfant d’âge scolaire. ANAE 56:13–16.
subjects and posterior split-brain patients. Brain 123(Pt 2):291–307.
JambaquØ I, Dellatolas G, Fohlen M, Bulteau C, Watier L, Dorfmuller G, Cohen L, Martinaud O, Lemer C, Lehericy S, Samson Y, Obadia M, Sla- Chiron C, Delalande O. (2007) Memory functions following surgery for chevsky A, Dehaene S. (2003) Visual word recognition in the left and temporal lobe epilepsy in children. Neuropsychologia 45:2850–2862.
right hemispheres: anatomical and functional correlates of peripheral Janszky J, Jokeit H, Schulz R, Hoppe M, Ebner A. (2000) EEG predicts sur- alexias. Cereb Cortex 13:1313–1333.
gical outcome in lesional frontal lobe epilepsy. Neurology 54:1470– Cohen L, Lehericy S, Henry C, Bourgeois M, Larroque C, Sainte-Rose C, Dehaene S, Hertz-Pannier L. (2004) Learning to read without a left Kaufman AS, Kaufman NL. (1983) Kaufman Assessment Battery for Chil- occipital lobe: right-hemispheric shift of visual word form area. Ann dren (K-ABC). American Guidance Service[Adaptation franÅaise: Bat- terie pour l’examen psychologique de l’enfant.] 1993. Editions du CPA, Cohen L, Dehaene S, Vinckier F, Jobert A, Montavont A. (2008) Reading normal and degraded words: contribution of the dorsal and ventral Kim SK, Wang KC, Hwang YS, Kim KJ, Chae JH, Kim IO, Cho BK.
visual pathways. Neuroimage 40:353–366.
(2008) Epilepsy surgery in children: outcomes and complications. J Corbetta M, Shulman GL. (2002) Control of goal-directed and stimulus-dri- ven attention in the brain. Nat Rev Neurosci 3:201–215.
Korkman M, Kirk U, Kemp S. (1998) NEPSY: a developmental neuropsy- Cossu M, Lo Russo G, Francione S, Mai R, Nobili L, Sartori I, Tassi L, Cit- chological assessment. The Psychological Corporation, San Antonio, terio A, Colombo N, Bramerio M, Galli C, Castana L, Cardinale F.
(2008) Epilepsy surgery in children: results and predictors of outcome Laurent-Vannier A, Pradat-Diehl P, Chevignard M, Abada G, De Agostini M. (2003) Spatial and motor neglect in children. Neurology 60:202– Culham JC, Kanwisher NG. (2001) Neuroimaging of cognitive functions in human parietal cortex. Curr Opin Neurobiol 11:157–163.
Lefavrais P. (1967) Test de l'Alouette. Les Øditions du Centre de Psycholo- Dehaene S, Tzourio N, Frak V, Raynaud L, Cohen L, Mehler J, Mazoyer B.
(1996) Cerebral activations during number multiplication and compari- Leff AP, Scott SK, Rothwell JC, Wise RJ. (2001) The planning and guiding son: a PET study. Neuropsychologia 34:1097–1106.
of reading saccades: a repetitive transcranial magnetic stimulation Dehaene S, Naccache L, Cohen L, Bihan DL, Mangin JF, Poline JB, Riviere D. (2001) Cerebral mechanisms of word masking and unconscious rep- Lerner JT, Salamon N, Hauptman JS, Velasco TR, Hemb M, Wu JY, San- etition priming. Nat Neurosci 4:752–758.
kar R, Donald Shields W, Engel J Jr, Fried I, Cepeda C, Andre VM, de Schonen S, Mancini J, Camps R, Maes E, Laurent A. (2005) Early brain Levine MS, Miyata H, Yong WH, Vinters HV, Mathern GW. (2009) lesions and face-processing development. Dev Psychobiol 46:184–208.
Assessment and surgical outcomes for mild type I and severe type II Duchaine BC, Nakayama K. (2006) Developmental prosopagnosia: a win- cortical dysplasia: a critical review and the UCLA experience. Epilep- dow to content-specific face processing. Curr Opin Neurobiol 16:166– Lindgren SD, Benton AL. (1980) Developmental patterns of visuospatial Eger E, Henson RN, Driver J, Dolan RJ. (2004) BOLD repetition decreases judgment. J Pediatr Psychol 5:217–225.
in object-responsive ventral visual areas depend on spatial attention. J Lortie A, Plouin P, Chiron C, Delalande O, Dulac O. (2002) Characteristics of epilepsy in focal cortical dysplasia in infancy. Epilepsy Res 51:133– Eger E, Henson RN, Driver J, Dolan RJ. (2007) Mechanisms of top-down facilitation in perception of visual objects studied by FMRI. Cereb Cor- Luerding R, Boesebeck F, Ebner A. (2004) Cognitive changes after epi- lepsy surgery in the posterior cortex. J Neurol Neurosurg Psychiatry Epelbaum S, Pinel P, Gaillard R, Delmaire C, Perrin M, Dupont S, Dehaene S, Cohen L. (2008) Pure alexia as a disconnection syndrome: new diffu- Mancini J, de Schonen S, Deruelle C, Massoulier A. (1994) Face recogni- sion imaging evidence for an old concept. Cortex 44:962–974.
tion in children with early right or left brain damage. Dev Med Child Gaillard R, Naccache L, Pinel P, Clemenceau S, Volle E, Hasboun D, Dupont S, Baulac M, Dehaene S, Adam C, Cohen L. (2006) Direct Marinkovic K, Dhond RP, Dale AM, Glessner M, Carr V, Halgren E.
intracranial, FMRI, and lesion evidence for the causal role of left infero- (2003) Spatiotemporal dynamics of modality-specific and supramodal temporal cortex in reading. Neuron 50:191–204.
word processing. Neuron 38:487–497.
Epilepsia, 51(10):2047–2057, 2010doi: 10.1111/j.1528-1167.2010.02651.x Outcome of Posterior Resection in Children Mattingley JB, Driver J, Beschin N, Robertson IH. (1997) Attentional com- Sinclair DB, Wheatley M, Snyder T, Gross D, Ahmed N. (2005) Posterior petition between modalities: extinction between touch and vision after resection for childhood epilepsy. Pediatr Neurol 32:257–263.
right hemisphere damage. Neuropsychologia 35:867–880.
Smith M, Billingsley RL. (2001) Neuropsychology of parieto-occipital McCandliss BD, Cohen L, Dehaene S. (2003) The visual word form area: epilepsy. In JambaquØ I, Lassonde M, Dulac O (Eds) Neuropsychology expertise for reading in the fusiform gyrus. Trends Cogn Sci 7:293– of childhood epilepsy. Kluwer Academic/Plenum Publishers, New McDonald SA. (2006) Parafoveal preview benefit in reading is only Sujansky E, Conradi S. (1995) Outcome of Sturge-Weber syndrome in 52 obtained from the saccade goal. Vision Res 46:4416–4424.
Mechelli A, Crinion JT, Long S, Friston KJ, Lambon Ralph MA, Trauner DA. (2003) Hemispatial neglect in young children with early uni- Patterson K, McClelland JL, Price CJ. (2005) Dissociating reading lateral brain damage. Dev Med Child Neurol 45:160–166.
processes on the basis of neuronal interactions. J Cogn Neurosci Tzagarakis C, Jerde TA, Lewis SM, Ugurbil K, Georgopoulos AP. (2009) Cerebral cortical mechanisms of copying geometrical shapes: a multidi- Mesulam MM. (1981) A cortical network for directed attention and unilat- mensional scaling analysis of fMRI patterns of activation. Exp Brain eral neglect. Ann Neurol 10:309–325.
Mitchell JP. (2008) Activity in right temporo-parietal junction is not selec- Vallar G, Antonucci G, Guariglia C, Pizzamiglio L. (1993) Deficits of posi- tive for theory-of-mind. Cereb Cortex 18:262–271.
tion sense, unilateral neglect and optokinetic stimulation. Neuropsycho- Mussolin C, De Volder A, Grandin C, Schlogel X, Nassogne MC, Noel MP.
(2010) Neural correlates of symbolic number comparison in develop- Van Kleeck MH, Kosslyn SM. (1989) Gestalt laws of perceptual organiza- mental dyscalculia. J Cogn Neurosci 22:860–874.
tion in an embedded figures task: evidence for hemispheric specializa- Nachev P, Husain M. (2006) Disorders of visual attention and the posterior tion. Neuropsychologia 27:1179–1186.
parietal cortex. Cortex 42:766–773.
Vinckier F, Naccache L, Papeix C, Forget J, Hahn-Barma V, Dehaene S, Neurocognition LC-saLdPe. (2002) ODESYS Outil de DØpistage de la Cohen L. (2006) ‘‘What’’ and ‘‘where’’ in word reading: ventral coding Dyslexie. UIFM de Grenoble, Grenoble.
of written words revealed by parietal atrophy. J Cogn Neurosci Olivier A. (1992) Temporal resections in the surgical treatment of epilepsy.
Warrington EK, James M. (1991) A new test of object decision: 2D silhou- Pegna AJ, Khateb A, Michel CM, Landis T. (2004) Visual recognition of ettes featuring a minimal view. Cortex 27:370–383.
faces, objects, and words using degraded stimuli: where and when it Wiebe S, Blume WT, Girvin JP, Eliasziw M. (2001) A randomized, con- occurs. Hum Brain Mapp 22:300–311.
trolled trial of surgery for temporal-lobe epilepsy. N Engl J Med Pouthas V, George N, Poline JB, Pfeuty M, Vandemoorteele PF, Hugue- ville L, Ferrandez AM, Lehericy S, Lebihan D, Renault B. (2005) Neu- Wyllie E, Comair YG, Kotagal P, Bulacio J, Bingaman W, Ruggieri P.
ral network involved in time perception: an fMRI study comparing long (1998) Seizure outcome after epilepsy surgery in children and adoles- and short interval estimation. Hum Brain Mapp 25:433–441.
Rey A. (1959) Test de copie d'une figure complexe. Les Øditions du Centre Roland PE, Friberg L. (1985) Localization of cortical areas activated by thinking. J Neurophysiol 53:1219–1243.
Rousseaux M, Beis JM, Pradat-Diehl P, Martin Y, Bartolomeo P, Additional Supporting Information may be found in the Bernati T, Chokron SM, Leclercq M, Louis-Dreyfus A, Marchal F, Perennou DC, Prairial C, Rode G, Samuel C, Sieroff E, WiartL, Azouvi P. (2001) PrØsentation d’une batterie de dØpistage de la Figure S1. Postsurgery MRI of Patient 2.
nØgligence spatiale. Normes et effets de l’âge, du niveau d’Øducation, Figure S2. Postsurgery MRI of Patient 5.
du sexe, de la main et de la latØralitØ. Rev Neurol (Paris) 157:1385– Please note: Wiley-Blackwell is not responsible for the Shmuelof L, Zohary E. (2007) Watching others’ actions: mirror representa- content or functionality of any supporting information sup- tions in the parietal cortex. Neuroscientist 13:667–672.
plied by the authors. Any queries (other than missing mate- Simos PG, Breier JI, Fletcher JM, Foorman BR, Castillo EM, Papanicolaou rial) should be directed to the corresponding author for the AC. (2002) Brain mechanisms for reading words and pseudowords: anintegrated approach. Cereb Cortex 12:297–305.

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