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A preliminary study of the different memory systems in neurofibromatosis type 1: What is impaired and what is spared?

      Abstract

      Background

      Since 1990's, the cognitive profile of children with a neurofibromatosis type 1 (NF1) has been refined by many different studies. Children with NF1 may exhibit a variety of cognitive dysfunctions. Memory difficulties have been reported, but the results are contradictory and, compared to other cognitive functions, memory has been less evaluated.

      Objective

      The aim of this study was to investigate the memory profile in NF1 with a particular population, children with NF1 without attention deficit hyperactivity disorder (ADHD).

      Methods

      Eighteen children with NF1 without ADHD and eighteen typically developing aged from 8 to 12.6 years were compared in terms of both their verbal and visual working memory, anterograde memory, and procedural perceptual-motor memory. We also assessed semantic and autobiographical memory.

      Results

      Our results indicate the existence of memory difficulties in children with NF1 without ADHD in verbal working and anterograde memory but not in terms of the visual domain. They also experienced difficulties recalling personal memories but these were improved by cueing. However, semantic memory and procedural perceptual-motor memory was preserved.

      Conclusions

      These results highlight a difference between memory systems in children with NF1 without ADHD and the importance to assess the different memory systems, the nature of information and the processes in long-term memory in NF1 population. However, our results raise questions about the possible links between these difficulties and the executive functions. The specifics of memory profile in children with NF1 must be taken into consideration in these children’s clinical follow-up, in order to understand their learning difficulties and to make adaptations to their care.

      Keywords

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      References

        • Evans D.G.
        • Howard E.
        • Giblin C.
        • Clancy T.
        • Spencer H.
        • Huson S.M.
        • et al.
        Birth incidence and prevalence of tumor-prone syndromes: Estimates from a UK family genetic register service.
        Am J Med Genet Part A. 2010; 152A: 327-332
        • Hyman S.L.
        • Shores A.
        • North K.N.
        The nature and frequency of cognitive deficits in children with neurofibromatosis type 1.
        Neurology. 2005; 65: 1037-1044
        • Krab L.C.
        • Oostenbrink R.
        • de Goede-Bolder A.
        • Aarsen F.K.
        • Elgersma Y.
        • Moll H.A.
        Health-related quality of life in children with neurofibromatosis type 1: contribution of demographic factors, disease-related factors, and behavior.
        J Pediatr. 2009; 154: 420-425
        • Wessel L.E.
        • Gao F.
        • Gutmann D.H.
        • Dunn C.M.
        Longitudinal Analysis of Developmental Delays in Children with Neurofibromatosis Type 1.
        J Child Neurol. 2013; 28: 1689-1693
        • Hyman S.L.
        • Shores A.E.
        • North K.N.
        Learning disabilities in children with neurofibromatosis type 1: subtypes, cognitive profile, and attention-deficit-hyperactivity disorder.
        Dev Med Child Neurol. 2006; 48: 973-977
        • Krab L.C.
        • Aarsen F.K.
        • de Goede-Bolder A.
        • Catsman-Berrevoets C.E.
        • Arts W.F.
        • Moll H.A.
        • et al.
        Impact of Neurofibromatosis Type 1 on School Performance.
        J Child Neurol. 2008; 23: 1002-1010
        • Cutting L.E.
        • Clements A.M.
        • Lightman A.D.
        • Yerby-Hammack P.D.
        • Denckla M.B.
        Cognitive Profile of Neurofibromatosis Type 1: Rethinking Nonverbal Learning Disabilities.
        Learn Disabil Res Pract. 2004; 19: 155-165
        • Torres Nupan M.M.
        • Velez Van Meerbeke A.
        • López Cabra C.A.
        • Herrera Gomez P.M.
        Cognitive and Behavioral Disorders in Children with Neurofibromatosis Type 1.
        Front Pediatr. 2017; 5: 227
        • Lehtonen A.
        • Howie E.
        • Trump D.
        • Huson S.M.
        Behaviour in children with neurofibromatosis type 1: cognition, executive function, attention, emotion, and social competence.
        Dev Med Child Neurol. 2013; 55: 111-125
        • Watt S.E.
        • Shores E.A.
        • North K.N.
        An Examination of Lexical and Sublexical Reading Skills in Children with Neurofibromatosis Type 1.
        Child Neuropsychol. 2008; 14: 401-418
        • Chaix Y.
        • Lauwers-Cancès V.
        • Faure-Marie N.
        • Gentil C.
        • Lelong S.
        • Schweitzer E.
        • et al.
        Deficit in phonological processes: a characteristic of the neuropsychological profile of children with NF1.
        Child Neuropsychol. 2018; 24: 558-574
        • Hachon C.
        • Iannuzzi S.
        • Chaix Y.
        Behavioural and cognitive phenotypes in children with neurofibromatosis type 1 (NF1): the link with the neurobiological level.
        Brain and Development. 2011; 33: 52-61
        • Descheemaeker M.J.
        • Ghesquière P.
        • Symons H.
        • Fryns J.P.
        • Legius E.
        Behavioural, academic and neuropsychological profile of normally gifted Neurofibromatosis type 1 children.
        J Intellect Disabil Res. 2005; 49: 33-46
        • Roy A.
        • Roulin J.
        • Charbonnier V.
        • Allain P.
        • Fasotti L.
        • Barbarot S.
        • et al.
        Executive dysfunction in children with neurofibromatosis type 1: A study of action planning.
        J Int Neuropsychol Soc. 2010; 16: 1056-1063
        • North K.
        • Hyman S.
        • Barton B.
        Cognitive deficits in neurofibromatosis 1.
        J Child Neurol. 2002; 17: 605-612
        • Lorenzo J.
        • Barton B.
        • Acosta M.T.
        • North K.
        Mental, motor, and language development of toddlers with neurofibromatosis type 1.
        J Pediatr. 2011; 158: 660-665
        • Casnar C.L.
        • Klein-Tasman P.B.
        Parent and Teacher Perspectives on Emerging Executive Functioning in Preschoolers With Neurofibromatosis Type 1: Comparison to Unaffected Children and Lab-Based Measures.
        J Pediatr Psychol. 2017; 42: 198-207
        • Ullrich N.J.
        • Ayr L.
        • Leaffer E.
        • Irons M.B.
        • Rey-Casserly C.
        Pilot study of a novel computerized task to assess spatial learning in children and adolescents with neurofibromatosis type 1.
        J Child Neurol. 2010; 25: 1195-1202
        • Hofman K.J.
        • Harris E.L.
        • Bryan R.N.
        • Denckla M.B.
        Neurofibromatosis type 1: The cognitive phenotype.
        J Pediatr. 1994; 124: S1-S8
        • Bawden H.
        • Dooley J.
        • Buckley D.
        • Camfield P.
        • Gordon K.
        • Riding M.
        • et al.
        MRI and nonverbal cognitive deficits in children with neurofibromatosis 1.
        J Clin Exp Neuropsychol. 1996; 18: 784-792
        • Champion J.A.
        • Rose K.J.
        • Payne J.M.
        • Burns J.
        • North K.N.
        Relationship between cognitive dysfunction, gait, and motor impairment in children and adolescents with neurofibromatosis type 1.
        Dev Med Child Neurol. 2014; 56: 468-474
        • Lehtonen A.
        • Garg S.
        • Roberts S.A.
        • Trump D.
        • Evans D.G.
        • Green J.
        • et al.
        Cognition in children with neurofibromatosis type 1: data from a population-based study.
        Dev Med Child Neurol. 2015; 57: 645-651
        • Krab L.C.
        • de Goede-Bolder A.
        • Aarsen F.K.
        • Moll H.A.
        • De Zeeuw C.I.
        • Elgersma Y.
        • et al.
        Motor learning in children with neurofibromatosis type I.
        Cerebellum. 2011; 10: 14-21
      1. Zimerman M, Wessel MJ, Timmermann JE, Granström Sofian, Gerloff C, Mautner VF, et al. Impairment of Procedural Learning and Motor Intracortical Inhibition in Neurofibromatosis Type 1 Patients. EBioMedicine. 2015;1;2(10):1430–7.

        • Feldmann R.
        • Denecke J.
        • Grenzebach M.
        • Schuierer G.
        • Weglage J.
        Neurofibromatosis type 1: motor and cognitive function and T2-weighted MRI hyperintensities.
        Neurology. 2003; 61: 1725-1728
        • Sabol Z.
        • Rešić B.
        • Gjergja Juraški R.
        • Sabol F.
        • Kovač Šižgorić M.
        • Oršolić K.
        • et al.
        Clinical sensitivity and specificity of multiple T2-hyperintensities on brain magnetic resonance imaging in diagnosis of neurofibromatosis type 1 in children: diagnostic accuracy study.
        Croat Med J. 2011; 52: 488-496
        • DiPaolo D.P.
        • Zimmerman R.A.
        • Rorke L.B.
        • Zackai E.H.
        • Bilaniuk L.T.
        • Yachnis A.T.
        Neurofibromatosis type 1: pathologic substrate of high-signal-intensity foci in the brain.
        Radiology. 1995; 195: 721-724
        • Baudou E.
        • Nemmi F.
        • Biotteau M.
        • Maziero S.
        • Peran P.
        • Chaix Y.
        Can the Cognitive Phenotype in Neurofibromatosis Type 1 (NF1) Be Explained by Neuroimaging?.
        A Review Front Neurol. 2020; 10: 1373
      2. Wechsler D. WISC-IV. Echelle d’intelligence de Wechsler pour enfants (4e ed.). “Wechsler intelligence scale for children–Fourth edition”[translated from “french” by the present author]. ECPA. 2005. French.

      3. American psychiatric association. Diagnostic and statistical manual of mental disorders (DSM) (5th ed.). 2013.

      4. Wechsler D, Naglieri JA. WNV - Echelle non verbale d’intelligence de Wechsler. “Wechsler Nonverbal Scale of Ability”[translated from “french” by the present author]. ECPA. 2009. French.

      5. Auclair L, Jambaqué L. Naming pictures test for school-aged children: DEN48 revised and short version (DEN30). ANAE Approche Neuropsychol Apprentiss Enfant. ANAE. 2014;26(128):79-86. French.

      6. Jambaqué I, Dellatolas G, Dulac O, Signoret J-L. Standardization of the 144 memory efficiency battery in school-age children. ANAE Approch Neuropsychol Apprentiss Enfant. 1991;3(3):125-35. French.

        • Levine B.
        • Svoboda E.
        • Hay J.F.
        • Winocur G.
        • Moscovitch M.
        Aging and autobiographical memory : dissociating episodic from semantic retrieval.
        Psychol Aging. 2002; 17: 677-689
        • Nissen M.J.
        • Bullemer P.
        Attention requirements of learning: Evidence from performance measures.
        Cogn Psychol. 1987; 19: 1-32
      7. Jacquier-Roux M, Valdois S, Zorman M, Lequette C, Pouget G. ODÉDYS: Outil de dépistage des dyslexies, version 2.“Dyslexia screening tool, version 2”[translated from “french” by the present author]. UPMF. 2005. French.

      8. Benton AL, Sivan AB, Hamsher K deS., Varney NR, Spreen O. Benton Judgement of Line Orientation, Form V. Psychological Assessment Ressources. 1983. USA.

      9. Brickenkamp R. d2 Test d’Attention Concentrée. “d2 Test of Attention”[translated from “french” by the present author]. ECPA. 1998. French.

        • Billingsley R.L.
        • Slopis J.M.
        • Swank P.R.
        • Jackson E.F.
        • Moore B.D.
        Cortical morphology associated with language function in neurofibromatosis, type I.
        Brain Lang. 2003; 85: 125-139
        • Potvin D.
        • Hardy K.K.
        • Walsh K.S.
        The Relation Between ADHD and Cognitive Profiles of Children with NF1.
        J Pediatr Neuropsychol. 2015; 1: 42-49
        • Heimgärtner M.
        • Granström S.
        • Haas-Lude K.
        • Leark R.A.
        • Mautner V.-F.
        • Lidzba K.
        Attention Deficit Predicts Intellectual Functioning in Children with Neurofibromatosis Type 1.
        Int J Pediatr. 2019; 2019: 9493837
        • Pride N.A.
        • Payne J.M.
        • North K.N.
        The Impact of ADHD on the Cognitive and Academic Functioning of Children with NF1.
        Dev Neuropsychol. 2012; 37: 590-600
        • Payne J.M.
        • Arnold S.S.
        • Pride N.A.
        • North K.N.
        Does attention-deficit-hyperactivity disorder exacerbate executive dysfunction in children with neurofibromatosis type 1?.
        Dev Med Child Neurol. 2012; 54: 898-904
        • Shilyansky C.
        • Karlsgodt K.H.
        • Cummings D.M.
        • Sidiropoulou K.
        • Hardt M.
        • James A.S.
        • et al.
        Neurofibromin regulates corticostriatal inhibitory networks during working memory performance.
        Proc Natl Acad Sci U S A. 2010; 107: 13141-13146
        • Mazzocco M.M.M.
        • Turner J.E.
        • Denckla M.B.
        • Hofman K.J.
        • Scanlon D.C.
        • Vellutino F.R.
        Language and reading deficits associated with Neurofibromatosis Type 1: Evidence for a not-so-nonverbal Learning Disability.
        Dev Neuropsychol. 1995; 11: 503-522
        • Sangster J.
        • Shores E.A.
        • Watt S.
        • North K.N.
        The cognitive profile of preschool-aged children with neurofibromatosis type 1.
        Child Neuropsychol. 2011; 17: 1-16
        • Bulgheroni S.
        • Taddei M.
        • Saletti V.
        • Esposito S.
        • Micheli R.
        • Riva D.
        Visuoperceptual Impairment in Children with NF1: From Early Visual Processing to Procedural Strategies.
        Behav Neuology. 2019; 2019: 7146168
        • Piolino P.
        • Desgranges B.
        • Manning L.
        • North P.
        • Jokic C.
        • Eustache F.
        Autobiographical Memory, the Sense of Recollection and Executive Functions After Severe Traumatic Brain Injury.
        Cortex. 2006; 43: 176-195
        • Piolino P.
        • Hisland M.
        • Ruffeveille I.
        • Matuszewski V.
        • Jambaqué I.
        • Eustache F.
        Do school-age children remember or know the personal past ?.
        Conscious Cogn. 2007; 16: 84-101
        • Doyon J.
        • Benali H.
        Reorganization and plasticity in the adult brain during learning of motor skills.
        Curr Opin Neurobiol. 2005; 15: 161-167
        • Willoughby K.A.
        • Desrocher M.
        • Levine B.
        • Rovet J.F.
        Episodic and Semantic Autobiographical Memory and Everyday Memory during Late Childhood and Early Adolescence.
        Front Psychol. 2012; 3: 53
        • Beaussart M.L.
        • Barbarot S.
        • Mauger C.
        • Roy A.
        Systematic Review and Meta-analysis of Executive Functions in Preschool and School-Age Children with Neurofibromatosis Type 1.
        J Int Neuropsychol Soc. 2018; 24: 977-994