Skip to main content
Top
Published in: Journal of Neurodevelopmental Disorders 1/2018

Open Access 01-12-2018 | Research

Auditory repetition suppression alterations in relation to cognitive functioning in fragile X syndrome: a combined EEG and machine learning approach

Authors: Inga Sophia Knoth, Tarek Lajnef, Simon Rigoulot, Karine Lacourse, Phetsamone Vannasing, Jacques L. Michaud, Sébastien Jacquemont, Philippe Major, Karim Jerbi, Sarah Lippé

Published in: Journal of Neurodevelopmental Disorders | Issue 1/2018

Login to get access

Abstract

Background

Fragile X syndrome (FXS) is a neurodevelopmental genetic disorder causing cognitive and behavioural deficits. Repetition suppression (RS), a learning phenomenon in which stimulus repetitions result in diminished brain activity, has been found to be impaired in FXS. Alterations in RS have been associated with behavioural problems in FXS; however, relations between RS and intellectual functioning have not yet been elucidated.

Methods

EEG was recorded in 14 FXS participants and 25 neurotypical controls during an auditory habituation paradigm using repeatedly presented pseudowords. Non-phased locked signal energy was compared across presentations and between groups using linear mixed models (LMMs) in order to investigate RS effects across repetitions and brain areas and a possible relation to non-verbal IQ (NVIQ) in FXS. In addition, we explored group differences according to NVIQ and we probed the feasibility of training a support vector machine to predict cognitive functioning levels across FXS participants based on single-trial RS features.

Results

LMM analyses showed that repetition effects differ between groups (FXS vs. controls) as well as with respect to NVIQ in FXS. When exploring group differences in RS patterns, we found that neurotypical controls revealed the expected pattern of RS between the first and second presentations of a pseudoword. More importantly, while FXS participants in the ≤ 42 NVIQ group showed no RS, the > 42 NVIQ group showed a delayed RS response after several presentations. Concordantly, single-trial estimates of repetition effects over the first four repetitions provided the highest decoding accuracies in the classification between the FXS participant groups.

Conclusion

Electrophysiological measures of repetition effects provide a non-invasive and unbiased measure of brain responses sensitive to cognitive functioning levels, which may be useful for clinical trials in FXS.
Appendix
Available only for authorised users
Literature
1.
go back to reference Penagarikano O, Mulle JG, Warren ST. The pathophysiology of fragile X syndrome. Annu Rev Genomics Hum Genet. 2007;8:109–29.CrossRefPubMed Penagarikano O, Mulle JG, Warren ST. The pathophysiology of fragile X syndrome. Annu Rev Genomics Hum Genet. 2007;8:109–29.CrossRefPubMed
2.
go back to reference Bear MF, Huber KM, Warren ST. The mGluR theory of fragile X mental retardation. Trends Neurosci. 2004;27(7):370–7.CrossRefPubMed Bear MF, Huber KM, Warren ST. The mGluR theory of fragile X mental retardation. Trends Neurosci. 2004;27(7):370–7.CrossRefPubMed
3.
go back to reference Hessl D, Nguyen DV, Green C, Chavez A, Tassone F, Hagerman RJ, Senturk D, Schneider A, Lightbody A, Reiss AL, et al. A solution to limitations of cognitive testing in children with intellectual disabilities: the case of fragile X syndrome. J Neurodev Disord. 2009;1(1):33–45.CrossRefPubMed Hessl D, Nguyen DV, Green C, Chavez A, Tassone F, Hagerman RJ, Senturk D, Schneider A, Lightbody A, Reiss AL, et al. A solution to limitations of cognitive testing in children with intellectual disabilities: the case of fragile X syndrome. J Neurodev Disord. 2009;1(1):33–45.CrossRefPubMed
4.
go back to reference Schneider A, Hagerman RJ, Hessl D. Fragile X syndrome—from genes to cognition. Dev Disabil Res Rev. 2009;15(4):333–42.CrossRefPubMed Schneider A, Hagerman RJ, Hessl D. Fragile X syndrome—from genes to cognition. Dev Disabil Res Rev. 2009;15(4):333–42.CrossRefPubMed
5.
go back to reference Ornstein PA, Schaaf JM, Hooper SR, Hatton DD, Mirrett P, Bailey DB Jr. Memory skills of boys with fragile X syndrome. Am J Ment Retard. 2008;113(6):453–65.CrossRefPubMed Ornstein PA, Schaaf JM, Hooper SR, Hatton DD, Mirrett P, Bailey DB Jr. Memory skills of boys with fragile X syndrome. Am J Ment Retard. 2008;113(6):453–65.CrossRefPubMed
6.
go back to reference Bailey DB Jr, Raspa M, Bishop E, Holiday D. No change in the age of diagnosis for fragile X syndrome: findings from a national parent survey. Pediatrics. 2009;124(2):527–33.CrossRefPubMed Bailey DB Jr, Raspa M, Bishop E, Holiday D. No change in the age of diagnosis for fragile X syndrome: findings from a national parent survey. Pediatrics. 2009;124(2):527–33.CrossRefPubMed
8.
go back to reference Baranek GT, Roberts JE, David FJ, Sideris J, Mirrett PL, Hatton DD, Bailey DB Jr. Developmental trajectories and correlates of sensory processing in young boys with fragile X syndrome. Phys Occup Ther Pediatr. 2008;28(1):79–98.CrossRefPubMed Baranek GT, Roberts JE, David FJ, Sideris J, Mirrett PL, Hatton DD, Bailey DB Jr. Developmental trajectories and correlates of sensory processing in young boys with fragile X syndrome. Phys Occup Ther Pediatr. 2008;28(1):79–98.CrossRefPubMed
9.
go back to reference Ethridge LE, White SP, Mosconi MW, Wang J, Byerly MJ, Sweeney JA. Reduced habituation of auditory evoked potentials indicate cortical hyper-excitability in fragile X syndrome. Transl Psychiatry. 2016;6:e787.CrossRefPubMedPubMedCentral Ethridge LE, White SP, Mosconi MW, Wang J, Byerly MJ, Sweeney JA. Reduced habituation of auditory evoked potentials indicate cortical hyper-excitability in fragile X syndrome. Transl Psychiatry. 2016;6:e787.CrossRefPubMedPubMedCentral
10.
go back to reference Rogers SJ, Hepburn S, Wehner E. Parent reports of sensory symptoms in toddlers with autism and those with other developmental disorders. J Autism Dev Disord. 2003;33(6):631–42.CrossRefPubMed Rogers SJ, Hepburn S, Wehner E. Parent reports of sensory symptoms in toddlers with autism and those with other developmental disorders. J Autism Dev Disord. 2003;33(6):631–42.CrossRefPubMed
11.
12.
go back to reference Roberts TP, Cannon KM, Tavabi K, Blaskey L, Khan SY, Monroe JF, Qasmieh S, Levy SE, Edgar JC. Auditory magnetic mismatch field latency: a biomarker for language impairment in autism. Biol Psychiatry. 2011;70(3):263–9.CrossRefPubMedPubMedCentral Roberts TP, Cannon KM, Tavabi K, Blaskey L, Khan SY, Monroe JF, Qasmieh S, Levy SE, Edgar JC. Auditory magnetic mismatch field latency: a biomarker for language impairment in autism. Biol Psychiatry. 2011;70(3):263–9.CrossRefPubMedPubMedCentral
13.
go back to reference Castren M, Paakkonen A, Tarkka IM, Ryynanen M, Partanen J. Augmentation of auditory N1 in children with fragile X syndrome. Brain Topogr. 2003;15(3):165–71.CrossRefPubMed Castren M, Paakkonen A, Tarkka IM, Ryynanen M, Partanen J. Augmentation of auditory N1 in children with fragile X syndrome. Brain Topogr. 2003;15(3):165–71.CrossRefPubMed
14.
go back to reference Knoth IS, Vannasing P, Major P, Michaud JL, Lippe S. Alterations of visual and auditory evoked potentials in fragile X syndrome. Int J Dev Neurosci. 2014;36:90–7.CrossRefPubMed Knoth IS, Vannasing P, Major P, Michaud JL, Lippe S. Alterations of visual and auditory evoked potentials in fragile X syndrome. Int J Dev Neurosci. 2014;36:90–7.CrossRefPubMed
15.
go back to reference Schneider A, Leigh MJ, Adams P, Nanakul R, Chechi T, Olichney J, Hagerman R, Hessl D. Electrocortical changes associated with minocycline treatment in fragile X syndrome. J Psychopharmacol. 2013;27(10):956–63.CrossRefPubMed Schneider A, Leigh MJ, Adams P, Nanakul R, Chechi T, Olichney J, Hagerman R, Hessl D. Electrocortical changes associated with minocycline treatment in fragile X syndrome. J Psychopharmacol. 2013;27(10):956–63.CrossRefPubMed
16.
go back to reference St Clair DM, Blackwood DH, Oliver CJ, Dickens P. P3 abnormality in fragile X syndrome. Biol Psychiatry. 1987;22(3):303–12.CrossRefPubMed St Clair DM, Blackwood DH, Oliver CJ, Dickens P. P3 abnormality in fragile X syndrome. Biol Psychiatry. 1987;22(3):303–12.CrossRefPubMed
17.
go back to reference Van der Molen MJ, Van der Molen MW, Ridderinkhof KR, Hamel BC, Curfs LM, Ramakers GJ. Auditory and visual cortical activity during selective attention in fragile X syndrome: a cascade of processing deficiencies. Clin Neurophysiol. 2012;123(4):720–9.CrossRefPubMed Van der Molen MJ, Van der Molen MW, Ridderinkhof KR, Hamel BC, Curfs LM, Ramakers GJ. Auditory and visual cortical activity during selective attention in fragile X syndrome: a cascade of processing deficiencies. Clin Neurophysiol. 2012;123(4):720–9.CrossRefPubMed
18.
go back to reference Van der Molen MJ, Van der Molen MW, Ridderinkhof KR, Hamel BC, Curfs LM, Ramakers GJ. Auditory change detection in fragile X syndrome males: a brain potential study. Clin Neurophysiol. 2012;123(7):1309–18.CrossRefPubMed Van der Molen MJ, Van der Molen MW, Ridderinkhof KR, Hamel BC, Curfs LM, Ramakers GJ. Auditory change detection in fragile X syndrome males: a brain potential study. Clin Neurophysiol. 2012;123(7):1309–18.CrossRefPubMed
19.
go back to reference Luck SJ. An introduction to the event-related potential technique. Cambridge: MIT Press; 2005. Luck SJ. An introduction to the event-related potential technique. Cambridge: MIT Press; 2005.
20.
go back to reference Näätanen R, Paavilainen P, Rinne T, Alho K. The mismatch negativity (MMN) in basic research of central auditory processing: a review. Clin Neurophysiol. 2007;118(12):2544–90.CrossRefPubMed Näätanen R, Paavilainen P, Rinne T, Alho K. The mismatch negativity (MMN) in basic research of central auditory processing: a review. Clin Neurophysiol. 2007;118(12):2544–90.CrossRefPubMed
22.
go back to reference Bruno JL, Garrett AS, Quintin EM, Mazaika PK, Reiss AL. Aberrant face and gaze habituation in fragile X syndrome. Am J Psychiatry. 2014;171(10):1099–106.CrossRefPubMedPubMedCentral Bruno JL, Garrett AS, Quintin EM, Mazaika PK, Reiss AL. Aberrant face and gaze habituation in fragile X syndrome. Am J Psychiatry. 2014;171(10):1099–106.CrossRefPubMedPubMedCentral
23.
go back to reference Rigoulot S, Knoth IS, Lafontaine MP, Vannasing P, Major P, Jacquemont S, Michaud JL, Jerbi K, Lippé S. Altered visual repetition suppression in fragile X syndrome: new evidence from ERPs and oscillatory activity. Int J Dev Neurosci. 2017;59:52–59. Rigoulot S, Knoth IS, Lafontaine MP, Vannasing P, Major P, Jacquemont S, Michaud JL, Jerbi K, Lippé S. Altered visual repetition suppression in fragile X syndrome: new evidence from ERPs and oscillatory activity. Int J Dev Neurosci. 2017;59:52–59.
24.
go back to reference Garrido MI, Kilner JM, Kiebel SJ, Stephan KE, Baldeweg T, Friston KJ. Repetition suppression and plasticity in the human brain. NeuroImage. 2009;48(1):269–79.CrossRefPubMedPubMedCentral Garrido MI, Kilner JM, Kiebel SJ, Stephan KE, Baldeweg T, Friston KJ. Repetition suppression and plasticity in the human brain. NeuroImage. 2009;48(1):269–79.CrossRefPubMedPubMedCentral
25.
go back to reference Kavšek M. Predicting later IQ from infant visual habituation and dishabituation: a meta-analysis. J Appl Dev Psychol. 2004;25(3):369–93.CrossRef Kavšek M. Predicting later IQ from infant visual habituation and dishabituation: a meta-analysis. J Appl Dev Psychol. 2004;25(3):369–93.CrossRef
26.
go back to reference Kutas M, Federmeier KD. Thirty years and counting: finding meaning in the N400 component of the event-related brain potential (ERP). Annu Rev Psychol. 2011;62:621–47.CrossRefPubMedPubMedCentral Kutas M, Federmeier KD. Thirty years and counting: finding meaning in the N400 component of the event-related brain potential (ERP). Annu Rev Psychol. 2011;62:621–47.CrossRefPubMedPubMedCentral
27.
go back to reference Yang JC, Chi L, Teichholtz S, Schneider A, Nanakul R, Nowacki R, Seritan A, Reed B, DeCarli C, Iragui VJ, et al. ERP abnormalities elicited by word repetition in fragile X-associated tremor/ataxia syndrome (FXTAS) and amnestic MCI. Neuropsychologia. 2014;63:34–42.CrossRefPubMedPubMedCentral Yang JC, Chi L, Teichholtz S, Schneider A, Nanakul R, Nowacki R, Seritan A, Reed B, DeCarli C, Iragui VJ, et al. ERP abnormalities elicited by word repetition in fragile X-associated tremor/ataxia syndrome (FXTAS) and amnestic MCI. Neuropsychologia. 2014;63:34–42.CrossRefPubMedPubMedCentral
28.
go back to reference Deacon D, Dynowska A, Ritter W, Grose-Fifer J. Repetition and semantic priming of nonwords: implications for theories of N400 and word recognition. Psychophysiology. 2004;41(1):60–74.CrossRefPubMed Deacon D, Dynowska A, Ritter W, Grose-Fifer J. Repetition and semantic priming of nonwords: implications for theories of N400 and word recognition. Psychophysiology. 2004;41(1):60–74.CrossRefPubMed
29.
go back to reference Lovelace JW, Wen TH, Reinhard S, Hsu MS, Sidhu H, Ethell IM, Binder DK, Razak KA. Matrix metalloproteinase-9 deletion rescues auditory evoked potential habituation deficit in a mouse model of fragile X syndrome. Neurobiol Dis. 2016;89:126–35.CrossRefPubMedPubMedCentral Lovelace JW, Wen TH, Reinhard S, Hsu MS, Sidhu H, Ethell IM, Binder DK, Razak KA. Matrix metalloproteinase-9 deletion rescues auditory evoked potential habituation deficit in a mouse model of fragile X syndrome. Neurobiol Dis. 2016;89:126–35.CrossRefPubMedPubMedCentral
30.
go back to reference Rotschafer S, Razak K. Altered auditory processing in a mouse model of fragile X syndrome. Brain Res. 2013;1506:12–24.CrossRefPubMed Rotschafer S, Razak K. Altered auditory processing in a mouse model of fragile X syndrome. Brain Res. 2013;1506:12–24.CrossRefPubMed
31.
go back to reference Sinclair D, Oranje B, Razak KA, Siegel SJ, Schmid S. Sensory processing in autism spectrum disorders and fragile X syndrome—from the clinic to animal models. Neurosci Biobehav Rev. 2016;76(pt B):235–53. Sinclair D, Oranje B, Razak KA, Siegel SJ, Schmid S. Sensory processing in autism spectrum disorders and fragile X syndrome—from the clinic to animal models. Neurosci Biobehav Rev. 2016;76(pt B):235–53.
32.
go back to reference Roid GH, Miller LJ. Leiter International Performance Scale—Revised: examiner’s manual. In: Roid GH, Miller LJ, editors. Leiter International Performance Scale—revised edn. Wood Dale: Stoelting Co.; 1997. Roid GH, Miller LJ. Leiter International Performance Scale—Revised: examiner’s manual. In: Roid GH, Miller LJ, editors. Leiter International Performance Scale—revised edn. Wood Dale: Stoelting Co.; 1997.
33.
go back to reference Wechsler D. Wechsler Abbreviated Scale of Intelligence. San Antonio: The Psychological Corporation; 1999. Wechsler D. Wechsler Abbreviated Scale of Intelligence. San Antonio: The Psychological Corporation; 1999.
34.
go back to reference Lam KSL, Aman MG. The Repetitive Behavior Scale-Revised: independent validation in individuals with autism spectrum disorders. J Autism Dev Disord. 2007;37(5):855–66.CrossRefPubMed Lam KSL, Aman MG. The Repetitive Behavior Scale-Revised: independent validation in individuals with autism spectrum disorders. J Autism Dev Disord. 2007;37(5):855–66.CrossRefPubMed
35.
go back to reference Aman MG, Singh NN, Stewart AW, Field CJ. The aberrant behavior checklist: a behavior rating scale for the assessment of treatment effects. Am J Ment Defic. 1985;89(5):485–91.PubMed Aman MG, Singh NN, Stewart AW, Field CJ. The aberrant behavior checklist: a behavior rating scale for the assessment of treatment effects. Am J Ment Defic. 1985;89(5):485–91.PubMed
36.
go back to reference Mousty P, Leybaert J, Alegria J, Content A, Morais J. BELEC. Batterie d’évaluation du langage écrit et de ces troubles. Bruxelles: De Boeck; 1994. Mousty P, Leybaert J, Alegria J, Content A, Morais J. BELEC. Batterie d’évaluation du langage écrit et de ces troubles. Bruxelles: De Boeck; 1994.
37.
go back to reference Jacquier-Roux M, Valdois S, Zorman M, Lequette C, Pouget G. ODÉDYS Outil de DÉpistage des DYSlexies Version 2. Université Pierre Mendes France: Laboratoire de Psychologie et Neurocognition; 2009. Jacquier-Roux M, Valdois S, Zorman M, Lequette C, Pouget G. ODÉDYS Outil de DÉpistage des DYSlexies Version 2. Université Pierre Mendes France: Laboratoire de Psychologie et Neurocognition; 2009.
38.
go back to reference Tucker DM. Spatial sampling of head electrical fields: the geodesic sensor net. Electroencephalogr Clin Neurophysiol. 1993;87(3):154–63.CrossRefPubMed Tucker DM. Spatial sampling of head electrical fields: the geodesic sensor net. Electroencephalogr Clin Neurophysiol. 1993;87(3):154–63.CrossRefPubMed
39.
go back to reference Plank M. Ocular correction ICA. In: Brain product press release 49: brain product press release 49; 2013. p. 1–4. Plank M. Ocular correction ICA. In: Brain product press release 49: brain product press release 49; 2013. p. 1–4.
40.
go back to reference Lafontaine MP, Lacourse K, Lina JM, McIntosh AR, Gosselin F, Theoret H, Lippe S. Brain signal complexity rises with repetition suppression in visual learning. Neuroscience. 2016;326:1–9.CrossRefPubMed Lafontaine MP, Lacourse K, Lina JM, McIntosh AR, Gosselin F, Theoret H, Lippe S. Brain signal complexity rises with repetition suppression in visual learning. Neuroscience. 2016;326:1–9.CrossRefPubMed
41.
go back to reference Ceponiene R, Rinne T, Näätänen R. Maturation of cortical sound processing as indexed by event-related potentials. Clin Neurophysiol. 2002;113(6):870–82.CrossRefPubMed Ceponiene R, Rinne T, Näätänen R. Maturation of cortical sound processing as indexed by event-related potentials. Clin Neurophysiol. 2002;113(6):870–82.CrossRefPubMed
42.
go back to reference Rigoulot S, Delplanque S, Despretz P, Defoort-Dhellemmes S, Honore J, Sequeira H. Peripherally presented emotional scenes: a spatiotemporal analysis of early ERP responses. Brain Topogr. 2008;20(4):216–23.CrossRefPubMed Rigoulot S, Delplanque S, Despretz P, Defoort-Dhellemmes S, Honore J, Sequeira H. Peripherally presented emotional scenes: a spatiotemporal analysis of early ERP responses. Brain Topogr. 2008;20(4):216–23.CrossRefPubMed
43.
go back to reference Rigoulot S, Fish K, Pell MD. Neural correlates of inferring speaker sincerity from white lies: an event-related potential source localization study. Brain Res. 2014;1565:48–62.CrossRefPubMed Rigoulot S, Fish K, Pell MD. Neural correlates of inferring speaker sincerity from white lies: an event-related potential source localization study. Brain Res. 2014;1565:48–62.CrossRefPubMed
44.
go back to reference Spencer KM, Dien J, Donchin E. A componential analysis of the ERP elicited by novel events using a dense electrode array. Psychophysiology. 1999;36(3):409–14.CrossRefPubMed Spencer KM, Dien J, Donchin E. A componential analysis of the ERP elicited by novel events using a dense electrode array. Psychophysiology. 1999;36(3):409–14.CrossRefPubMed
45.
go back to reference Spencer KM, Dien J, Donchin E. Spatiotemporal analysis of the late ERP responses to deviant stimuli. Psychophysiology. 2001;38(2):343–58.CrossRefPubMed Spencer KM, Dien J, Donchin E. Spatiotemporal analysis of the late ERP responses to deviant stimuli. Psychophysiology. 2001;38(2):343–58.CrossRefPubMed
46.
go back to reference Pourtois G, Delplanque S, Michel C, Vuilleumier P. Beyond conventional event-related brain potential (ERP): exploring the time-course of visual emotion processing using topographic and principal component analyses. Brain Topogr. 2008;20(4):265–77.CrossRefPubMed Pourtois G, Delplanque S, Michel C, Vuilleumier P. Beyond conventional event-related brain potential (ERP): exploring the time-course of visual emotion processing using topographic and principal component analyses. Brain Topogr. 2008;20(4):265–77.CrossRefPubMed
47.
go back to reference Field A. Discovering statistics using IBM SPSS statistics. Thousand Oaks: Sage; 2013. Field A. Discovering statistics using IBM SPSS statistics. Thousand Oaks: Sage; 2013.
48.
go back to reference Kaushal N, Rhodes RE. Exercise habit formation in new gym members: a longitudinal study. J Behav Med. 2015;38(4):652–63.CrossRefPubMed Kaushal N, Rhodes RE. Exercise habit formation in new gym members: a longitudinal study. J Behav Med. 2015;38(4):652–63.CrossRefPubMed
49.
go back to reference Shek DT, Ma CM. Longitudinal data analyses using linear mixed models in SPSS: concepts, procedures and illustrations. ScientificWorldJournal. 2011;11:42–76.CrossRefPubMedPubMedCentral Shek DT, Ma CM. Longitudinal data analyses using linear mixed models in SPSS: concepts, procedures and illustrations. ScientificWorldJournal. 2011;11:42–76.CrossRefPubMedPubMedCentral
50.
go back to reference West BT. Analyzing longitudinal data with the linear mixed models procedure in SPSS. Eval Health Prof. 2009;32(3):207–28.CrossRefPubMed West BT. Analyzing longitudinal data with the linear mixed models procedure in SPSS. Eval Health Prof. 2009;32(3):207–28.CrossRefPubMed
51.
go back to reference Combrisson E, Jerbi K. Exceeding chance level by chance: the caveat of theoretical chance levels in brain signal classification and statistical assessment of decoding accuracy. J Neurosci Methods. 2015;250:126–36.CrossRefPubMed Combrisson E, Jerbi K. Exceeding chance level by chance: the caveat of theoretical chance levels in brain signal classification and statistical assessment of decoding accuracy. J Neurosci Methods. 2015;250:126–36.CrossRefPubMed
52.
go back to reference Rosburg T, Zimmerer K, Huonker R. Short-term habituation of auditory evoked potential and neuromagnetic field components in dependence of the interstimulus interval. Exp Brain Res. 2010;205(4):559–70.CrossRefPubMed Rosburg T, Zimmerer K, Huonker R. Short-term habituation of auditory evoked potential and neuromagnetic field components in dependence of the interstimulus interval. Exp Brain Res. 2010;205(4):559–70.CrossRefPubMed
53.
go back to reference Snyder KA, Keil A. Repetition suppression of induced gamma activity predicts enhanced orienting toward a novel stimulus in 6-month-old infants. J Cogn Neurosci. 2008;20(12):2137–52.CrossRefPubMed Snyder KA, Keil A. Repetition suppression of induced gamma activity predicts enhanced orienting toward a novel stimulus in 6-month-old infants. J Cogn Neurosci. 2008;20(12):2137–52.CrossRefPubMed
54.
55.
go back to reference Rankin CH, Abrams T, Barry RJ, Bhatnagar S, Clayton DF, Colombo J, Coppola G, Geyer MA, Glanzman DL, Marsland S, et al. Habituation revisited: an updated and revised description of the behavioral characteristics of habituation. Neurobiol Learn Mem. 2009;92(2):135–8.CrossRefPubMed Rankin CH, Abrams T, Barry RJ, Bhatnagar S, Clayton DF, Colombo J, Coppola G, Geyer MA, Glanzman DL, Marsland S, et al. Habituation revisited: an updated and revised description of the behavioral characteristics of habituation. Neurobiol Learn Mem. 2009;92(2):135–8.CrossRefPubMed
56.
go back to reference Rose DH, Slater A, Perry H. Prediction of childhood intelligence from habituation in early infancy. Intelligence. 1986;10(3):251–63.CrossRef Rose DH, Slater A, Perry H. Prediction of childhood intelligence from habituation in early infancy. Intelligence. 1986;10(3):251–63.CrossRef
57.
go back to reference Budd TW, Barry RJ, Gordon E, Rennie C, Michie PT. Decrement of the N1 auditory event-related potential with stimulus repetition: habituation vs. refractoriness. Int J Psychophysiol. 1998;31(1):51–68.CrossRefPubMed Budd TW, Barry RJ, Gordon E, Rennie C, Michie PT. Decrement of the N1 auditory event-related potential with stimulus repetition: habituation vs. refractoriness. Int J Psychophysiol. 1998;31(1):51–68.CrossRefPubMed
59.
go back to reference Grill-Spector K, Henson R, Martin A. Repetition and the brain: neural models of stimulus-specific effects. Trends Cogn Sci. 2006;10(1):14–23.CrossRefPubMed Grill-Spector K, Henson R, Martin A. Repetition and the brain: neural models of stimulus-specific effects. Trends Cogn Sci. 2006;10(1):14–23.CrossRefPubMed
60.
go back to reference Wiggs CL, Martin A. Properties and mechanisms of perceptual priming. Curr Opin Neurobiol. 1998;8(2):227–33.CrossRefPubMed Wiggs CL, Martin A. Properties and mechanisms of perceptual priming. Curr Opin Neurobiol. 1998;8(2):227–33.CrossRefPubMed
61.
go back to reference Friston K. A theory of cortical responses. Philos Trans R Soc Lond Ser B Biol Sci. 2005;360(1456):815–36.CrossRef Friston K. A theory of cortical responses. Philos Trans R Soc Lond Ser B Biol Sci. 2005;360(1456):815–36.CrossRef
62.
go back to reference Summerfield C, Egner T, Greene M, Koechlin E, Mangels J, Hirsch J. Predictive codes for forthcoming perception in the frontal cortex. Science. 2006;314(5803):1311–4.CrossRefPubMed Summerfield C, Egner T, Greene M, Koechlin E, Mangels J, Hirsch J. Predictive codes for forthcoming perception in the frontal cortex. Science. 2006;314(5803):1311–4.CrossRefPubMed
63.
go back to reference Baldeweg T. Repetition effects to sounds: evidence for predictive coding in the auditory system. Trends Cogn Sci. 2006;10(3):93–4.CrossRefPubMed Baldeweg T. Repetition effects to sounds: evidence for predictive coding in the auditory system. Trends Cogn Sci. 2006;10(3):93–4.CrossRefPubMed
64.
go back to reference Gibson JR, Bartley AF, Hays SA, Huber KM. Imbalance of neocortical excitation and inhibition and altered UP states reflect network hyperexcitability in the mouse model of fragile X syndrome. J Neurophysiol. 2008;100(5):2615–26.CrossRefPubMedPubMedCentral Gibson JR, Bartley AF, Hays SA, Huber KM. Imbalance of neocortical excitation and inhibition and altered UP states reflect network hyperexcitability in the mouse model of fragile X syndrome. J Neurophysiol. 2008;100(5):2615–26.CrossRefPubMedPubMedCentral
65.
go back to reference Portera-Cailliau C. Which comes first in fragile X syndrome, dendritic spine dysgenesis or defects in circuit plasticity? Neuroscientist. 2012;18(1):28–44.CrossRefPubMed Portera-Cailliau C. Which comes first in fragile X syndrome, dendritic spine dysgenesis or defects in circuit plasticity? Neuroscientist. 2012;18(1):28–44.CrossRefPubMed
66.
go back to reference Irwin SA, Galvez R, Greenough WT. Dendritic spine structural anomalies in fragile-X mental retardation syndrome. Cereb Cortex. 2000;10(10):1038–44.CrossRefPubMed Irwin SA, Galvez R, Greenough WT. Dendritic spine structural anomalies in fragile-X mental retardation syndrome. Cereb Cortex. 2000;10(10):1038–44.CrossRefPubMed
67.
go back to reference Irwin SA, Patel B, Idupulapati M, Harris JB, Crisostomo RA, Larsen BP, Kooy F, Willems PJ, Cras P, Kozlowski PB, et al. Abnormal dendritic spine characteristics in the temporal and visual cortices of patients with fragile-X syndrome: a quantitative examination. Am J Med Genet. 2001;98(2):161–7.CrossRefPubMed Irwin SA, Patel B, Idupulapati M, Harris JB, Crisostomo RA, Larsen BP, Kooy F, Willems PJ, Cras P, Kozlowski PB, et al. Abnormal dendritic spine characteristics in the temporal and visual cortices of patients with fragile-X syndrome: a quantitative examination. Am J Med Genet. 2001;98(2):161–7.CrossRefPubMed
68.
go back to reference Deng PY, Rotman Z, Blundon JA, Cho Y, Cui J, Cavalli V, Zakharenko SS, Klyachko VA. FMRP regulates neurotransmitter release and synaptic information transmission by modulating action potential duration via BK channels. Neuron. 2013;77(4):696–711.CrossRefPubMedPubMedCentral Deng PY, Rotman Z, Blundon JA, Cho Y, Cui J, Cavalli V, Zakharenko SS, Klyachko VA. FMRP regulates neurotransmitter release and synaptic information transmission by modulating action potential duration via BK channels. Neuron. 2013;77(4):696–711.CrossRefPubMedPubMedCentral
69.
go back to reference Hebert B, Pietropaolo S, Meme S, Laudier B, Laugeray A, Doisne N, Quartier A, Lefeuvre S, Got L, Cahard D, et al. Rescue of fragile X syndrome phenotypes in Fmr1 KO mice by a BKCa channel opener molecule. Orphanet J Rare Dis. 2014;9:124.CrossRefPubMedPubMedCentral Hebert B, Pietropaolo S, Meme S, Laudier B, Laugeray A, Doisne N, Quartier A, Lefeuvre S, Got L, Cahard D, et al. Rescue of fragile X syndrome phenotypes in Fmr1 KO mice by a BKCa channel opener molecule. Orphanet J Rare Dis. 2014;9:124.CrossRefPubMedPubMedCentral
70.
go back to reference Typlt M, Mirkowski M, Azzopardi E, Ruettiger L, Ruth P, Schmid S. Mice with deficient BK channel function show impaired prepulse inhibition and spatial learning, but normal working and spatial reference memory. PLoS One. 2013;8(11):e81270.CrossRefPubMedPubMedCentral Typlt M, Mirkowski M, Azzopardi E, Ruettiger L, Ruth P, Schmid S. Mice with deficient BK channel function show impaired prepulse inhibition and spatial learning, but normal working and spatial reference memory. PLoS One. 2013;8(11):e81270.CrossRefPubMedPubMedCentral
71.
go back to reference Zhang Y, Bonnan A, Bony G, Ferezou I, Pietropaolo S, Ginger M, Sans N, Rossier J, Oostra B, LeMasson G, et al. Dendritic channelopathies contribute to neocortical and sensory hyperexcitability in Fmr1(-/y) mice. Nat Neurosci. 2014;17(12):1701–9.CrossRefPubMed Zhang Y, Bonnan A, Bony G, Ferezou I, Pietropaolo S, Ginger M, Sans N, Rossier J, Oostra B, LeMasson G, et al. Dendritic channelopathies contribute to neocortical and sensory hyperexcitability in Fmr1(-/y) mice. Nat Neurosci. 2014;17(12):1701–9.CrossRefPubMed
72.
go back to reference Bar M, Kassam KS, Ghuman AS, Boshyan J, Schmid AM, Dale AM, Hamalainen MS, Marinkovic K, Schacter DL, Rosen BR, et al. Top-down facilitation of visual recognition. Proc Natl Acad Sci U S A. 2006;103(2):449–54.CrossRefPubMedPubMedCentral Bar M, Kassam KS, Ghuman AS, Boshyan J, Schmid AM, Dale AM, Hamalainen MS, Marinkovic K, Schacter DL, Rosen BR, et al. Top-down facilitation of visual recognition. Proc Natl Acad Sci U S A. 2006;103(2):449–54.CrossRefPubMedPubMedCentral
73.
go back to reference O'Doherty J, Dayan P, Schultz J, Deichmann R, Friston K, Dolan RJ. Dissociable roles of ventral and dorsal striatum in instrumental conditioning. Science. 2004;304(5669):452–4.CrossRefPubMed O'Doherty J, Dayan P, Schultz J, Deichmann R, Friston K, Dolan RJ. Dissociable roles of ventral and dorsal striatum in instrumental conditioning. Science. 2004;304(5669):452–4.CrossRefPubMed
74.
go back to reference Lafontaine MP, Theoret H, Gosselin F, Lippe S. Transcranial direct current stimulation of the dorsolateral prefrontal cortex modulates repetition suppression to unfamiliar faces: an ERP study. PLoS One. 2013;8(12):e81721.CrossRefPubMedPubMedCentral Lafontaine MP, Theoret H, Gosselin F, Lippe S. Transcranial direct current stimulation of the dorsolateral prefrontal cortex modulates repetition suppression to unfamiliar faces: an ERP study. PLoS One. 2013;8(12):e81721.CrossRefPubMedPubMedCentral
75.
go back to reference Peng DX, Kelley RG, Quintin EM, Raman M, Thompson PM, Reiss AL. Cognitive and behavioral correlates of caudate subregion shape variation in fragile X syndrome. Hum Brain Mapp. 2014;35(6):2861–8.CrossRefPubMed Peng DX, Kelley RG, Quintin EM, Raman M, Thompson PM, Reiss AL. Cognitive and behavioral correlates of caudate subregion shape variation in fragile X syndrome. Hum Brain Mapp. 2014;35(6):2861–8.CrossRefPubMed
76.
go back to reference Bosch SE, Jehee JF, Fernandez G, Doeller CF. Reinstatement of associative memories in early visual cortex is signaled by the hippocampus. J Neurosci. 2014;34(22):7493–500.CrossRefPubMed Bosch SE, Jehee JF, Fernandez G, Doeller CF. Reinstatement of associative memories in early visual cortex is signaled by the hippocampus. J Neurosci. 2014;34(22):7493–500.CrossRefPubMed
77.
go back to reference Hindy NC, Ng FY, Turk-Browne NB. Linking pattern completion in the hippocampus to predictive coding in visual cortex. Nat Neurosci. 2016;19(5):665–7.CrossRefPubMedPubMedCentral Hindy NC, Ng FY, Turk-Browne NB. Linking pattern completion in the hippocampus to predictive coding in visual cortex. Nat Neurosci. 2016;19(5):665–7.CrossRefPubMedPubMedCentral
78.
go back to reference Kok P, Jehee JF, de Lange FP. Less is more: expectation sharpens representations in the primary visual cortex. Neuron. 2012;75(2):265–70.CrossRefPubMed Kok P, Jehee JF, de Lange FP. Less is more: expectation sharpens representations in the primary visual cortex. Neuron. 2012;75(2):265–70.CrossRefPubMed
79.
go back to reference Molnar K, Keri S. Bigger is better and worse: on the intricate relationship between hippocampal size and memory. Neuropsychologia. 2014;56:73–8.CrossRefPubMed Molnar K, Keri S. Bigger is better and worse: on the intricate relationship between hippocampal size and memory. Neuropsychologia. 2014;56:73–8.CrossRefPubMed
80.
go back to reference van der Molen MJ, Stam CJ, van der Molen MW. Resting-state EEG oscillatory dynamics in fragile X syndrome: abnormal functional connectivity and brain network organization. PLoS One. 2014;9(2):e88451.CrossRefPubMedPubMedCentral van der Molen MJ, Stam CJ, van der Molen MW. Resting-state EEG oscillatory dynamics in fragile X syndrome: abnormal functional connectivity and brain network organization. PLoS One. 2014;9(2):e88451.CrossRefPubMedPubMedCentral
81.
go back to reference Wang J, Ethridge LE, Mosconi MW, White SP, Binder DK, Pedapati EV, Erickson CA, Byerly MJ, Sweeney JA. A resting EEG study of neocortical hyperexcitability and altered functional connectivity in fragile X syndrome. J Neurodev Disord. 2017;9:11.CrossRefPubMedPubMedCentral Wang J, Ethridge LE, Mosconi MW, White SP, Binder DK, Pedapati EV, Erickson CA, Byerly MJ, Sweeney JA. A resting EEG study of neocortical hyperexcitability and altered functional connectivity in fragile X syndrome. J Neurodev Disord. 2017;9:11.CrossRefPubMedPubMedCentral
82.
go back to reference Abbeduto L, Brady N, Kover ST. Language development and fragile X syndrome: profiles, syndrome-specificity, and within-syndrome differences. Ment Retard Dev Disabil Res Rev. 2007;13(1):36–46.CrossRefPubMed Abbeduto L, Brady N, Kover ST. Language development and fragile X syndrome: profiles, syndrome-specificity, and within-syndrome differences. Ment Retard Dev Disabil Res Rev. 2007;13(1):36–46.CrossRefPubMed
83.
go back to reference Devitt NM, Gallagher L, Reilly RB. Autism spectrum disorder (ASD) and fragile X syndrome (FXS): two overlapping disorders reviewed through electroencephalography—what can be interpreted from the available information? Brain Sci. 2015;5(2):92–117.CrossRefPubMed Devitt NM, Gallagher L, Reilly RB. Autism spectrum disorder (ASD) and fragile X syndrome (FXS): two overlapping disorders reviewed through electroencephalography—what can be interpreted from the available information? Brain Sci. 2015;5(2):92–117.CrossRefPubMed
84.
go back to reference Fox AM, Anderson M, Reid C, Smith T, Bishop DV. Maturation of auditory temporal integration and inhibition assessed with event-related potentials (ERPs). BMC Neurosci. 2010;11:49.CrossRefPubMedPubMedCentral Fox AM, Anderson M, Reid C, Smith T, Bishop DV. Maturation of auditory temporal integration and inhibition assessed with event-related potentials (ERPs). BMC Neurosci. 2010;11:49.CrossRefPubMedPubMedCentral
Metadata
Title
Auditory repetition suppression alterations in relation to cognitive functioning in fragile X syndrome: a combined EEG and machine learning approach
Authors
Inga Sophia Knoth
Tarek Lajnef
Simon Rigoulot
Karine Lacourse
Phetsamone Vannasing
Jacques L. Michaud
Sébastien Jacquemont
Philippe Major
Karim Jerbi
Sarah Lippé
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Journal of Neurodevelopmental Disorders / Issue 1/2018
Print ISSN: 1866-1947
Electronic ISSN: 1866-1955
DOI
https://doi.org/10.1186/s11689-018-9223-3

Other articles of this Issue 1/2018

Journal of Neurodevelopmental Disorders 1/2018 Go to the issue