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BMC Neurology

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Open Access 01-12-2015 | Research article

Robust disruptions in electroencephalogram cortical oscillations and large-scale functional networks in autism

Authors: Sean Matlis, Katica Boric, Catherine J. Chu, Mark A. Kramer

Published in: BMC Neurology | Issue 1/2015

Abstract

Background

Autism spectrum disorders (ASD) are increasingly prevalent and have a significant impact on the lives of patients and their families. Currently, the diagnosis is determined by clinical judgment and no definitive physiological biomarker for ASD exists. Quantitative biomarkers obtainable from clinical neuroimaging data – such as the scalp electroencephalogram (EEG) - would provide an important aid to clinicians in the diagnosis of ASD. The interpretation of prior studies in this area has been limited by mixed results and the lack of validation procedures. Here we use retrospective clinical data from a well-characterized population of children with ASD to evaluate the rhythms and coupling patterns present in the EEG to develop and validate an electrophysiological biomarker of ASD.

Methods

EEG data were acquired from a population of ASD (n = 27) and control (n = 55) children 4–8 years old. Data were divided into training (n = 13 ASD, n = 24 control) and validation (n = 14 ASD, n = 31 control) groups. Evaluation of spectral and functional network properties in the first group of patients motivated three biomarkers that were computed in the second group of age-matched patients for validation.

Results

Three biomarkers of ASD were identified in the first patient group: (1) reduced posterior/anterior power ratio in the alpha frequency range (8–14 Hz), which we label the “peak alpha ratio”, (2) reduced global density in functional networks, and (3) a reduction in the mean connectivity strength of a subset of functional network edges. Of these three biomarkers, the first and third were validated in a second group of patients. Using the two validated biomarkers, we were able to classify ASD subjects with 83 % sensitivity and 68 % specificity in a post-hoc analysis.

Conclusions

This study demonstrates that clinical EEG can provide quantitative biomarkers to assist diagnosis of autism. These results corroborate the general finding that ASD subjects have decreased alpha power gradients and network connectivities compared to control subjects. In addition, this study demonstrates the necessity of using statistical techniques to validate EEG biomarkers identified using exploratory methods.

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American Psychiatric A. Task Force on DSM-V. Diagnostic and Statistical Manual of Mental Disorders. 2013;DSM-5:991.

Blaxill MF. What’s Going On? The Question of Time Trends in Autism. Public Health Rep. 2004;119:536–51.PubMedPubMedCentral

Autism and Developmental Disabilities Monitoring Network Surveillance Year 2008 Principal Investigators, Centers for Disease Control and Prevention. Prevalence of autism spectrum disorders--Autism and Developmental Disabilities Monitoring Network, 14 sites, United States, 2008. Morb Mortal Wkly Rep Surveill Summ Wash DC 2002. 2012;61:1–19.

Coben R, Clarke AR, Hudspeth W, Barry RJ. EEG power and coherence in autistic spectrum disorder. Clin Neurophysiol. 2008;119:1002–9.PubMed

Committee on Educational Interventions for Children with Autism NRC: Educating Children with Autism. Washington, DC: National Academy Press; [S.l.]: [s.n.]; 2001.

Matson JL. Current status of differential diagnosis for children with autism spectrum disorders. Res Dev Disabil. 2007;28:109–18.PubMed

Bosl W, Tierney A, Tager-Flusberg H, Nelson C. EEG complexity as a biomarker for autism spectrum disorder risk. BMC Med. 2011;9:18.PubMedPubMedCentral

Griffin R, Westbury C. Infant EEG activity as a biomarker for autism: a promising approach or a false promise? BMC Med. 2011;9:61.PubMedPubMedCentral

Bosl W, Tierney A, Tager-Flusberg H, Nelson C. Response: Infant EEG activity as a biomarker for autism: A promising approach or a false promise? BMC Med. 2011;9:60.PubMedPubMedCentral

10.

Betancur C. Etiological heterogeneity in autism spectrum disorders: More than 100 genetic and genomic disorders and still counting. Brain Res. 2011;1380:42–77.PubMed

11.

Bassett DS, Bullmore ET. Human brain networks in health and disease. Curr Opin Neurol. 2009;22:340.PubMedPubMedCentral

12.

Belmonte MK, Allen G, Beckel-Mitchener A, Carper R a, Webb SJ. Autism and abnormal development of brain connectivity. J Neurosci Off J Soc Neurosci. 2004;24:9228–31.

13.

Bullmore E, Sporns O. Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci. 2009;10:186–98.PubMed

14.

Frith C. Is autism a disconnection disorder? Lancet Neurol. 2004;3:577.PubMed

15.

Geschwind DH, Levitt P. Autism spectrum disorders: developmental disconnection syndromes. Curr Opin Neurobiol. 2007;17:103–11.PubMed

16.

Just MA, Cherkassky VL, Keller T a, Minshew NJ. Cortical activation and synchronization during sentence comprehension in high-functioning autism: evidence of underconnectivity. Brain J Neurol. 2004;127(Pt 8):1811–21.

17.

Just MA, Cherkassky VL, Keller TA, Kana RK, Minshew NJ. Functional and Anatomical Cortical Underconnectivity in Autism: Evidence from an fMRI Study of an Executive Function Task and Corpus Callosum Morphometry. Cereb Cortex. 2007;17:951–61.PubMed

18.

Just MA, Keller T a, Malave VL, Kana RK, Varma S. Autism as a neural systems disorder: A theory of frontal-posterior underconnectivity. Neurosci Biobehav Rev. 2012;1–22.

19.

Muller R-A, Shih P, Keehn B, Deyoe JR, Leyden KM, Shukla DK. Underconnected, but How? A Survey of Functional Connectivity MRI Studies in Autism Spectrum Disorders. Cereb Cortex. 2011;21:2233–43.PubMedPubMedCentral

20.

Muller R-A. The study of autism as a distributed disorder. Ment Retard Dev Disabil Res Rev. 2007;13:85–95.PubMedPubMedCentral

21.

Rippon G, Brock J, Brown C, Boucher J. Disordered connectivity in the autistic brain: Challenges for the “new psychophysiology”. Int J Psychophysiol. 2007;63:164–72.PubMed

22.

Sporns O. Networks of the Brain. Cambridge, Mass: MIT Press; 2011.

23.

Kolaczyk ED. Statistical Analysis of Network Data Methods and Models. New York; London: Springer; 2009.

24.

Sporns O, Tononi G, Edelman GM. Connectivity and complexity: the relationship between neuroanatomy and brain dynamics. Neural Netw Off J Int Neural Netw Soc. 2000;13:909–22.

25.

Sporns O, Chialvo DR, Kaiser M, Hilgetag CC. Organization, development and function of complex brain networks. Trends Cogn Sci. 2004;8:418–25.PubMed

26.

Buzsáki G. Rhythms of the Brain. Oxford. New York: Oxford University Press; 2006.

27.

Damarla SR, Keller TA, Kana RK, Cherkassky VL, Williams DL, Minshew NJ, Just MA. Cortical underconnectivity coupled with preserved visuospatial cognition in autism: Evidence from an fMRI study of an embedded figures task. Autism Res Off J Int Soc Autism Res. 2010;3:273–9.

28.

Kana RK, Keller TA, Cherkassky VL, Minshew NJ, Just MA. Sentence comprehension in autism: thinking in pictures with decreased functional connectivity. Brain. 2006;129:2484–93.PubMedPubMedCentral

29.

Kana RK, Keller TA, Cherkassky VL, Minshew NJ, Just MA. Atypical frontal-posterior synchronization of Theory of Mind regions in autism during mental state attribution. Soc Neurosci. 2009;4:135–52.PubMed

30.

Kana RK, Keller TA, Minshew NJ, Just MA. Inhibitory Control in High-Functioning Autism: Decreased Activation and Underconnectivity in Inhibition Networks. Biol Psychiatry. 2007;62:198–206.PubMed

31.

Koshino H, Carpenter PA, Minshew NJ, Cherkassky VL, Keller TA, Just MA. Functional connectivity in an fMRI working memory task in high-functioning autism. Neuroimage. 2005;24:810–21.PubMed

32.

Koshino H, Kana RK, Keller TA, Cherkassky VL, Minshew NJ, Just MA. fMRI Investigation of Working Memory for Faces in Autism: Visual Coding and Underconnectivity with Frontal Areas. Cereb Cortex. 2008;18:289–300.PubMed

33.

Mason RA, Williams DL, Kana RK, Minshew N, Just MA. Theory of Mind disruption and recruitment of the right hemisphere during narrative comprehension in autism. Neuropsychologia. 2008;46:269–80.PubMed

34.

Minshew NJ, Williams DL. The new neurobiology of autism: Cortex, connectivity, and neuronal organization. Arch Neurol. 2007;64:945–50.PubMedPubMedCentral

35.

Mizuno A, Liu Y, Williams DL, Keller TA, Minshew NJ, Just MA. The neural basis of deictic shifting in linguistic perspective-taking in high-functioning autism. Brain. 2011;134:2422–35.PubMedPubMedCentral

36.

Müller R-A, Shih P, Keehn B, Deyoe JR, Leyden KM, Shukla DK. Underconnected, but how? A survey of functional connectivity MRI studies in autism spectrum disorders. Cereb Cortex N Y N 1991. 2011;21:2233–43.

37.

Rubenstein JLR, Merzenich MM. Model of autism: increased ratio of excitation/inhibition in key neural systems. Genes Brain Behav. 2003;2:255–67.PubMed

38.

Schipul SE, Keller TA, Just MA. Inter-regional brain communication and its disturbance in autism. Front Syst Neurosci. 2011;5:10.PubMedPubMedCentral

39.

Wass S. Distortions and disconnections: disrupted brain connectivity in autism. Brain Cogn. 2011;75:18–28.PubMed

40.

Barttfeld P, Wicker B, Cukier S, Navarta S, Lew S, Sigman M. A big-world network in ASD: Dynamical connectivity analysis reflects a deficit in long-range connections and an excess of short-range connections (EEG). Neuropsychologia. 2011;49:254–63.PubMed

41.

Barttfeld P, Amoruso L, Ais J, Cukier S, Bavassi L, Tomio A, Manes F, Ibanez A, Sigman M. Organization of brain networks governed by long-range connections index autistic traits in the general population. J Neurodev Disord. 2013;5:16.PubMedPubMedCentral

42.

García Domínguez L, Stieben J, Pérez Velázquez JL, Shanker S. The imaginary part of coherency in autism: differences in cortical functional connectivity in preschool children. PLoS One. 2013;8, e75941.PubMedPubMedCentral

43.

Keown CL, Shih P, Nair A, Peterson N, Mulvey ME, Müller R-A. Local Functional Overconnectivity in Posterior Brain Regions Is Associated with Symptom Severity in Autism Spectrum Disorders. Cell Rep. 2013;5:567–72.PubMed

44.

Mizuno A, Villalobos ME, Davies MM, Dahl BC, Müller R-A. Partially enhanced thalamocortical functional connectivity in autism. Brain Res. 2006;1104:160–74.PubMed

45.

Noonan SK, Haist F, Müller R-A. Aberrant functional connectivity in autism: Evidence from low-frequency BOLD signal fluctuations. Brain Res. 2009;1262:48–63.PubMedPubMedCentral

46.

Supekar K, Uddin LQ, Khouzam A, Phillips J, Gaillard WD, Kenworthy LE, Yerys BE, Vaidya CJ, Menon V. Brain Hyperconnectivity in Children with Autism and its Links to Social Deficits. Cell Rep. 2013;5:738–47.PubMedPubMedCentral

47.

Turner KC, Frost L, Linsenbardt D, McIlroy JR, Müller R-A. Atypically diffuse functional connectivity between caudate nuclei and cerebral cortex in autism. Behav Brain Funct. 2006;2:34.PubMedPubMedCentral

48.

Villalobos ME, Mizuno A, Dahl BC, Kemmotsu N, Müller R-A. Reduced functional connectivity between V1 and inferior frontal cortex associated with visuomotor performance in autism. Neuroimage. 2005;25:916–25.PubMedPubMedCentral

49.

Welchew DE, Ashwin C, Berkouk K, Salvador R, Suckling J, Baron-Cohen S, Bullmore E. Functional disconnectivity of the medial temporal lobe in Asperger’s syndrome. Biol Psychiatry. 2005;57:991–8.PubMed

50.

Léveillé C, Barbeau EB, Bolduc C, Limoges É, Berthiaume C, Chevrier É, Mottron L, Godbout R. Enhanced connectivity between visual cortex and other regions of the brain in autism: a REM sleep EEG coherence study. Autism Res. 2010;3:280–5.PubMed

51.

Liu Y, Cherkassky VL, Minshew NJ, Just MA. Autonomy of lower-level perception from global processing in autism: Evidence from brain activation and functional connectivity. Neuropsychologia. 2011;49:2105–11.PubMedPubMedCentral

52.

Mostofsky SH, Powell SK, Simmonds DJ, Goldberg MC, Caffo B, Pekar JJ. Decreased connectivity and cerebellar activity in autism during motor task performance. Brain. 2009;132:2413–25.PubMedPubMedCentral

53.

Silber MH, Ancoli-Israel S, Bonnet MH, Chokroverty S, Grigg-Damberger MM, Hirshkowitz M, Kapen S, Keenan SA, Kryger MH, Penzel T, Pressman MR, Iber C. The visual scoring of sleep in adults. J Clin Sleep Med JCSM Off Publ Am Acad Sleep Med. 2007;3:121–31.

54.

Nunez PL, Srinivasan R. Electric Fields of the Brain: The Neurophysics of EEG. Oxford. New York: Oxford University Press; 2006.

55.

Lepage KQ, Kramer MA, Chu CJ. A statistically robust EEG re-referencing procedure to mitigate reference effect. J Neurosci Methods. 2014;235:101–16.PubMedPubMedCentral

56.

Bokil H, Andrews P, Kulkarni JE, Mehta S, Mitra PP. Chronux: A platform for analyzing neural signals. J Neurosci Methods. 2010;192:146–51.PubMedPubMedCentral

57.

Schomer DL, Silva FL da. Niedermeyer’s Electroencephalography: Basic Principles, Clinical Applications, and Related Fields. Philadelphia, PA: Lippincott Williams & Wilkins; 2012.

58.

Knyazev GG. Antero-Posterior EEG Spectral Power Gradient as a Correlate of Extraversion and Behavioral Inhibition. Open Neuroimaging J. 2010;4:114–20.

59.

Knyazev GG, Bocharov AV, Pylkova LV. Extraversion and fronto-posterior EEG spectral power gradient: An independent component analysis. Biol Psychol. 2012;89:515–24.PubMed

60.

Pereda E, Quiroga RQ, Bhattacharya J. Nonlinear multivariate analysis of neurophysiological signals. Prog Neurobiol. 2005;77:1–37.PubMed

61.

Nunez PL, Srinivasan R, Westdorp AF, Wijesinghe RS, Tucker DM, Silberstein RB, Cadusch PJ. EEG coherency: I: statistics, reference electrode, volume conduction, Laplacians, cortical imaging, and interpretation at multiple scales. Electroencephalogr Clin Neurophysiol. 1997;103:499–515.PubMed

62.

Ansari-Asl K, Senhadji L, Bellanger J-J, Wendling F. Quantitative evaluation of linear and nonlinear methods characterizing interdependencies between brain signals. Phys Rev E Stat Nonlin Soft Matter Phys. 2006;74(3 Pt 1):31916.PubMedCentral

63.

Osterhage H, Mormann F, Wagner T, Lehnertz K. MEASURING THE DIRECTIONALITY OF COUPLING: PHASE VERSUS STATE SPACE DYNAMICS AND APPLICATION TO EEG TIME SERIES. Int J Neural Syst. 2007;17:139–48.PubMed

64.

Chu CJ, Kramer MA, Pathmanathan J, Bianchi MT, Westover MB, Wizon L, Cash SS. Emergence of Stable Functional Networks in Long-Term Human Electroencephalography. J Neurosci. 2012;32:2703–13.PubMed

65.

Kramer MA, Eden UT, Kolaczyk ED, Zepeda R, Eskandar EN, Cash SS. Coalescence and Fragmentation of Cortical Networks during Focal Seizures. J Neurosci. 2010;30:10076–85.PubMedPubMedCentral

66.

Kramer MA, Eden UT, Lepage KQ, Kolaczyk ED, Bianchi MT, Cash SS. Emergence of Persistent Networks in Long-Term Intracranial EEG Recordings. J Neurosci. 2011;31:15757–67.PubMedPubMedCentral

67.

Kramer M, Eden U, Cash S, Kolaczyk E. Network inference with confidence from multivariate time series. Phys Rev E. 2009;79.

68.

Siegel M, Donner TH, Engel AK. Spectral fingerprints of large-scale neuronal interactions. Nat Rev Neurosci. 2012;13:121–34.PubMed

69.

Hipp JF, Engel AK, Siegel M. Oscillatory Synchronization in Large-Scale Cortical Networks Predicts Perception. Neuron. 2011;69:387–96.PubMed

70.

Garcia JO, Grossman ED, Srinivasan R. Evoked potentials in large-scale cortical networks elicited by TMS of the visual cortex. J Neurophysiol. 2011;106:1734–46.PubMedPubMedCentral

71.

Varela F, Lachaux JP, Rodriguez E, Martinerie J. The brainweb: phase synchronization and large-scale integration. Nat Rev Neurosci. 2001;2:229–39.PubMed

72.

Benjamini Y, Hochberg Y. Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. J R Stat Soc Ser B Methodol. 1995;57:289–300.

73.

Mitra P, Bokil H. Observed Brain Dynamics. 1 edition. Oxford. New York: Oxford University Press; 2007.

74.

Thut G, Nietzel A, Brandt SA, Pascual-Leone A. α-Band Electroencephalographic Activity over Occipital Cortex Indexes Visuospatial Attention Bias and Predicts Visual Target Detection. J Neurosci. 2006;26:9494–502.PubMed

75.

Worden MS, Foxe JJ, Wang N, Simpson GV. Anticipatory Biasing of Visuospatial Attention Indexed by Retinotopically Specific α-Bank Electroencephalography Increases over Occipital Cortex. J Neurosci. 2000;20:RC63–3.

76.

Goncharova II, McFarland DJ, Vaughan TM, Wolpaw JR. EMG contamination of EEG: spectral and topographical characteristics. Clin Neurophysiol. 2003;114:1580–93.PubMed

77.

Boersma M, Kemner C, de Reus MA, Collin G, Snijders TM, Hofman D, Buitelaar JK, Stam CJ, van den Heuvel MP. Disrupted Functional Brain Networks in Autistic Toddlers. Brain Connect. 2013;3:41–9.PubMed

78.

Isler JR, Martien KM, Grieve PG, Stark RI, Herbert MR. Reduced functional connectivity in visual evoked potentials in children with autism spectrum disorder. Clin Neurophysiol. 2010;121:2035–43.PubMed

79.

Khan S, Gramfort A, Shetty NR, Kitzbichler MG, Ganesan S, Moran JM, Lee SM, Gabrieli JDE, Tager-Flusberg HB, Joseph RM, Herbert MR, Hamalainen MS, Kenet T. Local and long-range functional connectivity is reduced in concert in autism spectrum disorders. Proc Natl Acad Sci. 2013;110:3107–12.PubMedPubMedCentral

80.

Vissers ME, Cohen MX, Geurts HM. Brain connectivity and high functioning autism: a promising path of research that needs refined models, methodological convergence, and stronger behavioral links. Neurosci Biobehav Rev. 2012;36:604–25.PubMed

81.

Weng S-J, Wiggins JL, Peltier SJ, Carrasco M, Risi S, Lord C, Monk CS. Alterations of resting state functional connectivity in the default network in adolescents with autism spectrum disorders. Brain Res. 2010;1313:202–14.PubMed

82.

Fombonne E. The Changing Epidemiology of Autism. J Appl Res Intellect Disabil. 2005;18:281–94.

83.

Newschaffer CJ, Croen LA, Daniels J, Giarelli E, Grether JK, Levy SE, Mandell DS, Miller LA, Pinto-Martin J, Reaven J, Reynolds AM, Rice CE, Schendel D, Windham GC. The Epidemiology of Autism Spectrum Disorders*. Annu Rev Public Health. 2007;28:235–58.PubMed

84.

Baron-Cohen S, Lombardo MV, Auyeung B, Ashwin E, Chakrabarti B, Knickmeyer R. Why Are Autism Spectrum Conditions More Prevalent in Males? PLoS Biol. 2011;9, e1001081.PubMedPubMedCentral

85.

Khouzam HR, El-Gabalawi F, Pirwani N, Priest F. Asperger’s disorder: A review of its diagnosis and treatment. Compr Psychiatry. 2004;45:184–91.PubMed

86.

He BJ, Zempel JM, Snyder AZ, Raichle ME. The Temporal Structures and Functional Significance of Scale-free Brain Activity. Neuron. 2010;66:353–69.PubMedPubMedCentral

87.

Vinck M, Oostenveld R, van Wingerden M, Battaglia F, Pennartz CMA. An improved index of phase-synchronization for electrophysiological data in the presence of volume-conduction, noise and sample-size bias. Neuroimage. 2011;55:1548–65.PubMed

88.

Courchesne E, Pierce K. Why the frontal cortex in autism might be talking only to itself: local over-connectivity but long-distance disconnection. Curr Opin Neurobiol. 2005;15:225–30.PubMed

89.

Lázár AS, Lázár ZI, Bíró A, Győri M, Tárnok Z, Prekop C, Keszei A, Stefanik K, Gádoros J, Halász P. Reduced fronto-cortical brain connectivity during NREM sleep in Asperger syndrome: An EEG spectral and phase coherence study. Clin Neurophysiol. 2010;121:1844–54.PubMed

90.

Mathewson KJ, Jetha MK, Drmic IE, Bryson SE, Goldberg JO, Schmidt LA. Regional EEG alpha power, coherence, and behavioral symptomatology in autism spectrum disorder. Clin Neurophysiol. 2012;123:1798–809.PubMed

91.

Murias M, Webb SJ, Greenson J, Dawson G. Resting state cortical connectivity reflected in EEG coherence in individuals with autism. Biol Psychiatry. 2007;62:270–3.PubMedPubMedCentral

92.

Koldewyn K, Yendiki A, Weigelt S, Gweon H, Julian J, Richardson H, Malloy C, Saxe R, Fischl B, Kanwisher N. Differences in the right inferior longitudinal fasciculus but no general disruption of white matter tracts in children with autism spectrum disorder. Proc Natl Acad Sci. 2014;111:1981–6.PubMedPubMedCentral

93.

Button KS, Ioannidis JPA, Mokrysz C, Nosek BA, Flint J, Robinson ESJ, Munafò MR. Power failure: why small sample size undermines the reliability of neuroscience. Nat Rev Neurosci. 2013;14:365–76.PubMed

94.

Chu-Shore CJ, Kramer MA, Bianchi MT, Caviness VS, Cash SS. Network Analysis: Applications for the Developing Brain. J Child Neurol. 2011;26:488–500.PubMedPubMedCentral

95.

Ecker C, Ronan L, Feng Y, Daly E, Murphy C, Ginestet CE, Brammer M, Fletcher PC, Bullmore ET, Suckling J, Baron-Cohen S, Williams S, Loth E, Murphy DGM, Bailey AJ, Baron-Cohen S, Bolton PF, Bullmore ET, Carrington S, Chakrabarti B, Daly EM, Deoni SC, Ecker C, Happe F, Henty J, Jezzard P, Johnston P, Jones DK, Lai MC, Lombardo MV, et al. Intrinsic gray-matter connectivity of the brain in adults with autism spectrum disorder. Proc Natl Acad Sci. 2013;110:13222–7.PubMedPubMedCentral

96.

Stigler KA, McDonald BC, Anand A, Saykin AJ, McDougle CJ. Structural and functional magnetic resonance imaging of autism spectrum disorders. Brain Res. 2011;1380:146–61.PubMed

97.

Duffy FH, Als H. A stable pattern of EEG spectral coherence distinguishes children with autism from neuro-typical controls-a large case control study. BMC Med. 2012;10:64.PubMedPubMedCentral

98.

Peters JM, Taquet M, Vega C, Jeste SS, Fernández I, Tan J, Nelson CA, Sahin M, Warfield SK. Brain functional networks in syndromic and non-syndromic autism: a graph theoretical study of EEG connectivity. BMC Med. 2013;11:54.PubMedPubMedCentral

99.

Happé F, Ronald A, Plomin R. Time to give up on a single explanation for autism. Nat Neurosci. 2006;9:1218–20.PubMed

100.

Kikuchi M, Shitamichi K, Yoshimura Y, Ueno S, Hiraishi H, Hirosawa T, Munesue T, Nakatani H, Tsubokawa T, Haruta Y, Oi M, Niida Y, Remijn GB, Takahashi T, Suzuki M, Higashida H, Minabe Y. Altered brain connectivity in 3-to 7-year-old children with autism spectrum disorder. NeuroImage Clin. 2013;2:394–401.PubMedPubMedCentral

101.

Monk CS, Peltier SJ, Wiggins JL, Weng S-J, Carrasco M, Risi S, Lord C. Abnormalities of intrinsic functional connectivity in autism spectrum disorders. Neuroimage. 2009;47:764–72.PubMedPubMedCentral

102.

Duffy FH, Shankardass A, McAnulty GB, Als H. The relationship of Asperger’s syndrome to autism: a preliminary EEG coherence study. BMC Med. 2013;11:175.PubMedPubMedCentral

103.

Baron-Cohen S, Wheelwright S, Skinner R, Martin J, Clubley E. The Autism-Spectrum Quotient (AQ): Evidence from Asperger Syndrome/High-Functioning Autism, Malesand Females, Scientists and Mathematicians. J Autism Dev Disord. 2001;31:5–17.PubMed

104.

Hoekstra RA, Vinkhuyzen AAE, Wheelwright S, Bartels M, Boomsma DI, Baron-Cohen S, Posthuma D, van der Sluis S. The Construction and Validation of an Abridged Version of the Autism-Spectrum Quotient (AQ-Short). J Autism Dev Disord. 2011;41:589–96.PubMed

105.

Arfken CL, Carney S, Boutros NN. Translating biological parameters into clinically useful diagnostic tests. Curr Psychiatry Rep. 2009;11:320–3.PubMed

106.

Arfken CL, Joseph A, Sandhu GR, Roehrs T, Douglass AB, Boutros NN. The status of sleep abnormalities as a diagnostic test for major depressive disorder. J Affect Disord. 2014;156:36–45.PubMed

Title: Robust disruptions in electroencephalogram cortical oscillations and large-scale functional networks in autism
Authors: Sean Matlis
Katica Boric
Catherine J. Chu
Mark A. Kramer
Publication date: 01-12-2015
Publisher: BioMed Central
Published in: BMC Neurology / Issue 1/2015
Electronic ISSN: 1471-2377
DOI: https://doi.org/10.1186/s12883-015-0355-8

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Robust disruptions in electroencephalogram cortical oscillations and large-scale functional networks in autism

Abstract

Background

Methods

Results

Conclusions

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

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