A stable pattern of EEG spectral coherence distinguishes children with autism from neuro-typical controls - a large case control study

BMC Medicine

Volumn 10, Issue , 2012, Pages

  Duffy, Frank H ^a   Als, Heidelise ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

Autism spectrum disorder; Coherence factors; Discriminant analysis; Eeg coherence; Pca; Pdd; Pervasive developmental disorder; Principal components analysis

Indexed keywords

ADOLESCENT; ADULT; ARTICLE; ARTIFACT; AUTISM; BRAIN FUNCTION; CASE CONTROL STUDY; CHILD; CLINICAL CLASSIFICATION; COMPUTER PROGRAM; CONTROLLED STUDY; ELECTROENCEPHALOGRAM; ELECTROENCEPHALOGRAPHY; FEMALE; HUMAN; INFANTILE AUTISM; MAJOR CLINICAL STUDY; MALE; PHENOTYPE; PRESCHOOL CHILD; PRINCIPAL COMPONENT ANALYSIS; SCHOOL CHILD; AGE; INFANT; NERVE CELL NETWORK; PATHOLOGY; PATHOPHYSIOLOGY; REPRODUCIBILITY;

ADOLESCENT; AGE FACTORS; AUTISTIC DISORDER; CASE-CONTROL STUDIES; CHILD; CHILD, PRESCHOOL; ELECTROENCEPHALOGRAPHY; HUMANS; INFANT; NERVE NET; PRINCIPAL COMPONENT ANALYSIS; REPRODUCIBILITY OF RESULTS;

EID: 84862679346     PISSN: None     EISSN: 17417015     Source Type: Journal    
DOI: 10.1186/1741-7015-10-64     Document Type: Article

References (80)

1. American Psychiatric Association Diagnostic and Statistical Manual of Mental Disorders Fourth Edition Text Revision (DSM-IV-TR) 2000, Washington, DC: American Psychiatric Publishing, Inc., American Psychiatric Association, American Psychiatric Association.
2. Rapin I. Autism. N Engl J Med 1997, 337:97-104. 10.1056/NEJM199707103370206, 9211680.
3. Shah A, Frith U. An islet of ability in autistic children: a research note. J Child Psychol Psychiatr 1983, 24:613-620.
4. Chakrabarti S, Fombonne E. Pervasive developmental disorders in preschool children. JAMA 2001, 285:3093-3099. 10.1001/jama.285.24.3093, 11427137.
5. Manning SE, Davin CA, Barfield WD, Kotelchuck M, Clements K, Diop H, Osbahr T, Smith LA. Early diagnoses of autism spectrum disorders in Massachusetts birth cohorts, 2001-2005. Pediatrics 2011, 127:1043-1051. 10.1542/peds.2010-2943, 21576313.
6. Bailey A, Le Couteur A, Gottesman I, Bolton P, Simonoff E, Yuzada E, Rutter M. Autism as a strongly genetic disorder: evidence from a British twin study. Psychol Med 1995, 52:63-77.
7. Folstein S, Rutter M. Infantile autism: a genetic study of 21 twin pairs. J Child Psychol Psychiatr 1977, 18:297-321.
8. Steffenburg S, Gillberg C, Steffenburg U. Psychiatric disorders in children and adolescents with mental retardation and active epilepsy. Arch Neurol 1996, 53:904-912. 10.1001/archneur.1996.00550090114017, 8815856.
9. Hallmayer J, Cleveland S, Torres A, Phillips J, Cohen B, Torigue T, Miller J, Fedele A, Collins J, Smith K, Lotspeich L, Croen LA, Ozonoff S, Lajonchere C, Grether JK, Risch N. Genetic heritability and shared environmental factors among twin pairs with autism. Arch Gen Psychiatry 2011, 68:1095-1102. 10.1001/archgenpsychiatry.2011.76, 21727249.
10. Risch N, Spiker D, Lotspeich L, Nouri N, Hinds D, Hallmayer J, Kalaydjieva L, McCague P, Dimicelli S, Pitts T, Nguyen L, Yang J, Harper C, Thorpe D, Vermeer S, Young H, Hebert J, Lin A, Ferguson J, Chiotti C, Wiese-Slater S, Rogers T, Salmon B, Nicholas P, Petersen PB, Pingree C, McMahon W, Wong DL, Cavalli-Sforza LL, Kraemer HC, et al. A genomic screen of autism: evidence for a multilocus etiology. Am J Hum Genet 1999, 65:493-507. 10.1086/302497, 1377948, 10417292.
11. Sakai Y, Shaw CA, Dawson BC, Dugas DV, Al-Mohaseb Z, Hill DE, Zoghbi HY. Protein interactome reveals converging molecular pathways among autism disorders. Sci Transl Med 2011, 3:86. 86ra49.
12. Voineaugu I, Wang X, Johnston P, Lowe JK, Tian Y, Horvath S, Mill J, Cantor RM, Blencowe BJ, Geschwind DH. Transcriptomic analysis of autistic brain reveals convergent molecular pathology. Nature 2011, 474:380-384. 10.1038/nature10110, 21614001.
13. Herbert MR. Large brains in autism: the challenge of pervasive abnormality. Neuroscientist 2005, 11:417-440. 10.1177/0091270005278866, 16151044.
14. Pina-Camacho L, Villero S, Fraguas D, Boada L, Janssen J, Navas-Sánchez F, Mayoral M, Llorente C, Arango C, Parellada M. Autism spectrum disorder: does neuroimaging support the DSM-5 proposal for a symptom dyad? A systematic review of functional magnetic resonance imaging and diffusion tensor imaging studies. J Autism Dev Disord 2011,
15. Anagnostou E, Taylor M. Review of neuroimaging in autism spectrum disorders: what have we learned and where we go from here. Mol Autism 2011, 2:4. 10.1186/2040-2392-2-4, 3102613, 21501488.
16. Chen R, Jiao Y, Herskovits EH. Structural MRI in autism spectrum disorder. Pediatr Res 2011, 69:63R-68R. 10.1203/PDR.0b013e318212c2b3, 3081653, 21289538.
17. Just M, Cherkassky V, Keller T, Kana R, Minshew N. Functional and anatomical cortical underconnectivity in autism: evidence from an fMRI study of an executive function task and corpus callosum morphometry. Cerebral Cortex 2007, 17:951-961.
18. Just MACV, Keller TA, Kana RK, Minshew NJ. Cortical activation and synchronization during sentence comprehension in high functioning autism: evidence of underconnectivity. Brain 2004, 127:1811-1821. 10.1093/brain/awh199, 15215213.
19. Ben Bashat D, Kornfield-Duenias V, Zachar DA, Ekstein PM, Hendler T, Tarrasch R, Even A, Levy Y, Ben Sira L. Accelerated maturation of white matter in young children with autism: a high b value DWI study. Neuroimaging 2010, 35:40-47.
20. Cheng Y, Chou KH, Fan YT, Decety J, Lin C. Atypical development of white matter microstructure in adolescents with autism spectrum disorders. Neuroimage 2010, 50:873-882. 10.1016/j.neuroimage.2010.01.011, 20074650.
21. Cantor DS, Thatcher RW, Hrybyk M, Kaye H. Computerized EEG analysis of autistic children. J Autism Dev Disord 1986, 16:169-187. 10.1007/BF01531728, 3722118.
22. Murias M, Webb SJ, Greenson J, Dawson G. Resting state cortical connectivity reflected in EEG coherence in individuals with autism. Biol Psychiatr 2007, 62:270-273.
23. Coben R, Clarke AR, Hudspeth W, Barry RJ. EEG power and coherence in autistic spectrum disorder. Clin Neurophysiol 2008, 119:1002-1009. 10.1016/j.clinph.2008.01.013, 18331812.
24. Lazarev VV, Pontes A, Mitrofanov AA, deAzevedo LC. Interhemispheric asymmetry in EEG photic driving coherence in childhood autism. Clin Neurophysiol 2009, 121:145-152.
25. 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, 121:2035-2043. 10.1016/j.clinph.2010.05.004, 20605520.
26. Sheikhani A, Behnam H, Mohammadi MR, Noroozian M, Mohammadi M. Detection of abnormalities for diagnosing of children with autism disorders using of quantitative electroencephalography analysis. J Med Syst 2010, 36:957-963.
27. Leveille C, Barbeau EB, Bolduc C, Limoges E, Berthiaume C, Chevrier E, 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, 3:280-285. 10.1002/aur.155, 20717953.
28. 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. Neuropsychologia 2011, 49:254-263. 10.1016/j.neuropsychologia.2010.11.024, 21110988.
29. Srinivasan R, Winter WR, Ding J, Nunez PL. EEG and MEG coherence: measures of functional connectivity at distinct spatial scales of neocortical dynamics. J Neurosci Methods 2007, 166:41-52. 10.1016/j.jneumeth.2007.06.026, 2151962, 17698205.
30. van Drongelen W. Signal Processing for Neuroscientists: An Introduction to the Analysis of Physiological Signals 2011, 5. Oxford: Elsevier.
31. Nunez PL. Electric Fields of the Brain 1981, New York: Oxford University Press.
32. Happe F, Ronald A, Plomin A. Time to give up on a single explanation for autism. Nat Neurosci 2006, 9:1218-1220. 10.1038/nn1770, 17001340.
33. Milne E. Increased intra-participant variability in children with autistic spectrum disorders: evidence from single trial analysis of evoked EEG data. Front Psychol 2011, 2:51. 3110871, 21716921.
34. Le Couteur A, Lord C, Rutter M. The Autism Diagnostic Interview-Revised (ADI-R) 2003, Torrance, CA: Western Psychological Services.
35. Lord C. Autism Diagnostic Observation Schedule-Toddler Module (ADOS-T). 2009, Torrance, CA: Western Psychological Services (WPS).
36. Lord C, Risi S, Lambrecht L, Cook EH, Leventhal BL, DiLavore PC, Pickles A, Rutter M. The Autism Diagnostic Observation Schedule-Generic: a standard measure of social and communication deficits associated with the spectrum of autism. J Autism Dev Disord 2000, 30:205-223. 10.1023/A:1005592401947, 11055457.
37. Press WH, Teukolsky SA, Vetterling WT, Flannery BP. Numerical Recipes in C; the Art of Scientific Computing 1995, Cambridge, England: Cambridge University Press, 2.
38. Duffy FH. Issues facing the clinical use of brain electrical activity. Functional Brain Imaging 1988, 149-160. Stuttgart: Hans Huber Publishers, Pfurtscheller G, Lopes da Silva F.
39. Duffy FH, Jones K, Bartels P, McAnulty G, Albert M. Unrestricted principal components analysis of brain electrical activity: Issues of data dimensionality, artifact, and utility. Brain Topogr 1992, 4:291-307. 10.1007/BF01135567, 1510873.
40. Karson CN, Coppola R, Morihisa JM, Weinberger DR. Computed electroencephalographic activity mapping in schizophrenia. The resting state reconsidered. Arch Gen Psychiatry 1987, 44:514-517. 10.1001/archpsyc.1987.01800180024003, 3495249.
41. Zar JH. Biostatistical Analysis 1984, Englewood Cliffs, N. J.: Prentice Hall.
42. Lins OG, Picton TW, Berg P, Scherg M. Ocular artifacts in recording EEGs and event-related potentials. II: Source dipoles and source components. Brain Topogr 1993, 6:65-78. 10.1007/BF01234128, 8260328.
43. Berg P, Scherg M. Dipole modeling of eye activity and its application to the removal of eye artifacts from EEG and MEG. Clin Phys Physiol Meas 1991, 12(Suppl A):49-54.
44. Perrin F, Pernier J, Bertrand O, Echallier JF. Spherical splines for scalp potential; and current density mapping. Electroencephalogr Clin Neurophysiol 1989, 72:184-187. 10.1016/0013-4694(89)90180-6, 2464490.
45. Nunez PL, Silberstein RB, Shi Z, Carpenter MR, Srinvasan R, Tucker DM, Doran SM, Cadusch PJ, Wijesinghe RS. EEG coherency II: experimental comparisons of multiple measures. Clin Neurophysiol 1999, 110:469-486. 10.1016/S1388-2457(98)00043-1, 10363771.
46. Sun FT, Miller LM, D'Esposito M. Measuring interregional functional connectivity using coherence and partial coherence analysis of fMRI data. Neuroimage 2004, 21:647-658. 10.1016/j.neuroimage.2003.09.056, 14980567.
47. Fiecas FM, Ombao H, Linkletter C, Thompson W, Sanes J. Functional connectivity: Shrinkage estimation and randomization test. Neuroimage 2010, 49:3005-3014. 10.1016/j.neuroimage.2009.12.022, 3128923, 20006714.
48. Fiecas M, Ombao H. The generalized shrinkage estimator for the analysis of functional connectivity of brain signals. Ann Applied Stat 2011, 5:1102-1125.
49. Duffy FH, McAnulty GM, McCreary MC, Cuchural GJ, Komaroff AL. EEG spectral coherence data distinguish chronic fatigue syndrome patients from healthy controls and depressed patients - a case control study. BMC Neurol 2011, 11:82. 10.1186/1471-2377-11-82, 3146818, 21722376.
50. Semlitch HV, Anderer P, Schuster P, Presslich O. A solution for reliable and valid reduction of ocular artifacts, applied to the P300 ERP. Psychophysiology 1986, 23:695-703. 10.1111/j.1469-8986.1986.tb00696.x, 3823345.
51. Dixon WJ. BMDP Statistical Software Manual 1988, Berkeley: University of California Press.
52. Bartels PH. Numerical evaluation of cytologic data. IX. Search for data structure by principal components transformation. Anal Quant Cytol 1981, 3:167-177.
53. Duffy FH, Jones KH, McAnulty GB, Albert MS. Spectral coherence in normal adults: unrestricted principal components analysis - relation of factors to age, gender, and neuropsychologic data. Clin Electroencephalogr 1995, 26:30-46.
54. Golub GH, Kahane W. Calculating the singular values and pseudo-inverse of a matrix. J Numer Anal 1965, 2:202-224.
55. Kaiser HJ. A Varimax criterion for analytic rotation in factor analysis. Psychometrika 1958, 23:187-200.
56. Golub GH. Matrix Computations 1989, Baltimore, MD: Johns Hopkins University Press, 2.
57. Duffy FH, Als H, McAnulty GB. Infant EEG spectral coherence data during quiet sleep: unrestricted principal components analysis - relation of factors to gestational age, medical risk, and neurobehavioral status. Clin Electroencephalogr 2003, 34:54-69.
58. Cooley WW, Lohnes PR. Multivariate Data Analysis 1971, New York: J. Wiley and Sons.
59. Bartels PH. Numerical evaluation of cytologic data IV. discrimination and classification. Anal Quant Cytol 1980, 2:19-24.
60. Marascuilo LA, Levin JR. Multivariate Statistics in the Social Sciences, A Researchers Guide 1983, Monterey, CA: Brooks/Cole Publishing Co..
61. Lachenbruch PA. Discriminant Analysis 1975, New York: Hafner Press.
62. Lachenbruch P, Mickey RM. Estimation of error rates in discriminant analysis. Technometrics 1968, 10:1-11.
63. Duffy FH, Burchfiel JL, Lombroso CT. Brain electrical activity mapping (BEAM): A method for extending the clinical utility of EEG and evoked potential data. Ann Neurol 1979, 5:309-321. 10.1002/ana.410050402, 443765.
64. Duffy FH, Bartels PH, Burchfiel JL. Significance probability mapping: an aid in the topographic analysis of brain electrical activity. Electroencephalogr Clin Neurophysiol 1981, 51:455-462. 10.1016/0013-4694(81)90221-2, 6165544.
65. Hughes JR. EEG in Clinical Practice 1994, Boston: Butterworth-Heineman, 2.
66. Gasser T, Verleger R, Bacher P, Sroka L. Development of the EEG of school-age children and adolescents. I. Analysis of band power. Electroencephalogr Clin Neurophysiol 1988, 69:91-99. 10.1016/0013-4694(88)90204-0, 2446839.
67. Matthis P, Scheffner D, Benninger C, Lipinski C, Stolzis L. Changes in the background activity of the electroencephalogram according to age. Electroencephalogr Clin Neurophysiol 1980, 49:626-635. 10.1016/0013-4694(80)90403-4, 6158442.
68. Whiteley P, Todd L, Carr K, Shattock P. Gender ratios in autism, Asperger syndrome and autism spectrum disorder. Autism Insights 2010, 2:17-24.
69. Miles TR, Haslum MN, Wheeler TJ. Gender ratio in dyslexia. Ann Dyslexia 1998, 48:27-55.
70. Rutter M, Caspi A, Fergusson D, Horwood LJ, Goodman R, Maughn B, Moffitt TE, Meltzer H, Carroll J. Sex differences in developmental reading disability: New findings from 4 epidemiological studies. JAMA 2004, 291:2007-2012. 10.1001/jama.291.16.2007, 15113820.
71. Wing L, Gould J, Gillberg C. Autism spectrum disorders in the DSM-V: better or worse than the DSM-IV?. Res Dev Disabil 2011, 32:768-773. 10.1016/j.ridd.2010.11.003, 21208775.
72. Belmonte MK, Allen G, Beckel-Mitchener A, Boulanger LM, Carper RA, Webb SJ. Autism and abnormal development of brain connectivity. J Neurosci 2004, 24:9228-9231. 10.1523/JNEUROSCI.3340-04.2004, 15496656.
73. Cherkassky VL, Kana RK, Keller TA, Just MA. Functional connectivity in a baseline resting-state network in autism. NeuroReport 2006, 17:1687-1690. 10.1097/01.wnr.0000239956.45448.4c, 17047454.
74. 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, 15:225-230. 10.1016/j.conb.2005.03.001, 15831407.
75. Markram H, Rinaldi T, Markram K. The intense world syndrome - an alternative hypothesis for autism. Front Neurosci 2007, 1:77-96. 10.3389/neuro.01.1.1.006.2007, 2518049, 18982120.
76. Wicker B, Fonlupt P, Hubert B, Tardif C, Gepner B, Deruelle C. Abnormal cerebral effective connectivity during explicit emotional processing in adults with autism spectrum disorder. Soc Cogn Affect Neurosci 2008, 3:135-143. 10.1093/scan/nsn007, 2555468, 19015104.
77. Fletcher PT, Whitaker RT, Tao R, DuBray MB, Froehlich A, Ravichandran C, Alexander AL, Bigler ED, Lange N, Lainhart JE. Microstructural connectivity of the arcuate fasciculus in adolescents with high-functioning autism. Neuroimage 2010, 51:1117-1125. 10.1016/j.neuroimage.2010.01.083, 2966943, 20132894.
78. Spence SJ, Schneider MT. The role of epilepsy and epileptiform EEGs in autism spectrum disorders. Pediatr Res 2009, 65:599-606. 10.1203/PDR.0b013e31819e7168, 2692092, 19454962.
79. Fink DG, Beaty HW. Standard Handbook in Electrical Engineering 2006, New York, NY: McGraw-Hill Professional, 15.
80. Bosl W, Tierney A, Tager-Flusberg H, Nelson C. EEG complexity as a biomarker for autism spectrum disorder risk. BMC Med 2011, 9:18. 10.1186/1741-7015-9-18, 3050760, 21342500.