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Published in: BMC Medicine 1/2011

Open Access 01-12-2011 | Research article

EEG complexity as a biomarker for autism spectrum disorder risk

Authors: William Bosl, Adrienne Tierney, Helen Tager-Flusberg, Charles Nelson

Published in: BMC Medicine | Issue 1/2011

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Abstract

Background

Complex neurodevelopmental disorders may be characterized by subtle brain function signatures early in life before behavioral symptoms are apparent. Such endophenotypes may be measurable biomarkers for later cognitive impairments. The nonlinear complexity of electroencephalography (EEG) signals is believed to contain information about the architecture of the neural networks in the brain on many scales. Early detection of abnormalities in EEG signals may be an early biomarker for developmental cognitive disorders. The goal of this paper is to demonstrate that the modified multiscale entropy (mMSE) computed on the basis of resting state EEG data can be used as a biomarker of normal brain development and distinguish typically developing children from a group of infants at high risk for autism spectrum disorder (ASD), defined on the basis of an older sibling with ASD.

Methods

Using mMSE as a feature vector, a multiclass support vector machine algorithm was used to classify typically developing and high-risk groups. Classification was computed separately within each age group from 6 to 24 months.

Results

Multiscale entropy appears to go through a different developmental trajectory in infants at high risk for autism (HRA) than it does in typically developing controls. Differences appear to be greatest at ages 9 to 12 months. Using several machine learning algorithms with mMSE as a feature vector, infants were classified with over 80% accuracy into control and HRA groups at age 9 months. Classification accuracy for boys was close to 100% at age 9 months and remains high (70% to 90%) at ages 12 and 18 months. For girls, classification accuracy was highest at age 6 months, but declines thereafter.

Conclusions

This proof-of-principle study suggests that mMSE computed from resting state EEG signals may be a useful biomarker for early detection of risk for ASD and abnormalities in cognitive development in infants. To our knowledge, this is the first demonstration of an information theoretic analysis of EEG data for biomarkers in infants at risk for a complex neurodevelopmental disorder.
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Literature
1.
2.
go back to reference Barabasi AL: Scale-free networks: a decade and beyond. Science. 2009, 325: 412-413. 10.1126/science.1173299.CrossRefPubMed Barabasi AL: Scale-free networks: a decade and beyond. Science. 2009, 325: 412-413. 10.1126/science.1173299.CrossRefPubMed
3.
go back to reference Bassett DS, Bullmore E: Small-world brain networks. Neuroscientist. 2006, 12: 512-523. 10.1177/1073858406293182.CrossRefPubMed Bassett DS, Bullmore E: Small-world brain networks. Neuroscientist. 2006, 12: 512-523. 10.1177/1073858406293182.CrossRefPubMed
4.
go back to reference Ravasz E, Barabási AL: Hierarchical organization in complex networks. Phys Rev E Stat Nonlin Soft Matter Phys. 2003, 67: 026112-10.1103/PhysRevE.67.026112.CrossRefPubMed Ravasz E, Barabási AL: Hierarchical organization in complex networks. Phys Rev E Stat Nonlin Soft Matter Phys. 2003, 67: 026112-10.1103/PhysRevE.67.026112.CrossRefPubMed
5.
go back to reference Supekar K, Musen M, Menon V: Development of large-scale functional brain networks in children. PLoS Biol. 2009, 7: e1000157-10.1371/journal.pbio.1000157.CrossRefPubMedPubMedCentral Supekar K, Musen M, Menon V: Development of large-scale functional brain networks in children. PLoS Biol. 2009, 7: e1000157-10.1371/journal.pbio.1000157.CrossRefPubMedPubMedCentral
6.
go back to reference Noonan SK, Haist F, Muller RA: Aberrant functional connectivity in autism: evidence from low-frequency BOLD signal fluctuations. Brain Res. 2009, 1262: 48-63. 10.1016/j.brainres.2008.12.076.CrossRefPubMedPubMedCentral Noonan SK, Haist F, Muller RA: Aberrant functional connectivity in autism: evidence from low-frequency BOLD signal fluctuations. Brain Res. 2009, 1262: 48-63. 10.1016/j.brainres.2008.12.076.CrossRefPubMedPubMedCentral
7.
go back to reference Johnson MH: Brain Development and Cognition: A Reader. 1993, Cambridge, MA: Blackwell Johnson MH: Brain Development and Cognition: A Reader. 1993, Cambridge, MA: Blackwell
8.
go back to reference Kulisek R, Hrncir Z, Hrdlicka M, Faladova L, Sterbova K, Krsek P, Vymlatilova E, Palus M, Zumrová A, Komárek V: Nonlinear analysis of the sleep EEG in children with pervasive developmental disorder. Neuro Endocrinol Lett. 2008, 29: 512-517.PubMed Kulisek R, Hrncir Z, Hrdlicka M, Faladova L, Sterbova K, Krsek P, Vymlatilova E, Palus M, Zumrová A, Komárek V: Nonlinear analysis of the sleep EEG in children with pervasive developmental disorder. Neuro Endocrinol Lett. 2008, 29: 512-517.PubMed
9.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
10.
go back to reference Belmonte MK, Cook EH, Anderson GM, Rubenstein JL, Greenough WT, Beckel-Mitchener A, Courchesne E, Boulanger LM, Powell SB, Levitt PR, Perry EK, Jiang YH, DeLorey TM, Tierney E: Autism as a disorder of neural information processing: directions for research and targets for therapy. Mol Psychiatry. 2004, 9: 646-663.PubMed Belmonte MK, Cook EH, Anderson GM, Rubenstein JL, Greenough WT, Beckel-Mitchener A, Courchesne E, Boulanger LM, Powell SB, Levitt PR, Perry EK, Jiang YH, DeLorey TM, Tierney E: Autism as a disorder of neural information processing: directions for research and targets for therapy. Mol Psychiatry. 2004, 9: 646-663.PubMed
11.
go back to reference Sörnmo L, Laguna P: Bioelectrical Signal Processing in Cardiac and Neurological Applications. 2005, Boston: Elsevier Academic Press Sörnmo L, Laguna P: Bioelectrical Signal Processing in Cardiac and Neurological Applications. 2005, Boston: Elsevier Academic Press
12.
go back to reference Nunez PL, Srinivasan R: Electric Fields of the Brain: The Neurophysics of EEG. 2006, New York: Oxford University Press, 2CrossRef Nunez PL, Srinivasan R: Electric Fields of the Brain: The Neurophysics of EEG. 2006, New York: Oxford University Press, 2CrossRef
13.
go back to reference Gans F, Schumann AY, Kantelhardt JW, Penzel T, Fietze I: Cross-modulated amplitudes and frequencies characterize interacting components in complex systems. Phys Rev Lett. 2009, 102: 098701-10.1103/PhysRevLett.102.098701.CrossRefPubMed Gans F, Schumann AY, Kantelhardt JW, Penzel T, Fietze I: Cross-modulated amplitudes and frequencies characterize interacting components in complex systems. Phys Rev Lett. 2009, 102: 098701-10.1103/PhysRevLett.102.098701.CrossRefPubMed
14.
go back to reference Van Drongelen W: Signal Processing for Neuroscientists: Introduction to the Analysis of Physiological Signals. 2007, Burlington, MA: Academic Press Van Drongelen W: Signal Processing for Neuroscientists: Introduction to the Analysis of Physiological Signals. 2007, Burlington, MA: Academic Press
15.
go back to reference Cowan WM, Kandel ER: Prospects for neurology and psychiatry. JAMA. 2001, 285: 594-600. 10.1001/jama.285.5.594.CrossRefPubMed Cowan WM, Kandel ER: Prospects for neurology and psychiatry. JAMA. 2001, 285: 594-600. 10.1001/jama.285.5.594.CrossRefPubMed
16.
go back to reference Hyman SE: Can neuroscience be integrated into the DSM-V?. Nat Rev Neurosci. 2007, 8: 725-732. 10.1038/nrn2218.CrossRefPubMed Hyman SE: Can neuroscience be integrated into the DSM-V?. Nat Rev Neurosci. 2007, 8: 725-732. 10.1038/nrn2218.CrossRefPubMed
17.
18.
19.
go back to reference Varela F, Lachaux JP, Rodriguez E, Martinerie J: The brainweb: phase synchronization and large-scale integration. Nat Rev Neurosci. 2001, 2: 229-239. 10.1038/35067550.CrossRefPubMed Varela F, Lachaux JP, Rodriguez E, Martinerie J: The brainweb: phase synchronization and large-scale integration. Nat Rev Neurosci. 2001, 2: 229-239. 10.1038/35067550.CrossRefPubMed
20.
go back to reference Le Van Quyen M: Disentangling the dynamic core: a research program for a neurodynamics at the large-scale. Biol Res. 2003, 36: 67-88. 10.4067/S0716-97602003000100006.CrossRefPubMed Le Van Quyen M: Disentangling the dynamic core: a research program for a neurodynamics at the large-scale. Biol Res. 2003, 36: 67-88. 10.4067/S0716-97602003000100006.CrossRefPubMed
21.
go back to reference Pikovsky A, Rosenblum M, Kurths J: Synchronization: A Universal Concept in Nonlinear Sciences. 2001, Cambridge, UK: Cambridge University PressCrossRef Pikovsky A, Rosenblum M, Kurths J: Synchronization: A Universal Concept in Nonlinear Sciences. 2001, Cambridge, UK: Cambridge University PressCrossRef
22.
go back to reference Stam CJ: Nonlinear dynamical analysis of EEG and MEG: review of an emerging field. Clin Neurophysiol. 2005, 116: 2266-2301. 10.1016/j.clinph.2005.06.011.CrossRefPubMed Stam CJ: Nonlinear dynamical analysis of EEG and MEG: review of an emerging field. Clin Neurophysiol. 2005, 116: 2266-2301. 10.1016/j.clinph.2005.06.011.CrossRefPubMed
23.
go back to reference Costa M, Goldberger AL, Peng CK: Multiscale entropy analysis of biological signals. Phys Rev E Stat Nonlin Soft Matter Phys. 2005, 71: 021906-10.1103/PhysRevE.71.021906.CrossRefPubMed Costa M, Goldberger AL, Peng CK: Multiscale entropy analysis of biological signals. Phys Rev E Stat Nonlin Soft Matter Phys. 2005, 71: 021906-10.1103/PhysRevE.71.021906.CrossRefPubMed
24.
go back to reference Li Y, Tong S, Liu D, Gai Y, Wang X, Wang J, Qiu Y, Zhu Y: Abnormal EEG complexity in patients with schizophrenia and depression. Clin Neurophysiol. 2008, 119: 1232-1241. 10.1016/j.clinph.2008.01.104.CrossRefPubMed Li Y, Tong S, Liu D, Gai Y, Wang X, Wang J, Qiu Y, Zhu Y: Abnormal EEG complexity in patients with schizophrenia and depression. Clin Neurophysiol. 2008, 119: 1232-1241. 10.1016/j.clinph.2008.01.104.CrossRefPubMed
25.
go back to reference Na SH, Jin SH, Kim SY, Ham BJ: EEG in schizophrenic patients: mutual information analysis. Clin Neurophysiol. 2002, 113: 1954-1960. 10.1016/S1388-2457(02)00197-9.CrossRefPubMed Na SH, Jin SH, Kim SY, Ham BJ: EEG in schizophrenic patients: mutual information analysis. Clin Neurophysiol. 2002, 113: 1954-1960. 10.1016/S1388-2457(02)00197-9.CrossRefPubMed
26.
go back to reference Chen W, Zhuang J, Yu W, Wang Z: Measuring complexity using FuzzyEn, ApEn, and SampEn. Med Eng Phys. 2009, 31: 61-68. 10.1016/j.medengphy.2008.04.005.CrossRefPubMed Chen W, Zhuang J, Yu W, Wang Z: Measuring complexity using FuzzyEn, ApEn, and SampEn. Med Eng Phys. 2009, 31: 61-68. 10.1016/j.medengphy.2008.04.005.CrossRefPubMed
27.
go back to reference Kuusela TA, Jartti TT, Tahvanainen KU, Kaila TJ: Nonlinear methods of biosignal analysis in assessing terbutaline-induced heart rate and blood pressure changes. Am J Physiol Heart Circ Physiol. 2002, 282: H773-H783.CrossRefPubMed Kuusela TA, Jartti TT, Tahvanainen KU, Kaila TJ: Nonlinear methods of biosignal analysis in assessing terbutaline-induced heart rate and blood pressure changes. Am J Physiol Heart Circ Physiol. 2002, 282: H773-H783.CrossRefPubMed
28.
go back to reference Scher MS, Ludington-Hoe S, Kaffashi F, Johnson MW, Holditch-Davis D, Loparo KA: Neurophysiologic assessment of brain maturation after an 8-week trial of skin-to-skin contact on preterm infants. Clin Neurophysiol. 2009, 120: 1812-1818. 10.1016/j.clinph.2009.08.004.CrossRefPubMedPubMedCentral Scher MS, Ludington-Hoe S, Kaffashi F, Johnson MW, Holditch-Davis D, Loparo KA: Neurophysiologic assessment of brain maturation after an 8-week trial of skin-to-skin contact on preterm infants. Clin Neurophysiol. 2009, 120: 1812-1818. 10.1016/j.clinph.2009.08.004.CrossRefPubMedPubMedCentral
29.
go back to reference De la Cruz DM, Mañas S, Pereda E, Garrido JM, López S, De Vera L, González JJ: Maturational changes in the interdependencies between cortical brain areas of neonates during sleep. Cereb Cortex. 2007, 17: 583-590. 10.1093/cercor/bhk002.CrossRefPubMed De la Cruz DM, Mañas S, Pereda E, Garrido JM, López S, De Vera L, González JJ: Maturational changes in the interdependencies between cortical brain areas of neonates during sleep. Cereb Cortex. 2007, 17: 583-590. 10.1093/cercor/bhk002.CrossRefPubMed
30.
go back to reference Zhang D, Ding H, Liu Y, Zhou C, Ye D: Neurodevelopment in newborns: a sample entropy analysis of electroencephalogram. Physiol Meas. 2009, 30: 491-504. 10.1088/0967-3334/30/5/006.CrossRefPubMed Zhang D, Ding H, Liu Y, Zhou C, Ye D: Neurodevelopment in newborns: a sample entropy analysis of electroencephalogram. Physiol Meas. 2009, 30: 491-504. 10.1088/0967-3334/30/5/006.CrossRefPubMed
31.
go back to reference Costa MD, Peng CK, Goldberger AL: Multiscale analysis of heart rate dynamics: entropy and time irreversibility measures. Cardiovasc Eng. 2008, 8: 88-93. 10.1007/s10558-007-9049-1.CrossRefPubMedPubMedCentral Costa MD, Peng CK, Goldberger AL: Multiscale analysis of heart rate dynamics: entropy and time irreversibility measures. Cardiovasc Eng. 2008, 8: 88-93. 10.1007/s10558-007-9049-1.CrossRefPubMedPubMedCentral
32.
go back to reference Costa M, Goldberger AL, Peng CK: Broken asymmetry of the human heartbeat: loss of time irreversibility in aging and disease. Phys Rev Lett. 2005, 95: 198102-10.1103/PhysRevLett.95.198102.CrossRefPubMed Costa M, Goldberger AL, Peng CK: Broken asymmetry of the human heartbeat: loss of time irreversibility in aging and disease. Phys Rev Lett. 2005, 95: 198102-10.1103/PhysRevLett.95.198102.CrossRefPubMed
33.
go back to reference Gautama T, Mandic DP, Van Hulle MM: Indications of nonlinear structures in brain electrical activity. Phys Rev E Stat Nonlin Soft Matter Phys. 2003, 67: 046204-10.1103/PhysRevE.67.046204.CrossRefPubMed Gautama T, Mandic DP, Van Hulle MM: Indications of nonlinear structures in brain electrical activity. Phys Rev E Stat Nonlin Soft Matter Phys. 2003, 67: 046204-10.1103/PhysRevE.67.046204.CrossRefPubMed
34.
go back to reference Ozonoff S, Iosif AM, Baguio F, Cook IC, Hill MM, Hutman T, Rogers SJ, Rozga A, Sangha S, Sigman M, Steinfeld MB, Young GS: A prospective study of the emergence of early behavioral signs of autism. J Am Acad Child Adolesc Psychiatry. 2010, 49: 256-266. e1-2PubMedPubMedCentral Ozonoff S, Iosif AM, Baguio F, Cook IC, Hill MM, Hutman T, Rogers SJ, Rozga A, Sangha S, Sigman M, Steinfeld MB, Young GS: A prospective study of the emergence of early behavioral signs of autism. J Am Acad Child Adolesc Psychiatry. 2010, 49: 256-266. e1-2PubMedPubMedCentral
35.
go back to reference Zwaigenbaum L, Bryson S, Rogers T, Roberts W, Brian J, Szatmari P: Behavioral manifestations of autism in the first year of life. Int J Dev Neurosci. 2005, 23: 143-152. 10.1016/j.ijdevneu.2004.05.001.CrossRefPubMed Zwaigenbaum L, Bryson S, Rogers T, Roberts W, Brian J, Szatmari P: Behavioral manifestations of autism in the first year of life. Int J Dev Neurosci. 2005, 23: 143-152. 10.1016/j.ijdevneu.2004.05.001.CrossRefPubMed
36.
go back to reference Zwaigenbaum L, Thurm A, Stone W, Baranek G, Bryson S, Iverson J, Kau A, Klin A, Lord C, Landa R, Rogers S, Sigman M: Studying the emergence of autism spectrum disorders in high-risk infants: methodological and practical issues. J Autism Dev Disord. 2007, 37: 466-480. 10.1007/s10803-006-0179-x.CrossRefPubMed Zwaigenbaum L, Thurm A, Stone W, Baranek G, Bryson S, Iverson J, Kau A, Klin A, Lord C, Landa R, Rogers S, Sigman M: Studying the emergence of autism spectrum disorders in high-risk infants: methodological and practical issues. J Autism Dev Disord. 2007, 37: 466-480. 10.1007/s10803-006-0179-x.CrossRefPubMed
37.
go back to reference Elsabbagh M, Volein A, Holmboe K, Tucker L, Csibra G, Baron-Cohen S, Bolton P, Charman T, Baird G, Johnson MH: Visual orienting in the early broader autism phenotype: disengagement and facilitation. J Child Psychol Psychiatry. 2009, 50: 637-642. 10.1111/j.1469-7610.2008.02051.x.CrossRefPubMedPubMedCentral Elsabbagh M, Volein A, Holmboe K, Tucker L, Csibra G, Baron-Cohen S, Bolton P, Charman T, Baird G, Johnson MH: Visual orienting in the early broader autism phenotype: disengagement and facilitation. J Child Psychol Psychiatry. 2009, 50: 637-642. 10.1111/j.1469-7610.2008.02051.x.CrossRefPubMedPubMedCentral
38.
go back to reference Courchesne E, Carper R, Akshoomoff N: Evidence of brain overgrowth in the first year of life in autism. JAMA. 2003, 290: 337-344. 10.1001/jama.290.3.337.CrossRefPubMed Courchesne E, Carper R, Akshoomoff N: Evidence of brain overgrowth in the first year of life in autism. JAMA. 2003, 290: 337-344. 10.1001/jama.290.3.337.CrossRefPubMed
39.
go back to reference Courchesne E, Pierce K, Schumann CM, Redcay E, Buckwalter JA, Kennedy DP, Morgan J: Mapping early brain development in autism. Neuron. 2007, 56: 399-413. 10.1016/j.neuron.2007.10.016.CrossRefPubMed Courchesne E, Pierce K, Schumann CM, Redcay E, Buckwalter JA, Kennedy DP, Morgan J: Mapping early brain development in autism. Neuron. 2007, 56: 399-413. 10.1016/j.neuron.2007.10.016.CrossRefPubMed
40.
go back to reference Elder LM, Dawson G, Toth K, Fein D, Munson J: Head circumference as an early predictor of autism symptoms in younger siblings of children with autism spectrum disorder. J Autism Dev Disord. 2008, 38: 1104-1111. 10.1007/s10803-007-0495-9.CrossRefPubMed Elder LM, Dawson G, Toth K, Fein D, Munson J: Head circumference as an early predictor of autism symptoms in younger siblings of children with autism spectrum disorder. J Autism Dev Disord. 2008, 38: 1104-1111. 10.1007/s10803-007-0495-9.CrossRefPubMed
41.
go back to reference Xie HB, He WX, Liu H: Measuring time series regularity using nonlinear similarity-based sample entropy. Phys Lett A. 2008, 372: 7140-7146. 10.1016/j.physleta.2008.10.049.CrossRef Xie HB, He WX, Liu H: Measuring time series regularity using nonlinear similarity-based sample entropy. Phys Lett A. 2008, 372: 7140-7146. 10.1016/j.physleta.2008.10.049.CrossRef
42.
go back to reference Schreiber T, Schmitz A: Discrimination power of measures for nonlinearity in a time series. Phys Rev E Stat Nonlin Soft Matter Phys. 1997, 55: 5443-5447. 10.1103/PhysRevE.55.5443.CrossRef Schreiber T, Schmitz A: Discrimination power of measures for nonlinearity in a time series. Phys Rev E Stat Nonlin Soft Matter Phys. 1997, 55: 5443-5447. 10.1103/PhysRevE.55.5443.CrossRef
43.
go back to reference Demšar J, Zupan B, Leban G, Curk T: Orange: from experimental machine learning to interactive data mining. Lecture Notes in Computer Science. Edited by: Boulicaut JF, Esposito F, Giannotti F, Pedreschi D. 2004, Berlin: Springer, 3202: 537-539. Knowledge Discovery in Databases: PKDD 2004, 8th European Conference on Principles and Practice of Knowledge Discovery in Databases, Pisa, Italy, September 20-24, 2004, Proceedings Demšar J, Zupan B, Leban G, Curk T: Orange: from experimental machine learning to interactive data mining. Lecture Notes in Computer Science. Edited by: Boulicaut JF, Esposito F, Giannotti F, Pedreschi D. 2004, Berlin: Springer, 3202: 537-539. Knowledge Discovery in Databases: PKDD 2004, 8th European Conference on Principles and Practice of Knowledge Discovery in Databases, Pisa, Italy, September 20-24, 2004, Proceedings
44.
go back to reference Golland P, Fischl B: Permutation tests for classification: towards statistical significance in image-based studies. Inf Process Med Imaging. 2003, 18: 330-341. full_text.CrossRefPubMed Golland P, Fischl B: Permutation tests for classification: towards statistical significance in image-based studies. Inf Process Med Imaging. 2003, 18: 330-341. full_text.CrossRefPubMed
45.
go back to reference Norris PR, Stein PK, Morris JA: Reduced heart rate multiscale entropy predicts death in critical illness: a study of physiologic complexity in 285 trauma patients. J Crit Care. 2008, 23: 399-405. 10.1016/j.jcrc.2007.08.001.CrossRefPubMed Norris PR, Stein PK, Morris JA: Reduced heart rate multiscale entropy predicts death in critical illness: a study of physiologic complexity in 285 trauma patients. J Crit Care. 2008, 23: 399-405. 10.1016/j.jcrc.2007.08.001.CrossRefPubMed
46.
go back to reference Behne T, Carpenter M, Call J, Tomasello M: Unwilling versus unable: infants' understanding of intentional action. Dev Psychol. 2005, 41: 328-337. 10.1037/0012-1649.41.2.328.CrossRefPubMed Behne T, Carpenter M, Call J, Tomasello M: Unwilling versus unable: infants' understanding of intentional action. Dev Psychol. 2005, 41: 328-337. 10.1037/0012-1649.41.2.328.CrossRefPubMed
47.
go back to reference Rivera-Gaxiola M, Silva-Pereyra J, Kuhl PK: Brain potentials to native and non-native speech contrasts in 7- and 11-month-old American infants. Dev Sci. 2005, 8: 162-172. 10.1111/j.1467-7687.2005.00403.x.CrossRefPubMed Rivera-Gaxiola M, Silva-Pereyra J, Kuhl PK: Brain potentials to native and non-native speech contrasts in 7- and 11-month-old American infants. Dev Sci. 2005, 8: 162-172. 10.1111/j.1467-7687.2005.00403.x.CrossRefPubMed
48.
go back to reference Pascalis O, de Haan M, Nelson CA: Is face processing species-specific during the first year of life?. Science. 2002, 296: 1321-1323. 10.1126/science.1070223.CrossRefPubMed Pascalis O, de Haan M, Nelson CA: Is face processing species-specific during the first year of life?. Science. 2002, 296: 1321-1323. 10.1126/science.1070223.CrossRefPubMed
49.
go back to reference Marcus DJ, Nelson CA: Neural bases and development of face recognition in autism. CNS Spectr. 2001, 6: 36-59.PubMed Marcus DJ, Nelson CA: Neural bases and development of face recognition in autism. CNS Spectr. 2001, 6: 36-59.PubMed
51.
go back to reference Kuhl PK: Is speech learning 'gated' by the social brain?. Dev Sci. 2007, 10: 110-120. 10.1111/j.1467-7687.2007.00572.x.CrossRefPubMed Kuhl PK: Is speech learning 'gated' by the social brain?. Dev Sci. 2007, 10: 110-120. 10.1111/j.1467-7687.2007.00572.x.CrossRefPubMed
52.
go back to reference Janjarasjitt S, Scher MS, Loparo KA: Nonlinear dynamical analysis of the neonatal EEG time series: the relationship between neurodevelopment and complexity. Clin Neurophysiol. 2008, 119: 822-836. 10.1016/j.clinph.2007.11.012.CrossRefPubMed Janjarasjitt S, Scher MS, Loparo KA: Nonlinear dynamical analysis of the neonatal EEG time series: the relationship between neurodevelopment and complexity. Clin Neurophysiol. 2008, 119: 822-836. 10.1016/j.clinph.2007.11.012.CrossRefPubMed
53.
go back to reference Lippé S, Kovacevic N, McIntosh AR: Differential maturation of brain signal complexity in the human auditory and visual system. Front Hum Neurosci. 2009, 3: 48.CrossRefPubMedPubMedCentral Lippé S, Kovacevic N, McIntosh AR: Differential maturation of brain signal complexity in the human auditory and visual system. Front Hum Neurosci. 2009, 3: 48.CrossRefPubMedPubMedCentral
54.
go back to reference Shaw P, Greenstein D, Lerch J, Clasen L, Lenroot R, Gogtay N, Evans A, Rapoport J, Giedd J: Intellectual ability and cortical development in children and adolescents. Nature. 2006, 440: 676-679. 10.1038/nature04513.CrossRefPubMed Shaw P, Greenstein D, Lerch J, Clasen L, Lenroot R, Gogtay N, Evans A, Rapoport J, Giedd J: Intellectual ability and cortical development in children and adolescents. Nature. 2006, 440: 676-679. 10.1038/nature04513.CrossRefPubMed
55.
go back to reference Sakkalis V, Tsiaras V, Michalopoulos K, Zervakis M: Assessment of neural dynamic coupling and causal interactions between independent EEG components from cognitive tasks using linear and nonlinear methods. Conf Proc IEEE Eng Med Biol Soc. 2008, 2008: 3767-3770.PubMed Sakkalis V, Tsiaras V, Michalopoulos K, Zervakis M: Assessment of neural dynamic coupling and causal interactions between independent EEG components from cognitive tasks using linear and nonlinear methods. Conf Proc IEEE Eng Med Biol Soc. 2008, 2008: 3767-3770.PubMed
56.
go back to reference Sauseng P, Klimesch W: What does phase information of oscillatory brain activity tell us about cognitive processes?. Neurosci Biobehav Rev. 2008, 32: 1001-1013. 10.1016/j.neubiorev.2008.03.014.CrossRefPubMed Sauseng P, Klimesch W: What does phase information of oscillatory brain activity tell us about cognitive processes?. Neurosci Biobehav Rev. 2008, 32: 1001-1013. 10.1016/j.neubiorev.2008.03.014.CrossRefPubMed
Metadata
Title
EEG complexity as a biomarker for autism spectrum disorder risk
Authors
William Bosl
Adrienne Tierney
Helen Tager-Flusberg
Charles Nelson
Publication date
01-12-2011
Publisher
BioMed Central
Published in
BMC Medicine / Issue 1/2011
Electronic ISSN: 1741-7015
DOI
https://doi.org/10.1186/1741-7015-9-18

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