Transient and steady-state auditory gamma-band responses in first-degree relatives of people with autism spectrum disorder

Donald C Rojas, Peter D Teale, Keeran Maharajh, Eugene Kronberg, Katie Youngpeter, Lisa B Wilson, Alissa Wallace, Susan Hepburn, Donald C Rojas, Peter D Teale, Keeran Maharajh, Eugene Kronberg, Katie Youngpeter, Lisa B Wilson, Alissa Wallace, Susan Hepburn

Abstract

Background: Stimulus-related γ-band oscillations, which may be related to perceptual binding, are reduced in people with autism spectrum disorders (ASD). The purpose of this study was to examine auditory transient and steady-state γ-band findings in first-degree relatives of people with ASD to assess the potential familiality of these findings in ASD.

Methods: Magnetoencephalography (MEG) recordings in 21 parents who had a child with an autism spectrum disorder (pASD) and 20 healthy adult control subjects (HC) were obtained. Gamma-band phase locking factor (PLF), and evoked and induced power to 32, 40 and 48 Hz amplitude-modulated sounds were measured for transient and steady-state responses. Participants were also tested on a number of behavioral and cognitive assessments related to the broad autism phenotype (BAP).

Results: Reliable group differences were seen primarily for steady-state responses. In the left hemisphere, pASD subjects exhibited lower phase-locked steady-state power in all three conditions. Total γ-band power, including the non-phase-locked component, was also reduced in the pASD group. In addition, pASD subjects had significantly lower PLF than the HC group. Correlations were seen between MEG measures and BAP measures.

Conclusions: The reduction in steady-state γ-band responses in the pASD group is consistent with previous results for children with ASD. Steady-state responses may be more sensitive than transient responses to phase-locking errors in ASD. Together with the lower PLF and phase-locked power in first-degree relatives, correlations between γ-band measures and behavioral measures relevant to the BAP highlight the potential of γ-band deficits as a potential new autism endophenotype.

Figures

Figure 1
Figure 1
Phase-locking factor results. Phase-locking factor (PLF) group results (mean ± SE) for the left and right hemisphere dipole waveforms (shown in left and right columns respectively). Results for the transient and steady-state responses are shown in the top and bottom rows respectively.
Figure 2
Figure 2
Evoked power results. Baseline normalized evoked amplitude group results (mean ± SE) for the left and right hemisphere dipole waveforms (shown in left and right columns respectively). Results for the transient and steady-state responses are shown in the top and bottom rows respectively.
Figure 3
Figure 3
Scatter plots of correlation results. (A)Transient γ-band response (tGBR) phase-locking factor (PLF) and evoked power; (B) auditory steady-state response (ASSR) PLF and evoked power; (C) tGBR PLF and Autism-specturm Quotient (AQ) communication subscale; (D) ASSR PLF and AQ communication subscale; (E) tGBR evoked power and SRS; (F) ASSR evoked power and Social Responsiveness Scale (SRS). Black lines indicate linear regression line.
Figure 4
Figure 4
Data example. (A) Unfiltered time-domain average 248-sensor waveforms from single subject. (B) Unfiltered, averaged dipole waveform for right auditory cortex corresponding to data in A. (C) Waveform in B filtered using a 35 to 45 Hz bandpass to emphasize γ-band in time-domain (not part of data analysis). (D) Time-frequency representation of phase-locked, baseline-normalized evoked power from same waveform in (B). (E) Time-frequency representation of phase-locking factor (PLF) corresponding to data in (B).

References

    1. Center for Disease Control. Prevalence of autism spectrum disorders: Autism and developmental disabilities monitoring network, United States, 2006. MMWR Surveillance Summaries. 2009;58:1–20.
    1. Kielinen M, Rantala H, Timonen E, Linna SL, Moilanen I. Associated medical disorders and disabilities in children with autistic disorder: a population-based study. Autism. 2004;8:49–60. doi: 10.1177/1362361304040638.
    1. Schaefer GB, Lutz RE. Diagnostic yield in the clinical genetic evaluation of autism spectrum disorders. Genet Med. 2006;8:549–556.
    1. Bailey A, Le Couteur A, Gottesman I, Bolton P, Simonoff E, Yuzda E, Rutter M. Autism as a strongly genetic disorder: evidence from a British twin study. Psychol Med. 1995;25:63–77. doi: 10.1017/S0033291700028099.
    1. Steffenburg S, Gillberg C, Hellgren L, Andersson L, Gillberg IC, Jakobsson G, Bohman M. A twin study of autism in Denmark, Finland, Iceland, Norway and Sweden. Journal of Child Psychology & Psychiatry & Allied Disciplines. 1989;30:405–416. doi: 10.1111/j.1469-7610.1989.tb00254.x.
    1. Losh M, Childress D, Lam K, Piven J. Defining key features of the broad autism phenotype: A comparison across parents of multiple- and single-incidence autism families. American Journal of Medical Genetics Part B: Neuropsychiatric Genetics. 2008;147B:424–433. doi: 10.1002/ajmg.b.30612.
    1. Piven J, Palmer P. Psychiatric disorder and the broad autism phenotype: evidence from a family study of multiple-incidence autism families. Am J Psychiatry. 1999;156:557–563.
    1. Piven J, Palmer P, Landa R, Santangelo S, Jacobi D, Childress D. Personality and language characteristics in parents from multiple-incidence autism families. American Journal of Medical Genetics. 1997;74:398–411. doi: 10.1002/(SICI)1096-8628(19970725)74:4<398::AID-AJMG11>;2-D.
    1. Landa R, Piven J, Wzorek MM, Gayle JO, Chase GA, Folstein SE. Social language use in parents of autistic individuals. Psychological Medicine. 1992;22:245–254. doi: 10.1017/S0033291700032918.
    1. Folstein SE, Santangelo SL, Gilman SE, Piven J, Landa R, Lainhart J, Hein J, Wzorek M. Predictors of cognitive test patterns in autism families. J Child Psychol Psychiatry. 1999;40:1117–1128. doi: 10.1111/1469-7610.00528.
    1. Fidler DJ, Bailey JN, Smalley SL. Macrocephaly in autism and other pervasive developmental disorders. Dev Med Child Neurol. 2000;42:737–740. doi: 10.1017/S0012162200001365.
    1. Lainhart JE, Bigler ED, Bocian M, Coon H, Dinh E, Dawson G, Deutsch CK, Dunn M, Estes A, Tager-Flusberg H. et al.Head circumference and height in autism: A study by the collaborative program of excellence in autism. American Journal of Medical Genetics Part A. 2006;140A:2257–2274. doi: 10.1002/ajmg.a.31465.
    1. Rojas DC, Smith JA, Benkers TL, Camou SL, Reite ML, Rogers SJ. Hippocampus and amygdala volumes in parents of children with autistic disorder. Am J Psychiatry. 2004;161:2038–2044. doi: 10.1176/appi.ajp.161.11.2038.
    1. Peterson E, Schmidt GL, Tregellas JR, Winterrowd E, Kopelioff L, Hepburn S, Reite M, Rojas DC. A voxel-based morphometry study of gray matter in parents of children with autism. Neuroreport. 2006;17:1289–1292. doi: 10.1097/01.wnr.0000233087.15710.87.
    1. Koczat DL, Rogers SJ, Pennington BF, Ross RG. Eye movement abnormality suggestive of a spatial working memory deficit is present in parents of autistic probands. J Autism Dev Disord. 2002;32:513–518. doi: 10.1023/A:1021246712459.
    1. Mosconi MW, Kay M, D'Cruz AM, Guter S, Kapur K, Macmillan C, Stanford LD, Sweeney JA. Neurobehavioral abnormalities in first-degree relatives of individuals with autism. Arch Gen Psychiatry. 2010;67:830–840. doi: 10.1001/archgenpsychiatry.2010.87.
    1. Abramson R, Wright H, Carpenter R, Brennan W, Lumpuy O, Cole E, Young S. Elevated blood serotonin in autistic probands and their first-degree relatives. Journal of Autism and Developmental Disorders. 1989;19:397–407. doi: 10.1007/BF02212938.
    1. Dawson G, Webb SJ, Wijsman E, Schellenberg G, Estes A, Munson J, Faja S. Neurocognitive and electrophysiological evidence of altered face processing in parents of children with autism: implications for a model of abnormal development of social brain circuitry in autism. Dev Psychopathol. 2005;17:679–697.
    1. Rojas DC, Maharajh K, Teale P, Rogers SJ. Reduced neural synchronization of gamma-band MEG oscillations in first-degree relatives of children with autism. BMC Psychiatry. 2008;8:66. doi: 10.1186/1471-244X-8-66.
    1. Boudreau JC. Computer Analysis of Electrical Activity in the Olfactory System of the Cat. Nature. 1964;201:155–158. doi: 10.1038/201155a0.
    1. Freeman WJ. Mass Action in the Nervous System. New York: Academic Press; 1975.
    1. Brock J, Brown CC, Boucher J, Rippon G. The temporal binding deficit hypothesis of autism. Dev Psychopathol. 2002;14:209–224.
    1. Rippon G, Brock J, Brown C, Boucher J. Disordered connectivity in the autistic brain: Challenges for the 'new psychophysiology'. Int J Psychophysiol. 2007;63:164–172. doi: 10.1016/j.ijpsycho.2006.03.012.
    1. 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. doi: 10.1523/JNEUROSCI.3340-04.2004.
    1. Uhlhaas PJ, Singer W. Neural synchrony in brain disorders: relevance for cognitive dysfunctions and pathophysiology. Neuron. 2006;52:155–168. doi: 10.1016/j.neuron.2006.09.020.
    1. Bartos M, Vida I, Jonas P. Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nat Rev Neurosci. 2007;8:45–56. doi: 10.1038/nrn2044.
    1. Pantev C, Makeig S, Hoke M, Galambos R, Hampson S, Gallen C. Human auditory evoked gamma-band magnetic fields. Proc Natl Acad Sci USA. 1991;88:8996–9000. doi: 10.1073/pnas.88.20.8996.
    1. Azzena GB, Conti G, Santarelli R, Ottaviani F, Paludetti G, Maurizi M. Generation of human auditory steady-state responses (SSRs). I: Stimulus rate effects. Hear Res. 1995;83:1–8. doi: 10.1016/0378-5955(94)00184-R.
    1. Hari R, Hamalainen M, Joutsiniemi SL. Neuromagnetic steady-state responses to auditory stimuli. Journal of the Acoustical Society of America. 1989;86:1033–1039. doi: 10.1121/1.398093.
    1. Ross B, Picton TW, Pantev C. Temporal integration in the human auditory cortex as represented by the development of the steady-state magnetic field. Hear Res. 2002;165:68–84. doi: 10.1016/S0378-5955(02)00285-X.
    1. Gutschalk A, Mase R, Roth R, Ille N, Rupp A, Hahnel S, Picton TW, Scherg M. Deconvolution of 40 Hz steady-state fields reveals two overlapping source activities of the human auditory cortex. Clinical Neurophysiology. 1999;110:856–868. doi: 10.1016/S1388-2457(99)00019-X.
    1. Presacco A, Bohórquez J, Yavuz E, Ozdamar O. Auditory steady-state responses to 40-Hz click trains: relationship to middle latency, gamma band and beta band responses studied with deconvolution. Clin Neurophysiol. 2010;121:1540–1550. doi: 10.1016/j.clinph.2010.03.020.
    1. Santarelli R, Conti G. Generation of auditory steady-state responses: linearity assessment. Scand Audiol Suppl. 1999;51:23–32.
    1. Santarelli R, Maurizi M, Conti G, Ottaviani F, Paludetti G, Pettorossi VE. Generation of human auditory steady-state responses (SSRs). II: Addition of responses to individual stimuli. Hear Res. 1995;83:9–18. doi: 10.1016/0378-5955(94)00185-S.
    1. Wilson TW, Rojas DC, Reite ML, Teale PD, Rogers SJ. Children and Adolescents with Autism Exhibit Reduced MEG Steady-State Gamma Responses. Biol Psychiatry. 2007;62:192–197. doi: 10.1016/j.biopsych.2006.07.002.
    1. Brown C, Gruber T, Boucher J, Rippon G, Brock J. Gamma abnormalities during perception of illusory figures in autism. Cortex. 2005;41:364–376. doi: 10.1016/S0010-9452(08)70273-9.
    1. Grice S, Spratling MW, Karmiloff-Smith A, Halit H, Csibra G, de Haan M, Johnson MH. Disordered visual processing and oscillatory brain activity in autism and Williams syndrome. Neuroreport. 2001;12:2697–2700. doi: 10.1097/00001756-200108280-00021.
    1. Orekhova EV, Stroganova TA, Nygren G, Tsetlin MM, Posikera IN, Gillberg C, Elam M. Excess of high frequency electroencephalogram oscillations in boys with autism. Biol Psychiatry. 2007;62:1022–1029. doi: 10.1016/j.biopsych.2006.12.029.
    1. Gandal MJ, Edgar JC, Ehrlichman RS, Mehta M, Roberts TPL, Siegel SJ. Validating γ Oscillations and Delayed Auditory Responses as Translational Biomarkers of Autism. Biological Psychiatry. 2010;68:1100–1106. doi: 10.1016/j.biopsych.2010.09.031.
    1. Stapells DR, Makeig S, Galambos R. Auditory steady-state responses: threshold prediction using phase coherence. Electroencephalogr Clin Neurophysiol. 1987;67:260–270. doi: 10.1016/0013-4694(87)90024-1.
    1. Baron-Cohen S, Wheelwright S, Skinner R, Martin J, Clubley E. The autism-spectrum quotient (AQ): evidence from Asperger syndrome/high-functioning autism, males and females, scientists and mathematicians. J Autism Dev Disord. 2001;31:5–17. doi: 10.1023/A:1005653411471.
    1. Constantino JN, Todd RD. Intergenerational transmission of subthreshold autistic traits in the general population. Biol Psychiatry. 2005;57:655–660. doi: 10.1016/j.biopsych.2004.12.014.
    1. Rojas DC, Bawn SD, Benkers TL, Reite ML, Rogers SJ. Smaller left hemisphere planum temporale in adults with autistic disorder. Neuroscience Letters. 2002;323:237–240.
    1. Rojas DC, Camou SL, Reite ML, Rogers SJ. Planum temporale volume in children and adolescents with autism. J Autism Dev Disord. 2005;35:479–486. doi: 10.1007/s10803-005-5038-7.
    1. De Fosse L, Hodge SM, Makris N, Kennedy DN, Caviness VS, McGrath L, Steele S, Ziegler DA, Herbert MR, Frazier JA. et al.Language-association cortex asymmetry in autism and specific language impairment. Ann Neurol. 2004;56:757–766. doi: 10.1002/ana.20275.
    1. Herbert MR, Ziegler DA, Deutsch CK, O'Brien LM, Kennedy DN, Filipek PA, Bakardjiev AI, Hodgson J, Takeoka M, Makris N, Caviness VS Jr. Brain asymmetries in autism and developmental language disorder: a nested whole-brain analysis. Brain. 2005;128:213–226.
    1. Spencer KM, Niznikiewicz MA, Nestor PG, Shenton ME, McCarley RW. Left auditory cortex gamma synchronization and auditory hallucination symptoms in schizophrenia. BMC neuroscience. 2009;10:85. doi: 10.1186/1471-2202-10-85.
    1. Teale P, Collins D, Maharajh K, Rojas DC, Kronberg E, Reite M. Cortical source estimates of gamma band amplitude and phase are different in schizophrenia. Neuroimage. 2008;42:1481–1489. doi: 10.1016/j.neuroimage.2008.06.020.
    1. Ross B, Herdman AT, Pantev C. Right hemispheric laterality of human 40 Hz auditory steady-state responses. Cereb Cortex. 2005;15:2029–2039. doi: 10.1093/cercor/bhi078.
    1. Schoonhoven R, Boden CJ, Verbunt JP, de Munck JC. A whole head MEG study of the amplitude-modulation-following response: phase coherence, group delay and dipole source analysis. Clin Neurophysiol. 2003;114:2096–2106. doi: 10.1016/S1388-2457(03)00200-1.
    1. Ross B, Pantev C. Auditory steady-state responses reveal amplitude modulation gap detection thresholds. J Acoust Soc Am. 2004;115:2193–2206. doi: 10.1121/1.1694996.
    1. Gloveli T, Dugladze T, Saha S, Monyer H, Heinemann U, Traub RD, Whittington MA, Buhl EH. Differential involvement of oriens/pyramidale interneurones in hippocampal network oscillations in vitro. J Physiol. 2005;562:131–147.
    1. Whittington MA, Traub RD, Jefferys JG. Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature. 1995;373:612–615. doi: 10.1038/373612a0.
    1. Hajos N, Palhalmi J, Mann EO, Nemeth B, Paulsen O, Freund TF. Spike timing of distinct types of GABAergic interneuron during hippocampal gamma oscillations in vitro. J Neurosci. 2004;24:9127–9137. doi: 10.1523/JNEUROSCI.2113-04.2004.
    1. Brunel N, Wang XJ. What determines the frequency of fast network oscillations with irregular neural discharges? I. Synaptic dynamics and excitation-inhibition balance. J Neurophysiol. 2003;90:415–430. doi: 10.1152/jn.01095.2002.
    1. Muthukumaraswamy SD, Singh KD, Swettenham JB, Jones DK. Visual gamma oscillations and evoked responses: variability, repeatability and structural MRI correlates. Neuroimage. 2010;49:3349–3357. doi: 10.1016/j.neuroimage.2009.11.045.
    1. Muthukumaraswamy SD, Edden RA, Jones DK, Swettenham JB, Singh KD. Resting GABA concentration predicts peak gamma frequency and fMRI amplitude in response to visual stimulation in humans. Proc Natl Acad Sci USA. 2009;106:8356–8361. doi: 10.1073/pnas.0900728106.
    1. Edden RA, Muthukumaraswamy SD, Freeman TC, Singh KD. Orientation discrimination performance is predicted by GABA concentration and gamma oscillation frequency in human primary visual cortex. J Neurosci. 2009;29:15721–15726. doi: 10.1523/JNEUROSCI.4426-09.2009.
    1. Gogolla N, LeBlanc JJ, Quast KB, Südhof TC, Fagiolini M, Hensch TK. Common circuit defect of excitatory-inhibitory balance in mouse models of autism. Journal of Neurodevelopmental Disorders. 2009;1:172–181. doi: 10.1007/s11689-009-9023-x.
    1. Hussman JP. Suppressed GABAergic inhibition as a common factor in suspected etiologies of autism. J Autism Dev Disord. 2001;31:247–248. doi: 10.1023/A:1010715619091.
    1. Blatt GJ, Fitzgerald CM, Guptill JT, Booker AB, Kemper TL, Bauman ML. Density and distribution of hippocampal neurotransmitter receptors in autism: an autoradiographic study. Journal of Autism & Developmental Disorders. 2001;31:537–543. doi: 10.1023/A:1013238809666.
    1. Fatemi SH, Reutiman TJ, Folsom TD, Thuras PD. GABA(A) receptor downregulation in brains of subjects with autism. J Autism Dev Disord. 2009;39:223–230. doi: 10.1007/s10803-008-0646-7.
    1. Dhossche D, Applegate H, Abraham A, Maertens P, Bland L, Bencsath A, Martinez J. Elevated plasma gamma-aminobutyric acid (GABA) levels in autistic youngsters: stimulus for a GABA hypothesis of autism. Med Sci Monit. 2002;8:PR1–6.
    1. Yip J, Soghomonian JJ, Blatt GJ. Decreased GAD67 mRNA levels in cerebellar Purkinje cells in autism: pathophysiological implications. Acta Neuropathol (Berl) 2007;113:559–568. doi: 10.1007/s00401-006-0176-3.
    1. Fatemi SH, Halt AR, Stary JM, Kanodia R, Schulz SC, Realmuto GR. Glutamic acid decarboxylase 65 and 67 kDa proteins are reduced in autistic parietal and cerebellar cortices. Biol Psychiatry. 2002;52:805–810. doi: 10.1016/S0006-3223(02)01430-0.
    1. Page LA, Daly E, Schmitz N, Simmons A, Toal F, Deeley Q, Ambery F, McAlonan GM, Murphy KC, Murphy DG. In vivo 1H-magnetic resonance spectroscopy study of amygdala-hippocampal and parietal regions in autism. Am J Psychiatry. 2006;163:2189–2192. doi: 10.1176/appi.ajp.163.12.2189.
    1. Shinohe A, Hashimoto K, Nakamura K, Tsujii M, Iwata Y, Tsuchiya KJ, Sekine Y, Suda S, Suzuki K, Sugihara G. et al.Increased serum levels of glutamate in adult patients with autism. Prog Neuropsychopharmacol Biol Psychiatry. 2006;30:1472–1477. doi: 10.1016/j.pnpbp.2006.06.013.
    1. Fatemi SH. The hyperglutamatergic hypothesis of autism. Prog Neuropsychopharmacol Biol Psychiatry. 2008;32:911. doi: 10.1016/j.pnpbp.2007.11.004. author reply 912-913.
    1. Rubenstein JL, Merzenich MM. Model of autism: increased ratio of excitation/inhibition in key neural systems. Genes Brain Behav. 2003;2:255–267. doi: 10.1034/j.1601-183X.2003.00037.x.
    1. Basirat A, Sato M, Schwartz J, Kahane P, Lachaux J. Parieto-frontal gamma band activity during the perceptual emergence of speech forms. Neuroimage. 2008;42:404–413. doi: 10.1016/j.neuroimage.2008.03.063.
    1. Kaiser J. Hearing Lips: Gamma-band Activity During Audiovisual Speech Perception. Cerebral Cortex. 2004;15:646–653. doi: 10.1093/cercor/bhh166.
    1. Lutzenberger W, Pulvermuller F, Birbaumer N. Words and pseudowords elicit distinct patterns of 30-Hz EEG responses in humans. Neurosci Lett. 1994;176:115–118. doi: 10.1016/0304-3940(94)90884-2.
    1. Benasich A, Gou Z, Choudhury N, Harris K. Early cognitive and language skills are linked to resting frontal gamma power across the first 3 years. Behavioural Brain Research. 2008;195:215–222. doi: 10.1016/j.bbr.2008.08.049.
    1. Elsabbagh M, Volein A, Csibra G, Holmboe K, Garwood H, Tucker L, Krljes S, Baron-Cohen S, Bolton P, Charman T. et al.Neural correlates of eye gaze processing in the infant broader autism phenotype. Biol Psychiatry. 2009;65:31–38. doi: 10.1016/j.biopsych.2008.09.034.
    1. Virkud YV, Todd RD, Abbacchi AM, Zhang Y, Constantino JN. Familial aggregation of quantitative autistic traits in multiplex versus simplex autism. American Journal of Medical Genetics Part B: Neuropsychiatric Genetics. 2009;150B:328–334. doi: 10.1002/ajmg.b.30810.
    1. Wheelwright S, Auyeung B, Allison C, Baron-Cohen S. Defining the broader, medium and narrow autism phenotype among parents using the Autism Spectrum Quotient (AQ) Mol Autism. 2010;1:10. doi: 10.1186/2040-2392-1-10.
    1. Kwon JS, O'Donnell BF, Wallenstein GV, Greene RW, Hirayasu Y, Nestor PG, Hasselmo ME, Potts GF, Shenton ME, McCarley RW. Gamma frequency-range abnormalities to auditory stimulation in schizophrenia. Arch Gen Psychiatry. 1999;56:1001–1005. doi: 10.1001/archpsyc.56.11.1001.
    1. Hong LE, Summerfelt A, McMahon R, Adami H, Francis G, Elliott A, Buchanan RW, Thaker GK. Evoked gamma band synchronization and the liability for schizophrenia. Schizophr Res. 2004;70:293–302. doi: 10.1016/j.schres.2003.12.011.
    1. Hall MH, Taylor G, Sham P, Schulze K, Rijsdijk F, Picchioni M, Toulopoulou T, Ettinger U, Bramon E, Murray RM, Salisbury DF. The Early Auditory Gamma-Band Response Is Heritable and a Putative Endophenotype of Schizophrenia. Schizophr Bull. 2009.
    1. 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. doi: 10.1023/A:1005592401947.
    1. Lord C, Rutter M, Le Couteur A. Autism Diagnostic Interview - Revised: A revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. Journal of Autism and Developmental Disorders. 1994;25:659–685.
    1. Psychological Corporation. The Wechsler Abbreviated Scale of Intelligence. San Antonio, TX: Harcourt Brace and Company; 1999.
    1. Hollingshead AB. Four factor index of social position. New Haven, CT: Yale University; 1975.
    1. Tesche CD, Uusitalo MA, Ilmoniemi RJ, Huotilainen M, Kajola M, Salonen O. Signal-space projections of MEG data characterize both distributed and well-localized neuronal sources. Electroencephalogr Clin Neurophysiol. 1995;95:189–200. doi: 10.1016/0013-4694(95)00064-6.
    1. Torrence C, Compo GP. A practical guide to wavelet analysis. Bulletin of the American Meteorological Society. 1998;79:61–78. doi: 10.1175/1520-0477(1998)079<0061:APGTWA>;2.
    1. Tallon-Baudry C, Bertrand O, Delpuech C, Pernier J. Stimulus specificity of phase-locked and non-phase-locked 40 Hz visual responses in human. J Neurosci. 1996;16:4240–4249.
    1. Makeig S, Debener S, Onton J, Delorme A. Mining event-related brain dynamics. Trends Cogn Sci. 2004;8:204–210. doi: 10.1016/j.tics.2004.03.008.

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