Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

Keynote webinar | Spotlight on medication adherence

LIVE: Thursday 27th June 2024, 18:00-19:30 (CEST)
Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.
ADVANCED SEARCH
Log in
Top
BMC Psychiatry
Published in: BMC Psychiatry 1/2012

Open Access 01-12-2012 | Research article

Abnormalities in gamma-band responses to language stimuli in first-degree relatives of children with autism spectrum disorder: an MEG study

Authors: Kristina L McFadden, Susan Hepburn, Erin Winterrowd, Gwenda L Schmidt, Donald C Rojas

Published in: BMC Psychiatry | Issue 1/2012

Login to get access

Abstract

Background

Synchronous neural oscillatory activity in the gamma range (30–80 Hz) has been shown to be abnormal in individuals with autism spectrum disorders (ASD) and their first-degree relatives in response to simple auditory stimuli. Gamma-band abnormalities in ASD probands have been seen in response to language stimuli, but this has not been investigated in first-degree relatives. This is of particular interest given that language impairments are a core symptom of ASD and may be part of the broad autism phenotype (BAP) seen in relatives.

Methods

Magnetoencephalography recordings during a continuous word recognition task were obtained for 23 parents of a child with ASD (pASD) and 28 adult control participants. Total and evoked gamma-band activity, as well as inter-trial phase-locking factor (PLF), were measured in response to the task. Beta-band activity was also measured, due to its suggested role in language processing. Participants completed a series of language measures to assess the relationship between brain activity and language function, and lateralization of task-related activity was assessed.

Results

The pASD group showed increased evoked gamma and beta activity, while controls had decreased evoked activity. Additionally, while both groups showed a reduction in total gamma power (commonly seen in language tasks), this reduction was more prominent in the control group. The pASD group demonstrated significantly worse performance on a measure of phonology compared to controls. Significant but distinct relationships were found between gamma/beta activity and language measures within the two groups. In addition, while the overall task generally elicited left lateralized responses, pASD showed greater left lateralization than controls in some regions of interest.

Conclusions

Abnormalities in oscillatory responses to language were seen in pASD that are consistent with previous findings in ASD probands. Gamma-band responses to language stimuli have not previously been assessed in first-degree relatives of ASD probands and these findings are supportive of gamma-band activity as a heritable, neurophysiological biomarker of ASD. The possible relationship seen between language function and neural activity in the current study should be investigated further to assess if oscillatory response abnormalities may contribute to behavioural manifestations of the BAP.
Appendix
Available only for authorised users
Literature
1.
American Psychiatric Association: Diagnostic and Statistical Manual of Mental Disorders. 1994, Washington, D.C: American Psychiatric Association, 4
2.
Centers for Disease Control: Prevalance of autism spectrum disorders: autism and developmental disabilities monitoring network, United States, 2006. MMWR CDC Surveill Summ. 2009, 58: 1-20.
3.
Tallon-Baudry C, Bertrand O: Oscillatory gamma activity in humans and its role in object representation. Trends Cogn Sci. 1999, 3: 151-162. 10.1016/S1364-6613(99)01299-1.CrossRefPubMed
4.
Roach BJ, Mathalon DH: Event-related EEG time-frequency analysis: an overview of measures and an analysis of early gamma band phase locking in schizophrenia. Schizophr Bull. 2008, 34: 907-926. 10.1093/schbul/sbn093.CrossRefPubMedPubMedCentral
5.
Tiitinen H, Sinkkonen J, Reinikainen K, Alho K, Lavikainen J, Naatanen R: Selective attention enhances the auditory 40-Hz transient response in humans. Nature. 1993, 364: 59-60. 10.1038/364059a0.CrossRefPubMed
6.
Taylor K, Mandon S, Freiwald WA, Kreiter AK: Coherent oscillatory activity in monkey area v4 predicts successful allocation of attention. Cereb Cortex. 2005, 15: 1424-1437.CrossRefPubMed
7.
Lakatos P, Karmos G, Mehta AD, Ulbert I, Schroeder CE: Entrainment of neuronal oscillations as a mechanism of attentional selection. Science. 2008, 320: 110-113. 10.1126/science.1154735.CrossRefPubMed
8.
Tallon-Baudry C, Bertrand O, Peronnet F, Pernier J: Induced gamma-band activity during the delay of a visual short-term memory task in humans. J Neurosci. 1998, 18: 4244-4254.PubMed
9.
Pipa G, Stadtler ES, Rodriguez EF, Waltz JA, Muckli LF, Singer W, Goebel R, Munk MH: Performance- and stimulus-dependent oscillations in monkey prefrontal cortex during short-term memory. Front Integr Neurosci. 2009, 3: 25-CrossRefPubMedPubMedCentral
10.
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. 10.1073/pnas.88.20.8996.CrossRefPubMedPubMedCentral
11.
Pantev C, Elbert T, Makeig S, Hampson S, Eulitz C, Hoke M: Relationship of transient and steady-state auditory evoked fields. Electroencephalogr Clin Neurophysiol. 1993, 88: 389-396. 10.1016/0168-5597(93)90015-H.CrossRefPubMed
12.
Pulvermuller F, Eulitz C, Pantev C, Mohr B, Feige B, Lutzenberger W, Elbert T, Birbaumer N: High-frequency cortical responses reflect lexical processing: an MEG study. Electroencephalogr Clin Neurophysiol. 1996, 98: 76-85. 10.1016/0013-4694(95)00191-3.CrossRefPubMed
13.
Ihara A, Hirata M, Sakihara K, Izumi H, Takahashi Y, Kono K, Imaoka H, Osaki Y, Kato A, Yoshimine T, Yorifuji S: Gamma-band desynchronization in language areas reflects syntactic process of words. Neurosci Lett. 2003, 339: 135-138. 10.1016/S0304-3940(03)00005-3.CrossRefPubMed
14.
Pena M, Melloni L: Brain oscillations during spoken sentence processing. J Cogn Neurosci. 2012, 24: 1149-1164. 10.1162/jocn_a_00144.CrossRefPubMed
15.
Tavabi K, Embick D, Roberts TP: Spectral-temporal analysis of cortical oscillations during lexical processing. NeuroReport. 2011, 22: 474-478. 10.1097/WNR.0b013e3283476b84.CrossRefPubMed
16.
Gray CM, Konig P, Engel AK, Singer W: Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature. 1989, 338: 334-337. 10.1038/338334a0.CrossRefPubMed
17.
Singer W: Neuronal synchrony: a versatile code for the definition of relations?. Neuron. 1999, 24: 49-65. 10.1016/S0896-6273(00)80821-1. 111–125CrossRefPubMed
18.
Allen G, Courchesne E: Attention function and dysfunction in autism. Front Biosci. 2001, 6: D105-D119. 10.2741/allen.CrossRefPubMed
19.
Goldstein G, Johnson CR, Minshew NJ: Attentional processes in autism. J Autism Dev Disord. 2001, 31: 433-440. 10.1023/A:1010620820786.CrossRefPubMed
20.
Brock J, Brown CC, Boucher J, Rippon G: The temporal binding deficit hypothesis of autism. Dev Psychopathol. 2002, 14: 209-224.CrossRefPubMed
21.
22.
Kern JK, Trivedi MH, Garver CR, Grannemann BD, Andrews AA, Savla JS, Johnson DG, Mehta JA, Schroeder JL: The pattern of sensory processing abnormalities in autism. Autism. 2006, 10: 480-494. 10.1177/1362361306066564.CrossRefPubMed
23.
Ames C, Fletcher-Watson S: A review of methods in the study of attention in autism. Dev Rev. 2010, 30: 52-73. 10.1016/j.dr.2009.12.003.CrossRef
24.
Marco EJ, Hinkley LB, Hill SS, Nagarajan SS: Sensory processing in autism: a review of neurophysiologic findings. Pediatr Res. 2011, 69: 48R-54R. 10.1203/PDR.0b013e3182130c54.CrossRefPubMedPubMedCentral
25.
Grice SJ, 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. 10.1097/00001756-200108280-00021.CrossRefPubMed
26.
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. 10.1016/j.biopsych.2006.07.002.CrossRefPubMed
27.
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: 66-10.1186/1471-244X-8-66.CrossRefPubMedPubMedCentral
28.
Gandal MJ, Edgar JC, Ehrlichman RS, Mehta M, Roberts TP, Siegel SJ: Validating gamma oscillations and delayed auditory responses as translational biomarkers of autism. Biol Psychiatry. 2010, 68: 1100-1106. 10.1016/j.biopsych.2010.09.031.CrossRefPubMed
29.
Braeutigam S, Swithenby SJ, Bailey AJ: Contextual integration the unusual way: a magnetoencephalographic study of responses to semantic violation in individuals with autism spectrum disorders. Eur J Neurosci. 2008, 27: 1026-1036. 10.1111/j.1460-9568.2008.06064.x.CrossRefPubMed
30.
Rojas DC, Teale PD, Maharajh K, Kronberg E, Youngpeter K, Wilson L, Wallace A, Hepburn S: Transient and steady-state auditory gamma-band responses in first-degree relatives of people with autism spectrum disorder. Mol Autism. 2011, 2: 11-10.1186/2040-2392-2-11.CrossRefPubMedPubMedCentral
31.
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. 10.1017/S0033291700028099.CrossRefPubMed
32.
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. J Child Psychol Psychiatry. 1989, 30: 405-416. 10.1111/j.1469-7610.1989.tb00254.x.CrossRefPubMed
33.
Hallmayer J, Cleveland S, Torres A, Phillips J, Cohen B, Torigoe T, Miller J, Fedele A, Collins J, Smith K, et al: Genetic heritability and shared environmental factors among twin pairs with autism. Arch Gen Psychiatry. 2011, 68: 1095-1102. 10.1001/archgenpsychiatry.2011.76.CrossRefPubMedPubMedCentral
34.
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.PubMed
35.
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. Am J Med Genet B Neuropsychiatr Genet. 2008, 147B: 424-433. 10.1002/ajmg.b.30612.CrossRefPubMedPubMedCentral
36.
Xiang J, Wilson D, Otsubo H, Ishii R, Chuang S: Neuromagnetic spectral distribution of implicit processing of words. NeuroReport. 2001, 12: 3923-3927. 10.1097/00001756-200112210-00014.CrossRefPubMed
37.
Hirata M, Kato A, Taniguchi M, Saitoh Y, Ninomiya H, Ihara A, Kishima H, Oshino S, Baba T, Yorifuji S, Yoshimine T: Determination of language dominance with synthetic aperture magnetometry: comparison with the Wada test. NeuroImage. 2004, 23: 46-53. 10.1016/j.neuroimage.2004.05.009.CrossRefPubMed
38.
Lee SY, Kim JS, Chung CK, Lee SK, Kim WS: Assessment of language dominance by event-related oscillatory changes in an auditory language task: magnetoencephalography study. J Clin Neurophysiol. 2010, 27: 263-269. 10.1097/WNP.0b013e3181eaaf3c.CrossRefPubMed
39.
Papanicolaou AC, Simos PG, Castillo EM, Breier JI, Sarkari S, Pataraia E, Billingsley RL, Buchanan S, Wheless J, Maggio V, Maggio WW: Magnetocephalography: a noninvasive alternative to the Wada procedure. J Neurosurg. 2004, 100: 867-876. 10.3171/jns.2004.100.5.0867.CrossRefPubMed
40.
Piven J, Palmer P, Landa R, Santangelo S, Jacobi D, Childress D: Personality and language characteristics in parents from multiple-incidence autism families. Am J Med Genet. 1997, 74: 398-411. 10.1002/(SICI)1096-8628(19970725)74:4<398::AID-AJMG11>3.0.CO;2-D.CrossRefPubMed
41.
Bailey A, Palferman S, Heavey L, Le Couteur A: Autism: the phenotype in relatives. J Autism Dev Disord. 1998, 28: 369-392. 10.1023/A:1026048320785.CrossRefPubMed
42.
Engel AK, Fries P: Beta-band oscillations–signalling the status quo?. Curr Opin Neurobiol. 2010, 20: 156-165. 10.1016/j.conb.2010.02.015.CrossRefPubMed
43.
Arnal LH, Wyart V, Giraud AL: Transitions in neural oscillations reflect prediction errors generated in audiovisual speech. Nat Neurosci. 2011, 14: 797-801. 10.1038/nn.2810.CrossRefPubMed
44.
Hirata M, Koreeda S, Sakihara K, Kato A, Yoshimine T, Yorifuji S: Effects of the emotional connotations in words on the frontal areas–a spatially filtered MEG study. NeuroImage. 2007, 35: 420-429. 10.1016/j.neuroimage.2006.11.025.CrossRefPubMed
45.
46.
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. 10.1016/j.biopsych.2006.12.029.CrossRefPubMed
47.
Flagg EJ, Cardy JE, Roberts W, Roberts TP: Language lateralization development in children with autism: insights from the late field magnetoencephalogram. Neurosci Lett. 2005, 386: 82-87. 10.1016/j.neulet.2005.05.037.CrossRefPubMed
48.
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.CrossRefPubMed
49.
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. J Autism Dev Disord. 1994, 24: 659-685. 10.1007/BF02172145.CrossRefPubMed
50.
Hollingshead A: Four-Factor Index of Social Status. 1975, New Haven, CT: Yale University Press
51.
Annett M: Left, right, hand, and brain: the right shift theory. 1985, UK: Hove
52.
Dunn LM, Dunn LM: PPVT-III: Peabody Picture Vocabulary Test-Third Edition. 1997, Circle Pines, MN: American Guidance Service, Inc.
53.
Williams KT: Expressive Vocabulary Test. 1997, Circle Pines, MN: American Guidance Service, Inc.
54.
Delis DC, Kaplan E, Kramer JH: Delis-Kaplan Executive Function System. 2001, San Antonio, TX: The Psychological Corporation
55.
Wiig EH, Secord WA: Test of Language Competence-Expanded Edition. 1989, San Antonio, TX: The Psychological Corporation
56.
Wagner R, Torgesen J, Rashotte C: Comprehensive Test of Phonological Processing. 1999, Austin, TX: PRO-ED
57.
Jasper HH: The ten-twenty electrode system of the International Federation. Electroencephalogr Clin Neurophysiol. 1958, 10: 371-375.
58.
Delorme A, Makeig S: EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods. 2004, 134: 9-21. 10.1016/j.jneumeth.2003.10.009.CrossRefPubMed
59.
Sarvas J: Basic mathematical and electromagnetic concepts of the biomagnetic inverse problem. Phys Med Biol. 1987, 32: 11-22. 10.1088/0031-9155/32/1/004.CrossRefPubMed
60.
61.
Litvak V, Mattout J, Kiebel S, Phillips C, Henson R, Kilner J, Barnes G, Oostenveld R, Daunizeau J, Flandin G, et al: EEG and MEG data analysis in SPM8. Comput Intell Neurosci. 2011, 2011: 852961-CrossRefPubMedPubMedCentral
62.
Genovese CR, Lazar NA, Nichols T: Thresholding of statistical maps in functional neuroimaging using the false discovery rate. NeuroImage. 2002, 15: 870-878. 10.1006/nimg.2001.1037.CrossRefPubMed
63.
Dronkers N, Pinker S, Damasio A: Language and the aphasias. Principles of Neural Science. Edited by: Kandel ER, Schwartz JH, Jessell TM. 2000, New York, NY: McGraw-Hill, 1169-1187. 4
64.
Hudspeth AJ: Hearing. Principles of Neural Science. Edited by: Kandel ER, Schwartz JH, Jessell TM. 2000, New York, NY: McGraw-Hill, 590-613. 4
65.
Binder JR, Desai RH, Graves WW, Conant LL: Where is the semantic system? A critical review and meta-analysis of 120 functional neuroimaging studies. Cereb Cortex. 2009, 19: 2767-2796. 10.1093/cercor/bhp055.CrossRefPubMedPubMedCentral
66.
Ross B, Borgmann C, Draganova R, Roberts LE, Pantev C: A high-precision magnetoencephalographic study of human auditory steady-state responses to amplitude-modulated tones. J Acoust Soc Am. 2000, 108: 679-691. 10.1121/1.429600.CrossRefPubMed
67.
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. 10.1016/0013-4694(95)00064-6.CrossRefPubMed
68.
Torrence C, Compo GP: A practical guide to wavelet analysis. Bull Am Meteorol Soc. 1998, 79: 61-78. 10.1175/1520-0477(1998)079<0061:APGTWA>2.0.CO;2.CrossRef
69.
Herrmann CS, Munk MH, Engel AK: Cognitive functions of gamma-band activity: memory match and utilization. Trends Cogn Sci. 2004, 8: 347-355. 10.1016/j.tics.2004.06.006.CrossRefPubMed
70.
Wilke M, Lidzba K: LI-tool: a new toolbox to assess lateralization in functional MR-data. J Neurosci Methods. 2007, 163: 128-136. 10.1016/j.jneumeth.2007.01.026.CrossRefPubMed
71.
Schmidt GL, Kimel LK, Winterrowd E, Pennington BF, Hepburn SL, Rojas DC: Impairments in phonological processing and nonverbal intellectual function in parents of children with autism. J Clin Exp Neuropsychol. 2008, 30: 557-567. 10.1080/13803390701551225.CrossRefPubMed
72.
Debener S, Herrmann CS, Kranczioch C, Gembris D, Engel AK: Top-down attentional processing enhances auditory evoked gamma band activity. NeuroReport. 2003, 14: 683-686. 10.1097/00001756-200304150-00005.CrossRefPubMed
73.
Ross B, Picton TW, Herdman AT, Pantev C: The effect of attention on the auditory steady-state response. Neurol Clin Neurophysiol. 2004, 2004: 22-PubMed
74.
Skosnik PD, Krishnan GP, O’Donnell BF: The effect of selective attention on the gamma-band auditory steady-state response. Neurosci Lett. 2007, 420: 223-228. 10.1016/j.neulet.2007.04.072.CrossRefPubMed
75.
Lenz D, Fischer S, Schadow J, Bogerts B, Herrmann CS: Altered evoked gamma-band responses as a neurophysiological marker of schizophrenia?. Int J Psychophysiol. 2010, 79: 25-31.CrossRefPubMed
76.
Gruber T, Muller MM: Effects of picture repetition on induced gamma band responses, evoked potentials, and phase synchrony in the human EEG. Brain Res Cogn Brain Res. 2002, 13: 377-392. 10.1016/S0926-6410(01)00130-6.CrossRefPubMed
77.
Jensen O, Kaiser J, Lachaux JP: Human gamma-frequency oscillations associated with attention and memory. Trends Neurosci. 2007, 30: 317-324. 10.1016/j.tins.2007.05.001.CrossRefPubMed
78.
Jerbi K, Ossandon T, Hamame CM, Senova S, Dalal SS, Jung J, Minotti L, Bertrand O, Berthoz A, Kahane P, Lachaux JP: Task-related gamma-band dynamics from an intracerebral perspective: review and implications for surface EEG and MEG. Hum Brain Mapp. 2009, 30: 1758-1771. 10.1002/hbm.20750.CrossRefPubMed
79.
Brookes MJ, Wood JR, Stevenson CM, Zumer JM, White TP, Liddle PF, Morris PG: Changes in brain network activity during working memory tasks: a magnetoencephalography study. NeuroImage. 2011, 55: 1804-1815. 10.1016/j.neuroimage.2010.10.074.CrossRefPubMed
80.
Belmonte MK, Gomot M, Baron-Cohen S: Visual attention in autism families: ’unaffected’ sibs share atypical frontal activation. J Child Psychol Psychiatry. 2010, 51: 259-276. 10.1111/j.1469-7610.2009.02153.x.CrossRefPubMed
81.
Bigler ED, Mortensen S, Neeley ES, Ozonoff S, Krasny L, Johnson M, Lu J, Provencal SL, McMahon W, Lainhart JE: Superior temporal gyrus, language function, and autism. Dev Neuropsychol. 2007, 31: 217-238. 10.1080/87565640701190841.CrossRefPubMed
82.
Kleinhans NM, Muller RA, Cohen DN, Courchesne E: Atypical functional lateralization of language in autism spectrum disorders. Brain Res. 2008, 1221: 115-125.CrossRefPubMedPubMedCentral
Metadata
Title
Abnormalities in gamma-band responses to language stimuli in first-degree relatives of children with autism spectrum disorder: an MEG study
Authors
Kristina L McFadden
Susan Hepburn
Erin Winterrowd
Gwenda L Schmidt
Donald C Rojas
Publication date
01-12-2012
Publisher
BioMed Central
Published in
BMC Psychiatry / Issue 1/2012
Electronic ISSN: 1471-244X
DOI
https://doi.org/10.1186/1471-244X-12-213

Other articles of this Issue 1/2012

BMC Psychiatry 1/2012 Go to the issue

Research article

Prevalence of psychological distress and associated factors in tuberculosis patients in public primary care clinics in South Africa

Research article

Computer use and stress, sleep disturbances, and symptoms of depression among young adults – a prospective cohort study

Research article

Effective lifestyle interventions to improve type II diabetes self-management for those with schizophrenia or schizoaffective disorder: a systematic review

Research article

Medication adherence and utilization in patients with schizophrenia or bipolar disorder receiving aripiprazole, quetiapine, or ziprasidone at hospital discharge: A retrospective cohort study

Research article

Definitions and factors associated with subthreshold depressive conditions: a systematic review

Research article

The characteristics of serious suicide attempters in Japanese adolescents- comparison study between adolescents and adults