Neural synchrony examined with magnetoencephalography (MEG) during eye gaze processing in autism spectrum disorders: preliminary findings

Journal of Neurodevelopmental Disorders

Susan M Bowyer⁵  Aimee M Moore³  Laszlo A Erdodi²  Kelly Vogt³  Alfred Mansour³  Daniel Jacobson⁴  Lesley Pawluk⁶  Amy Olszewski¹  John E Moran⁶  Annette E Richard³  Renée Lajiness-O’Neill⁶ 

[1] Department of Psychiatry, SUNY Upstate Medical University, Syracuse, NY, USA;Dartmouth, Department of Psychiatry, Geisel School of Medicine at Dartmouth, Lebanon, NH, USA;Eastern Michigan University, Ypsilanti, MI, USA;United States Air Force, USMS, Biloxi, MS, USA;Oakland University, Rochester, MI, USA;Henry Ford Hospital, Detroit, MI, USA

关键词: Social cognition;    Magnetoencephalography;    Coherence;    Neural synchrony;    Eye gaze;    Autism spectrum disorder;   

Others  :  803348
DOI  :  10.1186/1866-1955-6-15

 received in 2013-08-28, accepted in 2014-06-04,  发布年份 2014

【 摘 要 】

Background

Gaze processing deficits are a seminal, early, and enduring behavioral deficit in autism spectrum disorder (ASD); however, a comprehensive characterization of the neural processes mediating abnormal gaze processing in ASD has yet to be conducted.

Methods

This study investigated whole-brain patterns of neural synchrony during passive viewing of direct and averted eye gaze in ASD adolescents and young adults (M_Age = 16.6) compared to neurotypicals (NT) (M_Age = 17.5) while undergoing magnetoencephalography. Coherence between each pair of 54 brain regions within each of three frequency bands (low frequency (0 to 15 Hz), beta (15 to 30 Hz), and low gamma (30 to 45 Hz)) was calculated.

Results

Significantly higher coherence and synchronization in posterior brain regions (temporo-parietal-occipital) across all frequencies was evident in ASD, particularly within the low 0 to 15 Hz frequency range. Higher coherence in fronto-temporo-parietal regions was noted in NT. A significantly higher number of low frequency cross-hemispheric synchronous connections and a near absence of right intra-hemispheric coherence in the beta frequency band were noted in ASD. Significantly higher low frequency coherent activity in bilateral temporo-parieto-occipital cortical regions and higher gamma band coherence in right temporo-parieto-occipital brain regions during averted gaze was related to more severe symptomology as reported on the Autism Diagnostic Interview-Revised (ADI-R).

Conclusions

The preliminary results suggest a pattern of aberrant connectivity that includes higher low frequency synchronization in posterior cortical regions, lack of long-range right hemispheric beta and gamma coherence, and decreased coherence in fronto-temporo-parietal regions necessary for orienting to shifts in eye gaze in ASD; a critical behavior essential for social communication.

【 授权许可】

   
2014 Lajiness-O¿Neill et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Emery NJ: The eyes have it: the neuroethology, function and evolution of social gaze. Neurosci Biobehav Rev 2000, 24:581-604.
• [2]American Psychiatric Association: Diagnostic and statistical manual of mental disorders. 4th edition. Washington, DC: APA; 2000.
• [3]Frischen A, Bayliss A, Tipper S: Gaze cueing of attention: visual attention, social cognition, and individual differences. Psychol Bull 2007, 133:694-724.
• [4]Baron-Cohen S, Baldwin DA, Crowson M: Do children with autism use the speaker’s direction of gaze strategy to crack the code of language? Child Dev 1997, 68:48-57.
• [5]Dawson G, Toth K, Abbott R, Osterling J, Munson J, Estes A, Liaw J: Early social attention impairments in autism: social orienting, joint attention, and attention to distress. Dev Psychol 2004, 40:271-283.
• [6]Luyster RJ, Kadlec MB, Carter A, Tager-Flusberg H: Language assessment and development in toddlers with autism spectrum disorders. J Autism Dev Disord 2008, 38:1426-1438.
• [7]Morales M, Mundy P, Delgado CEF, Yale M, Messinger D, Neal R, Schwartz HK: Responding to joint attention across the 6- through 24-month age period and early language acquisition. J Appl Dev Psychol 2000, 21:283-298.
• [8]Leekman SR, Lopez B, Moore C: Attention and joint attention in preschool children with autism. Dev Psychol 2000, 36:261-273.
• [9]Roeyers H, Van Oost P, Bothuyne S: Immediate imitation and joint attention in young children with autism. Dev Psychopathol 1998, 10:441-450.
• [10]Kylliäinen A, Hietanen JK: Attention orienting by another’s gaze direction in children with autism. J Autism Dev Disord 2004, 29:499-508.
• [11]Swettenham J, Condie S, Campbell R, Milne E, Coleman M: Does the perception of moving eyes trigger reflexive visual orienting in autism? Biol Sci 2003, 358:325-334.
• [12]Goldberg MC, Mostow AJ, Vecera SP, Larson JC, Mostofsky SH, Mahone EM, Denckla MB: Evidence for impairments in using static line drawings of eye gaze cues to orient visual-spatial attention in children with high functioning autism. J Autism Dev Disord 2008, 38:1405-1413.
• [13]Ristic J, Mottron L, Friesen CK, Iarocci G, Burack JA, Kingstone A: Eyes are special but not for everyone: the case of autism. Cogn Brain Res 2005, 24:715-718.
• [14]Senju A, Tojo Y, Dairoku H, Hasegawa T: Reflexive orienting in respsonse to eye gaze and an arrow in children with and without autism. J Child Psychol Psychiatry 2004, 45:445-458.
• [15]Vlamings PHJM, Stauder JEA, van Son IAM, Mottron L: Atypical visual orienting to gaze- and arrow-cues in adults with high functioning autism. J Autism Dev Disord 2005, 35:267-277.
• [16]Nation K, Penny S: Sensitivity to eye gaze in autism: Is it normal? Is it automatic? Is it social? Dev Psychopathol 2008, 20:79-97.
• [17]Elsabbagh M, Mercure E, Hudry K, Chandler S, Pasco G, Charman T, Pickles A, Baron-Cohen S, Bolton P, Johnson MH; BASIS Team: Infant neural sensitivity to dynamic eye gaze is associated with later emerging autism. Curr Biol 2012, 22:338-342.
• [18]Baldwin DA: Joint attention: its origins and role in development. In Understanding the link between joint attention and language. Edited by Moore C, Dunham PJ, Hillsdale NJ. Erlbaum; 1995:131-158.
• [19]Davies MS, Dapretto M, Sigman M, Sepeta L, Bookheimer SY: Neural bases of gaze and emotion processing in children with autism spectrum disorders. Brain Behav 2011, 1:1-11.
• [20]Elsabbagh M, Volein A, Csibra G, Holmboe K, Garwood H, Tucker L, Krljes S, Baron-Cohen S, Bolton P, Charman T, Baird G, Johnson MH: Neural correlates of eye gaze processing in the infant broader autism phenotype. Biol Psychiatry 2009, 65:31-38.
• [21]Grice S, Halit H, Farroni T, Baron-Cohen S, Bolton P, Johnson MH: Neural correlates of eye-gaze detection in young children with autism. Cortex 2005, 41:342-353.
• [22]Pelphrey KA, Morris JP, McCarthy G: Neural basis of eye gaze processing deficits in autism. Brain Am J Neurol 2005, 128:1038-1048.
• [23]Pitskel NB, Bolling DZ, Hudac CM, Lantz SD, Minshew NJ, Vander Wyk BC, Pelphrey KA: Brain mechanisms for processing direct and averted gaze in individuals with autism. J Autism Dev Disord 2011, 41:1686-1693.
• [24]Andrew C, Pfurtscheller G: Event-related coherence as a tool for studying dynamic interaction of brain regions. Electroencephalogr Clin Neurophysiol 1996, 98:144-148.
• [25]Brock J, Brown CC, Boucher J, Rippon G: The temporal binding deficit hypothesis of autism. Dev Psychopathol 2002, 14:209-224.
• [26]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.
• [27]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.
• [28]Schipul SE, Keller TA, Just MA: Inter-regional brain communication and its disturbance in autism. Front Syst Neurosci 2011, 5:10.
• [29]Dinstein I, Pierce K, Eyler L, Solso S, Malach R, Behrmann M, Courchesne E: Disrupted neural synchronization in toddlers with autism. Neuron 2011, 70:1218-1225.
• [30]Tallon-Baudry C, Bertrand O: Oscillatory gamma activity in humans and its role in object representation. Trends Cogn Sci 1999, 3:151-162.
• [31]Fries P, Reynolds JH, Rorie AE, Desimone R: Oscillatory synchronization by visual attention. Science (80- ) 2001, 291:1560-1563.
• [32]Uhlhaas PJ, Singer W: Neural synchrony in brain disorders: relevance for cognitive dysfunctions and pathophysiology. Neuron 2006, 52:155-168.
• [33]Khan S, Gramfort A, Shetty NR, Kitzbichler MG, Ganesan S, Moran JM, Lee SM, Gabrieli JD, 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 USA 2013, 110:3107-3112.
• [34]Kopell N, Ermentrout GB, Whittington MA: Traub RD. Gamma rhythms and beta rhythms have different synchronization properties. Proc Natl Acad Sci USA 2000, 97:1867-1872.
• [35]Wechsler D: Wechsler Abbreviated Scale of Intelligence. San Antonio, TX: Harcourt Assessment; 1999.
• [36]Lord C, Rutter M, LeCouteur 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.
• [37]Pelphrey KA, Singerman JD, Allison T, McCarthy G: Brain activation evoked by perception of gaze shifts: the influence of context. Neuropsychologia 2003, 41:156-170.
• [38]Richard A, Lajiness-O’Neill R, Bowyer S: Impaired prefrontal gamma band synchrony in autism spectrum disorders during a gaze cueing task. NeuroReport 2013, 13;24(16):894-897.
• [39]Moran JE, Bowyer SM, Mason KM, Tepley N, Smith BJ, Barkley GL, Greene D, Morrell M: MEG coherence imaging compared to electrocortical recordings from NeuroPace implants to determine the location of ictal onset in epilepsy patients. Int Congr Ser New Front Biomagn 2006, 1300:673-676.
• [40]Elisevich K, Shukla N, Moran JE, Smith B, Schultz L, Mason K, Barkley GL, Tepley N, Gumenyuk V, Bowyer SM: An assessment of MEG coherence imaging in the study of temporal lobe epilepsy. Epilepsia 2011, 52:1110-1119.
• [41]Moran JE, Bowyer SM, Tepley N: Multi-Resolution FOCUSS: a source imaging technique applied to MEG data. Brain Topogr 2005, 18:1-17.
• [42]Talairach J, Tournoux P: Co-Planar Steriotaxic Atlas of the human brain. 3-Dimensional Proportional System: An approach to cerebral imaging. New York, NY: Thieme Medical Publishers, Inc.; 1988.
• [43]Shattuck DW, Mirza M, Adisetiyo V, Hojatkashani C, Salamon G, Narr KL, Poldrack RA, Bilder RM, Toga AW: Construction of a 3D probabilistic atlas of human cortical structures. Neuroimage 2008, 39:1064-1080.
• [44]Woods RP, Grafton ST, Watson JDG, Sicotte NL, Mazziotta JC: Automated image registration: II. Intersubject validation of linear and nonlinear models. J Comput Assist Tomogr 1998, 22:153-165.
• [45]Benjamini Y, Hochberg Y: Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B 1995, 57:289-300.
• [46]Efron B: Large Scale Inference. Cambridge, UK: Cambridge University Press; 2010.
• [47]Bailey AJ, Braeutigam S, Jousmäki V, Swithenby SJ: Abnormal activation of face processing systems at early and intermediate latency in individuals with autism spectrum disorder: a magnetoencephalographic study. Eur J Neurosci 2005, 21:2575-2585.
• [48]Falter CM, Braeutigam S, Nathan R, Carrington S, Bailey AJ: Enhanced access to early visual processing of perceptual simultaneity in autism spectrum disorders. J Autism Dev Disord 2013, 43:1857-1866.
• [49]Kylliainen A, Braeutigam S, Hietanen JK, Swithenby SJ, Bailey AJ: Face and gaze processing in normally developing children: a magnetoencephalographic study. Eur J Neurosci 2006, 23:801-810.
• [50]Lajiness-O’Neill R, Chase AM, Olszewski A, Boyle MA, Pawluk L, Mansour A, Jacobson D, Gallaway ML, Lewandowski-Powley P, Gorka B, Moran J, Bowyer SM: Hemispheric differences in neural activation during gaze cueing in autism spectrum disorder (ASD) measured by magnetoencephalography (MEG). In IFMBE Proceedings: 17th International Conference on Biomagnetism Advances in Biomagnetism. Edited by Supek S, Susac A. New York, NY: Springer; 2010:381-384.
• [51]Wright B, Alderson-Day B, Prendergast G, Bennett S, Jordan J, Whitton C, Gouws A, Jones N, Attur R, Tomlinson H, Green G: Gamma activation in young people with autism spectrum disorders and typically-developing controls when viewing emotions on faces. PLoS One 2012, 7:e41326.
• [52]Gandal MJ, Edgar JC, Ehrlichman RS, Mehta M, Roberts TPL, Siegel SJ: Validating γ oscillations and delayed auditory responses as translational biomarkers of autism. Biol Psychiatry 2010, 68:1100-1106.
• [53]McFadden KL, Hepburn S, Winterrowd E, Schmidt GL, Rojas DC: Abnormalities in gamma-band responses to language stimuli in first-degree relatives of children with autism spectrum disorder: an MEG study. BMC Psychiatry 2012, 12:213.
• [54]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, 9:1-9.
• [55]Rojas DC, Teale PD, Maharajh K, Kronberg E, Youngpeter K, Wilson LB, 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.
• [56]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.
• [57]Cornew L, Roberts TPL, Blaskey L, Edgar JC: Resting-state oscillatory activity in autism spectrum disorders. J Autism Dev Disord 2012, 42:1884-1894.
• [58]Pollonini L, Patidar U, Situ N, Rezaie R, Papanicolaou AC, Zouridakis G: Functional connectivity networks in the autistic and healthy brain assessed using Granger causality. Conf Proceedings Annual Int Conf IEEE Eng Med Biol Soc 2010, 1:1730-1733.
• [59]Tsiaras V, Simos PG, Rezaie R, Sheth BR, Garyfallidis E, Castillo EM, Papanicolaou AC: Extracting biomarkers of autism from MEG resting-state functional connectivity networks. Comput Biol Med 2011, 41:1166-1177.
• [60]Murias M, Webb SJ, Greenson J, Dawson G: Resting state cortical connectivity reflected in EEG coherence in individuals with autism. Biol Psychiatry 2008, 62:270-273.
• [61]Ethofer T, Gschwind M, Vuilleumier P: Processing social aspects of human gaze: a combined fMRI-DTI study. Neuroimage 2011, 55:411-419.
• [62]Seghier M, Price C: Reading aloud boosts connectivity through the putamen. Cereb Cortex 2010, 20:570-582.
• [63]Stevenson JL, Kellett KA: Can magnetic resonance imaging aid diagnosis of the autism spectrum? J Neurosci 2010, 30:16763-16765.
• [64]Ecker C, Marquand A, Mourão-Miranda J, Johnston P, Daly EM, Brammer MJ, Maltezos S, Murphy CM, Robertson D, Williams SC, Murphy DG: Describing the brain in autism in five dimensions–magnetic resonance imaging-assisted diagnosis of autism spectrum disorder using a multiparameter classification approach. J Neurosci 2010, 30:10612-10623.
• [65]Centers for Disease Control and Prevention (CDC): Autism Spectrum Disorders 2012. Atlanta, GA: CDC; 2011. Available at: http://www.cdc.gov/ncbddd/autism/data.html webcite
• [66]Srinivasan R, Winter WR, Ding J, Nunez PL: EEG and MEG coherence: measures of functional connectivity at distinct spatial scales of neocortical dynamic. J Neurosci Methods 2007, 15:41-52.
• [67]Minzenberg MJ, Firl AJ, Yoon JH, Gomes GC, Reinking C, Carter CS: Gamma oscillatory power is impaired during cognitive control independent of medication status in first-episode schizophrenia. Neuropsychopharmacology 2010, 35:2590-2599.
• [68]Ozerdem A, Güntekin B, Tunca Z, Başar E: Brain oscillatory responses in patients with bipolar disorder manic episode before and after valproate treatment. Brain Res 2008, 1235:98-108.
• [69]Wilson TW, Heinrichs-Graham E, White ML, Knott NL, Wetzel MW: Estimating the passage of minutes: deviant oscillatory frontal activity in medicated and unmedicated ADHD. Neuropsychology 2013, 27:654-665.