Journal of Autism and Developmental Disorders

, Volume 47, Issue 7, pp 1944–1955 | Cite as

Neural Correlates of Explicit Versus Implicit Facial Emotion Processing in ASD

  • Christina Luckhardt
  • Anne Kröger
  • Hannah Cholemkery
  • Stephan Bender
  • Christine M. Freitag
Original Paper


The underlying neural mechanisms of implicit and explicit facial emotion recognition (FER) were studied in children and adolescents with autism spectrum disorder (ASD) compared to matched typically developing controls (TDC). EEG was obtained from N = 21 ASD and N = 16 TDC. Task performance, visual (P100, N170) and cognitive (late positive potential) event-related-potentials, as well as coherence were compared across groups. TDC showed a task-dependent increase and a stronger lateralization of P100 amplitude during the explicit task and task-dependent modulation of intra-hemispheric coherence in the beta band. In contrast, the ASD group showed no task dependent modulation. Results indicate disruptions in early visual processing and top-down attentional processes as contributing factors to FER deficits in ASD.


ERP Facial emotion recognition Intentional processing Autism ASD 

Supplementary material

10803_2017_3141_MOESM1_ESM.pdf (478 kb)
Supplementary material 1 (PDF 479 KB)


  1. American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders (DSM-5®). Washington, DC: American Psychiatric Publishing.CrossRefGoogle Scholar
  2. Apicella, F., Sicca, F., Federico, R. R., Campatelli, G., & Muratori, F. (2013). Fusiform gyrus responses to neutral and emotional faces in children with autism spectrum disorders: A high density ERP study. Behavioural Brain Research, 251, 155–162.CrossRefPubMedGoogle Scholar
  3. Bal, E., Harden, E., Lamb, D., van Hecke, A. V., Denver, J. W., & Porges, S. W. (2010). Emotion recognition in children with autism spectrum disorders: Relations to eye gaze and autonomic state. Journal of Autism and Developmental Disorders, 40(3), 358–370.CrossRefPubMedGoogle Scholar
  4. Batty, M., Meaux, E., Wittemeyer, K., Rogé, B., & Taylor, M. J. (2011). Early processing of emotional faces in children with autism: An event-related potential study. Journal of Experimental Child Psychology, 109(4), 430–444.CrossRefPubMedGoogle Scholar
  5. Begeer, S., Rieffe, C., Terwogt, M. M., & Stockmann, L. (2006). Attention to facial emotion expressions in children with autism. Autism: The International Journal of Research and Practice. doi:10.1177/1362361306057862.Google Scholar
  6. Benning, S. D., Kovac, M., Campbell, A., Miller, S., Hanna, E. K., Damiano, C. R., et al. (2016). Late positive potential ERP responses to social and nonsocial stimuli in youth with autism spectrum disorder. Journal of Autism and Developmental Disorders. doi:10.1007/s10803-016-2845-y.PubMedGoogle Scholar
  7. Bird, G., Catmur, C., Silani, G., Frith, C., & Frith, U. (2006). Attention does not modulate neural responses to social stimuli in autism spectrum disorders. NeuroImage, 31(4), 1614–1624.CrossRefPubMedGoogle Scholar
  8. Bölte, S., & Poustka, F. (2008). Skala zur Erfassung sozialer Reaktivität (SRS). Bern: Huber.Google Scholar
  9. Bölte, S., Poustka, F., Constantino, J. N., & Gruber, C. P. (2005). SRS: Skala zur Erfassung sozialer Reaktivität: dimensionale Autismus-Diagnostik. Bern: Verlag Hans Huber.Google Scholar
  10. Bölte, S., Rühl, D., Schmötzer, G., & Poustka, F. (2006). Diagnostisches interview für autismus-revidiert (ADI-R). Bern: Huber.Google Scholar
  11. Buschman, T. J., & Miller, E. K. (2007). Top-down versus bottom-up control of attention in the prefrontal and posterior parietal cortices. Science, 315(5820), 1860–1862.CrossRefPubMedGoogle Scholar
  12. Carson, A. M., Salowitz, N. M. G., Scheidt, R. A., Dolan, B. K., & van Hecke, A. V. (2014). Electroencephalogram coherence in children with and without autism spectrum disorders: Decreased interhemispheric connectivity in autism. Autism Research: Official Journal of the International Society for Autism Research, 7(3), 334–343.CrossRefGoogle Scholar
  13. Catarino, A., Andrade, A., Churches, O., Wagner, A. P., Baron-Cohen, S., & Ring, H. (2013). Task-related functional connectivity in autism spectrum conditions: An EEG study using wavelet transform coherence. Molecular autism, 4(1), 1.CrossRefPubMedPubMedCentralGoogle Scholar
  14. Challis, R. E., & Kitney, R. I. (1991). Biomedical signal processing (in four parts). III, The power spectrum and coherence function. Medical & Biological Engineering & Computing, 29(3), 225–241.CrossRefGoogle Scholar
  15. Churches, O., Wheelwright, S., Baron-Cohen, S., & Ring, H. (2010). The N170 is not modulated by attention in autism spectrum conditions. NeuroReport, 21(6), 399–403.CrossRefPubMedGoogle Scholar
  16. Coben, R., Clarke, A. R., Hudspeth, W., & Barry, R. J. (2008). EEG power and coherence in autistic spectrum disorder. Clinical Neurophysiology: Official Journal of the International Federation of Clinical Neurophysiology, 119(5), 1002–1009.CrossRefGoogle Scholar
  17. Corden, B., Chilvers, R., & Skuse, D. (2008). Avoidance of emotionally arousing stimuli predicts social-perceptual impairment in Asperger’s syndrome. Neuropsychologia, 46(1), 137–147. doi:10.1016/j.neuropsychologia.2007.08.005.CrossRefPubMedGoogle Scholar
  18. Critchley, H., Daly, E., Phillips, M., Brammer, M., Bullmore, E., Williams, S., et al. (2000). Explicit and implicit neural mechanisms for processing of social information from facial expressions: A functional magnetic resonance imaging study. Human Brain Mapping. doi:10.1002/(SICI)1097-0193(200002)9:2<93:AID-HBM4>3.0.CO;2-Z.PubMedGoogle Scholar
  19. Delorme, A., & Makeig, S. (2004). EEGLAB: An open source toolbox for analysis of single trial EEG dynamics including independent component analysis. Journal of Neuroscience Methods, 134, 9–21.CrossRefPubMedGoogle Scholar
  20. Duffy, F. H., & Als, H. (2012). A stable pattern of EEG spectral coherence distinguishes children with autism from neuro-typical controls—a large case control study. BMC Medicine, 10, 64.CrossRefPubMedPubMedCentralGoogle Scholar
  21. Ebner, N. C., Riediger, M., & Lindenberger, U. (2010). FACES–a database of facial expressions in young, middle-aged, and older women and men: Development and validation. Behavior Research Methods, 42(1), 351–362.CrossRefPubMedGoogle Scholar
  22. Enticott, P. G., Kennedy, H. A., Johnston, P. J., Rinehart, N. J., Tonge, B. J., Taffe, J. R., & Fitzgerald, P. B. (2014). Emotion recognition of static and dynamic faces in autism spectrum disorder. Cognition & Emotion, 28(6), 1110–1118.CrossRefGoogle Scholar
  23. Ferrari, V., Bradley, M. M., Codispoti, M., & Lang, P. J. (2010). Detecting novelty and significance. Journal of Cognitive Neuroscience, 22(2), 404–411.CrossRefPubMedPubMedCentralGoogle Scholar
  24. Golarai, G., Grill-Spector, K., & Reiss, A. L. (2006). Autism and the development of face processing. Clinical Neuroscience Research. doi:10.1016/j.cnr.2006.08.001.PubMedPubMedCentralGoogle Scholar
  25. Gorno-Tempini, M. L., Pradelli, S., Serafini, M., Pagnoni, G., Baraldi, P., Porro, C., et al. (2001). Explicit and incidental facial expression processing: An fMRI study. NeuroImage. doi:10.1006/nimg.2001.0811.PubMedGoogle Scholar
  26. Hajcak, G., & Olvet, D. M. (2008). The persistence of attention to emotion: Brain potentials during and after picture presentation. Emotion (Washington, D. C.), 8(2), 250.CrossRefGoogle Scholar
  27. Harms, M. B., Martin, A., & Wallace, G. L. (2010). Facial emotion recognition in autism spectrum disorders: A review of behavioral and neuroimaging studies. Neuropsychology Review, 20(3), 290–322.CrossRefPubMedGoogle Scholar
  28. Haxby, J. V., Hoffman, E. A., & Gobbini, M. (2000). The distributed human neural system for face perception. Trends in Cognitive Sciences. doi:10.1016/S1364-6613(00)01482-0.Google Scholar
  29. Herba, C. M., Landau, S., Russell, T., Ecker, C., & Phillips, M. L. (2006). The development of emotion-processing in children: Effects of age, emotion, and intensity. Journal of Child Psychology and Psychiatry, and Allied Disciplines. doi:10.1111/j.1469-7610.2006.01652.x.PubMedGoogle Scholar
  30. Hileman, C. M., Henderson, H., Mundy, P., Newell, L., & Jaime, M. (2011). Developmental and individual differences on the P1 and N170 ERP components in children with and without autism. Developmental Neuropsychology, 36(2), 214–236.CrossRefPubMedPubMedCentralGoogle Scholar
  31. Isler, J. R., Martien, K. M., Grieve, P. G., Stark, R. I., & Herbert, M. R. (2010). Reduced functional connectivity in visual evoked potentials in children with autism spectrum disorder. Clinical Neurophysiology: Official Journal of the International Federation of Clinical Neurophysiology, 121(12), 2035–2043.CrossRefGoogle Scholar
  32. Jaime, M., McMahon, C. M., Davidson, B. C., Newell, L. C., Mundy, P. C., & Henderson, H. A. (2016). Brief report: Reduced temporal-central EEG alpha coherence during joint attention perception in adolescents with autism spectrum disorder. Journal of Autism and Developmental Disorders, 46(4), 1477–1489.CrossRefPubMedPubMedCentralGoogle Scholar
  33. Kamio, Y., Wolf, J., & Fein, D. (2006). Automatic processing of emotional faces in high-functioning pervasive developmental disorders: An affective priming study. Journal of Autism and Developmental Disorders. doi:10.1007/s10803-005-0056-z.PubMedGoogle Scholar
  34. Keehn, B., Vogel-Farley, V., Tager-Flusberg, H., & Nelson, C. A. (2015). Atypical hemispheric specialization for faces in infants at risk for autism spectrum disorder. Autism Research, 8(2), 187–198.CrossRefPubMedPubMedCentralGoogle Scholar
  35. Kitzbichler, M. G., Khan, S., Ganesan, S., Vangel, M. G., Herbert, M. R., Hamalainen, M. S., & Kenet, T. (2015). Altered development and multifaceted band-specific abnormalities of resting state networks in autism. Biological Psychiatry, 77(9), 794–804.CrossRefPubMedGoogle Scholar
  36. Kleinhans, N. M., Richards, T., Sterling, L., Stegbauer, K. C., Mahurin, R., Johnson, L. C., et al. (2008). Abnormal functional connectivity in autism spectrum disorders during face processing. Brain: A Journal of Neurology. doi:10.1093/brain/awm334.Google Scholar
  37. Kliemann, D., Dziobek, I., Hatri, A., Steimke, R., & Heekeren, H. R. (2010). Atypical reflexive gaze patterns on emotional faces in autism spectrum disorders. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience. doi:10.1523/JNEUROSCI.0688-10.2010.Google Scholar
  38. Klimesch, W. (2012). alpha-band oscillations, attention, and controlled access to stored information. Trends in Cognitive Sciences, 16(12), 606–617.CrossRefPubMedPubMedCentralGoogle Scholar
  39. Koshino, H., Kana, R. K., Keller, T. A., Cherkassky, V. L., Minshew, N. J., & Just, M. A. (2008). fMRI investigation of working memory for faces in autism: Visual coding and underconnectivity with frontal areas. Cerebral cortex (New York, N.Y.: 1991). doi:10.1093/cercor/bhm054.Google Scholar
  40. Leung, R. C., Ye, A. X., Wong, S. M., Taylor, M. J., & Doesburg, S. M. (2014). Reduced beta connectivity during emotional face processing in adolescents with autism. Molecular Autism. doi:10.1186/2040-2392-5-51.PubMedPubMedCentralGoogle Scholar
  41. Lozier, L. M., Vanmeter, J. W., & Marsh, A. A. (2014). Impairments in facial affect recognition associated with autism spectrum disorders: A meta-analysis. Development and Psychopathology. doi:10.1017/S0954579414000479.PubMedGoogle Scholar
  42. Lynn, A. C., Padmanabhan, A., Simmonds, D., Foran, W., Hallquist, M. N., Luna, B., et al. (2016). Functional connectivity differences in autism during face and car recognition: Underconnectivity and atypical age-related changes. Developmental Science. doi:10.1111/desc.12508.PubMedGoogle Scholar
  43. Macmillan, N. A., & Creelman, C. D. (2004). Detection theory: A user’s guide (p. 7). New York: Psychology press.Google Scholar
  44. Maekawa, T., Tobimatsu, S., Inada, N., Oribe, N., Onitsuka, T., Kanba, S., & Kamio, Y. (2011). Top-down and bottom-up visual information processing of non-social stimuli in high-functioning autism spectrum disorder. Research in Autism Spectrum Disorders, 5(1), 201–209.CrossRefGoogle Scholar
  45. Mathersul, D., McDonald, S., & Rushby, J. A. (2013). Automatic facial responses to briefly presented emotional stimuli in autism spectrum disorder. Biological Psychology. doi:10.1016/j.biopsycho.2013.08.004.PubMedGoogle Scholar
  46. Mathewson, K. J., Jetha, M. K., Drmic, I. E., Bryson, S. E., Goldberg, J. O., & Schmidt, L. A. (2012). Regional EEG alpha power, coherence, and behavioral symptomatology in autism spectrum disorder. Clinical Neurophysiology: Official Journal of the International Federation of Clinical Neurophysiology, 123(9), 1798–1809.CrossRefGoogle Scholar
  47. McCleery, J. P., Akshoomoff, N., Dobkins, K. R., & Carver, L. J. (2009). Atypical face versus object processing and hemispheric asymmetries in 10-month-old infants at risk for autism. Biological Psychiatry, 66(10), 950–957.CrossRefPubMedPubMedCentralGoogle Scholar
  48. McPartland, J., Cheung, C. H. M., Perszyk, D., & Mayes, L. C. (2010). Face-related ERPs are modulated by point of gaze. Neuropsychologia. doi:10.1016/j.neuropsychologia.2010.07.020.PubMedPubMedCentralGoogle Scholar
  49. McPartland, J., Dawson, G., Webb, S. J., Panagiotides, H., & Carver, L. J. (2004). Event-related brain potentials reveal anomalies in temporal processing of faces in autism spectrum disorder. Journal of Child Psychology and Psychiatry, 45(7), 1235–1245.CrossRefPubMedGoogle Scholar
  50. Milne, E. (2011). Increased intra-participant variability in children with autistic spectrum disorders: Evidence from single-trial analysis of evoked EEG. Frontiers in Psychology, 2, 51.CrossRefPubMedPubMedCentralGoogle Scholar
  51. Monk, C. S., Weng, S. J., Wiggins, J. L., Kurapati, N., Louro, H. M., Carrasco, M., et al. (2010). Neural circuitry of emotional face processing in autism spectrum disorders. Journal of Psychiatry & Neuroscience: JPN, 35(2), 105.CrossRefGoogle Scholar
  52. Murias, M., Webb, S. J., Greenson, J., & Dawson, G. (2007). Resting state cortical connectivity reflected in EEG coherence in individuals with autism. Biological Psychiatry, 62(3), 270–273.CrossRefPubMedPubMedCentralGoogle Scholar
  53. Nunez, P. L., Srinivasan, R., Westdorp, A. F., Wijesinghe, R. S., Tucker, D. M., Silberstein, R. B., & Cadusch, P. J. (1997). EEG coherency: I: Statistics, reference electrode, volume conduction, Laplacians, cortical imaging, and interpretation at multiple scales. Electroencephalography and Clinical Neurophysiology, 103(5), 499–515.CrossRefPubMedGoogle Scholar
  54. O’Connor, K., Hamm, J. P., & Kirk, I. J. (2005). The neurophysiological correlates of face processing in adults and children with Asperger’s syndrome. Brain and Cognition, 59(1), 82–95.CrossRefPubMedGoogle Scholar
  55. Oldfield, R. C. (1971). The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia, 9(1), 97–113.CrossRefPubMedGoogle Scholar
  56. Peiker, I., David, N., Schneider, T. R., Nolte, G., Schöttle, D., & Engel, A. K. (2015). Perceptual integration deficits in autism spectrum disorders are associated with reduced interhemispheric gamma-band coherence. Journal of Neuroscience, 35(50), 16352–16361.CrossRefPubMedGoogle Scholar
  57. Pelphrey, K. A., Morris, J. P., McCarthy, G., & Labar, K. S. (2007). Perception of dynamic changes in facial affect and identity in autism. Social Cognitive and Affective Neuroscience. doi:10.1093/scan/nsm010.Google Scholar
  58. Petermann, F., & Petermann, U. (2010). HAWIK-IV. Hamburg-Wechsler-Intelligenztest für Kinder-IV (Wechsler Intelligence Scale for Children (WISC-IV)-German version). Bern: Huber.Google Scholar
  59. Rowland, N., Meile, M. J., & Nicolaidis, S. (1985). EEG alpha activity reflects attentional demands, and beta activity reflects emotional and cognitive processes. Science, 228, 750–752.CrossRefGoogle Scholar
  60. Rühl, D., Bölte, S., Feineis-Matthews, S., & Poustka, F. (2004). ADOS, autism diagnostic observation schedule for autistic disorders. Bern: Huber (German)Google Scholar
  61. Rump, K. M., Giovannelli, J. L., Minshew, N. J., & Strauss, M. S. (2009). The development of emotion recognition in individuals with autism. Child Development. doi:10.1111/j.1467-8624.2009.01343.x.PubMedPubMedCentralGoogle Scholar
  62. Rutman, A. M., Clapp, W. C., Chadick, J. Z., & Gazzaley, A. (2010). Early top-down control of visual processing predicts working memory performance. Journal of Cognitive Neuroscience, 22(6), 1224–1234. doi:10.1162/jocn.2009.21257.CrossRefPubMedPubMedCentralGoogle Scholar
  63. Schneider, S., Unnewehr, S., & Margraf, J. (Eds.). (2009). Kinder-DIPS: Diagnostisches Interview bei psychischen Störungen im Kindes- und Jugendalter (2., aktualisierte und erw. Aufl.). Heidelberg: Springer.Google Scholar
  64. Schultz, R. T., Gauthier, I., Klin, A., Fulbright, R. K., Anderson, A. W., Volkmar, F., et al. (2000). Abnormal ventral temporal cortical activity during face discrimination among individuals with autism and Asperger syndrome. Archives of General Psychiatry. doi:10.1001/archpsyc.57.4.331.PubMedGoogle Scholar
  65. Schupp, H., Cuthbert, B., Bradley, M., Hillman, C., Hamm, A., & Lang, P. (2004). Brain processes in emotional perception: Motivated attention. Cognition and Emotion, 18(5), 593–611.CrossRefGoogle Scholar
  66. Schupp, H. T., Cuthbert, B. N., Bradley, M. M., Cacioppo, J. T., Ito, T., & Lang, P. J. (2000). Affective picture processing: The late positive potential is modulated by motivational relevance. Psychophysiology, 37(2), 257–261.CrossRefPubMedGoogle Scholar
  67. Shah, P., Bird, G., & Cook, R. (2016). Face processing in autism: Reduced integration of cross-feature dynamics. Cortex: A Journal Devoted to the Study of the Nervous System and Behavior. doi:10.1016/j.cortex.2015.11.019.Google Scholar
  68. Sporns, O., Tononi, G., & Edelman, G. M. (2000). Theoretical neuroanatomy: Relating anatomical and functional connectivity in graphs and cortical connection matrices. Cerebral Cortex, 10(2), 127–141.CrossRefPubMedGoogle Scholar
  69. Taylor, M. J. (2002). Non-spatial attentional effects on P1. Clinical Neurophysiology, 113(12), 1903–1908.CrossRefPubMedGoogle Scholar
  70. van Ede, F., de Lange, F., Jensen, O., & Maris, E. (2011). Orienting attention to an upcoming tactile event involves a spatially and temporally specific modulation of sensorimotor alpha- and beta-band oscillations. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 31(6), 2016–2024.CrossRefGoogle Scholar
  71. von Aster, M., Neubauer, A., & Horn, R. (2006). Wechsler-Intelligenztest für Erwachsene: Ubersetzung und Adaptation der WAIS-III von David Wechsler [Wechsler intelligence test for adults: translation and adaptation of WAIS-III by David Wechsler]. Harcourt Test Services, Frankfurt/M.Google Scholar
  72. Waldmann, H.-C. (2008). Kurzformen des HAWIK-IV: Statistische Bewertung in verschiedenen Anwendungsszenarien. Diagnostica, 54(4), 202–210.CrossRefGoogle Scholar
  73. Wallace, S., Coleman, M., & Bailey, A. (2008). An investigation of basic facial expression recognition in autism spectrum disorders. Cognition & Emotion, 22(7), 1353–1380.CrossRefGoogle Scholar
  74. Webb, S. J., Merkle, K., Murias, M., Richards, T., Aylward, E., & Dawson, G. (2012). ERP responses differentiate inverted but not upright face processing in adults with ASD. Social Cognitive and Affective Neuroscience. doi:10.1093/scan/nsp002.PubMedGoogle Scholar
  75. Wicker, B., Fonlupt, P., Hubert, B., Tardif, C., Gepner, B., & Deruelle, C. (2008). Abnormal cerebral effective connectivity during explicit emotional processing in adults with autism spectrum disorder. Social Cognitive and Affective Neuroscience. doi:10.1093/scan/nsn007.PubMedPubMedCentralGoogle Scholar
  76. Wong, T. K. W., Fung, P. C. W., Chua, S. E., & McAlonan, G. M. (2008). Abnormal spatiotemporal processing of emotional facial expressions in childhood autism: Dipole source analysis of event-related potentials. The European Journal of Neuroscience, 28(2), 407–416.CrossRefPubMedGoogle Scholar
  77. World Health Organization (1992). The ICD-10 classification of mental and behavioural disorders: Clinical descriptions and diagnostic guidelines. Geneva: World Health Organization.Google Scholar
  78. Yeung, M. K., Han, Y. M., Sze, S. L., & Chan, A. S. (2014). Altered right frontal cortical connectivity during facial emotion recognition in children with autism spectrum disorders. Research in Autism Spectrum Disorders, 8(11), 1567–1577.CrossRefGoogle Scholar
  79. Zerouali, Y., Lina, J.-M., & Jemel, B. (2013). Optimal eye-gaze fixation position for face-related neural responses. PLoS ONE. doi:10.1371/journal.pone.0060128.PubMedPubMedCentralGoogle Scholar

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© Springer Science+Business Media New York 2017

Authors and Affiliations

  1. 1.Department of Child and Adolescent Psychiatry, Psychosomatics and Psychotherapy, Autism Research and Intervention Center of ExcellenceUniversity Hospital Frankfurt, Goethe UniversityFrankfurt am MainGermany
  2. 2.Department of Child and Adolescent Psychiatry, Psychosomatics and Psychotherapy, Medical FacultyUniversity of CologneCologneGermany

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