Journal of Neural Transmission

, Volume 121, Issue 9, pp 1171–1181 | Cite as

Impairment in face processing in autism spectrum disorder: a developmental perspective

  • Ellen GreimelEmail author
  • Martin Schulte-Rüther
  • Inge Kamp-Becker
  • Helmut Remschmidt
  • Beate Herpertz-Dahlmann
  • Kerstin Konrad
Psychiatry and Preclinical Psychiatric Studies - Original Article


Findings on face identity and facial emotion recognition in autism spectrum disorder (ASD) are inconclusive. Moreover, little is known about the developmental trajectory of face processing skills in ASD. Taking a developmental perspective, the aim of this study was to extend previous findings on face processing skills in a sample of adolescents and adults with ASD. N = 38 adolescents and adults (13–49 years) with high-functioning ASD and n = 37 typically developing (TD) control subjects matched for age and IQ participated in the study. Moreover, n = 18 TD children between the ages of 8 and 12 were included to address the question whether face processing skills in ASD follow a delayed developmental pattern. Face processing skills were assessed using computerized tasks of face identity recognition (FR) and identification of facial emotions (IFE). ASD subjects showed impaired performance on several parameters of the FR and IFE task compared to TD control adolescents and adults. Whereas TD adolescents and adults outperformed TD children in both tasks, performance in ASD adolescents and adults was similar to the group of TD children. Within the groups of ASD and control adolescents and adults, no age-related changes in performance were found. Our findings corroborate and extend previous studies showing that ASD is characterised by broad impairments in the ability to process faces. These impairments seem to reflect a developmentally delayed pattern that remains stable throughout adolescence and adulthood.


Autism spectrum disorder Development Age Face recognition Emotion 



We are grateful to all participants with their families who took part in this study.

Conflict of interest

B. H.-D. receives industry research funding from Vifor Pharma. K. K. received speaking fees from Novartis and Medice. All other authors declare that they have no conflicts of interest.


  1. Achenbach TM (1993) Empirically based taxonomy: how to use syndromes and profile types derived from the CBCL from 4 to 18, TRF, and WSR. University of Vermont, Department of Psychiatry, BurlingtonGoogle Scholar
  2. Adolphs R, Sears L, Piven J (2001) Abnormal processing of social information from faces in autism. J Cogn Neurosci 13:232–240PubMedCrossRefGoogle Scholar
  3. American Psychological Association (1994) Diagnostic and statistical manual of mental disorders (DSM-IV). American Psychiatric Press, Washington, DCGoogle Scholar
  4. Aylward EH, Minshew NJ, Goldstein G, Honeycutt NA, Augustine AM, Yates KO, Barta PE, Pearlson GD (1999) MRI volumes of amygdala and hippocampus in non-mentally retarded autistic adolescents and adults. Neurology 53(9):2145–2150PubMedCrossRefGoogle Scholar
  5. Aylward EH, Park JE, Field KM, Parsons AC, Richards TL, Cramer SC, Meltzoff AN (2005) Brain activation during face perception: evidence of a developmental change. J Cogn Neurosci 17(2):308–319PubMedCrossRefGoogle Scholar
  6. Bal E, Harden E, Lamb D, Van Hecke AV, Denver JW, Porges SW (2010) Emotion recognition in children with autism spectrum disorders: relations to eye gaze and autonomic state. J Autism Dev Disord 40:358–370PubMedCrossRefGoogle Scholar
  7. Baron-Cohen S, Jolliffe T, Mortimore C, Robertson M (1997) Another advanced test of theory of mind: evidence from very high functioning adults with autism or Asperger syndrome. J Child Psychol Psychiat 38:813–822PubMedCrossRefGoogle Scholar
  8. Baron-Cohen S, Wheelwright S, Skinner R, Martin J, Clubley E (2001) The autism-spectrum quotient (AQ): evidence from Asperger syndrome/high-functioning autism, males and females, scientists and mathematicians. J Autism Dev Disord 31(1):5–17PubMedCrossRefGoogle Scholar
  9. Batty M, Taylor MJ (2006) The development of emotional face processing during childhood. Dev Sci 9(2):207–220PubMedCrossRefGoogle Scholar
  10. Baudouin JY, Gallay M, Durand K, Robichon F (2010) The development of perceptual sensitivity to second-order facial relations in children. J Exp Child Psychol 107(3):195–206PubMedCrossRefGoogle Scholar
  11. Blass EM, Camp CA (2004) The ontogeny of face identity: I. Eight- to 21-week-old infants use internal and external face features in identity. Cognition 92(3):305–327. doi: 10.1016/j.cognition.2003.10.004 PubMedCrossRefGoogle Scholar
  12. Boelte S, Poustka F (2003) The recognition of facial affect in autistic and schizophrenic subjects and their first-degree relatives. Psychol Med 33:907–915CrossRefGoogle Scholar
  13. Boelte S, Poustka F (2006) Fragebogen zur Sozialen Kommunikation (FSK): Autismus Screening. Hans Huber, BernGoogle Scholar
  14. Boelte S, Ruehl D, Schmoetzer G, Poustka F (2006a) ADI-R Diagnostisches Interview for Autismus-Revidiert. Deutsche Fassung des Autism Diagnostic Interview: revised. Hogrefe, GöttingenGoogle Scholar
  15. Boelte SHD, Feineis-Matthews S, Prvulovic D, Dierks T, Poustka F (2006b) Facial affect recognition training in autism: can we animate the fusiform gyrus? Behav Neurosci 120(1):211–216CrossRefGoogle Scholar
  16. Boraston Z, Blakemore SJ, Chilvers R, Skuse D (2007) Impaired sadness recognition is linked to social interaction deficit in autism. Neuropsychologia 45:1501–1510PubMedCrossRefGoogle Scholar
  17. Bormann-Kischkel C, Vilsmeider M, Baude B (1995) The development of emotional concepts in autism. J Child Psychol Psychiat 36:1243–1259PubMedCrossRefGoogle Scholar
  18. Boucher J, Lewis V (1992) Unfamiliar face recognition in relatively able autistic children. J Child Psychol Psychiat 33:843–859PubMedCrossRefGoogle Scholar
  19. Carey S, Diamond R, Woods B (1980) The development of face recognition: a maturational component. Dev Psychol 16:257–269CrossRefGoogle Scholar
  20. Celani G, Battacchi MW, Arcidiacono L (1999) The understanding of the emotional meaning of facial expressions in people with autism. J Autism Dev Disord 29:57–66PubMedCrossRefGoogle Scholar
  21. Crookes K, McKone E (2009) Early maturity of face recognition: no childhood development of holistic processing, novel face encoding, or face-space. Cognition 111(2):219–247. doi: 10.1016/j.cognition.2009.02.004 PubMedCrossRefGoogle Scholar
  22. Dalton KM, Nacewicz BM, Alexander AL, Davidson RJ (2007) Gaze-fixation, brain activation and amygdala volume in unaffected siblings of individuals with autism. Biol Psychiatry 61:512–520PubMedCrossRefGoogle Scholar
  23. Derogatis LR (1993) Brief Symptom Inventory (BSI), administration, scoring, and procedures manual. National Computer Services, MinneapolisGoogle Scholar
  24. Deruelle C, Rondan C, Gepner B, Tardif C (2004) Spatial frequency and face processing in children with autism and Asperger syndrome. J Autism Dev Disord 34(2):199–210PubMedCrossRefGoogle Scholar
  25. DeSonneville LMJ (2001) ANT 2.1 Amsterdam Neuropsychological Tasks, Manual. Sonar, AmstelveenGoogle Scholar
  26. Doepfner M, Schmeck K, Berner W (1994) Handbuch: Elternfragebogen über das Verhalten von Kindern und Jugendlichen. Forschungsergebnisse zur deutschen Fassung der Child Behavior Checklist (CBCL/4-18). Arbeitsgruppe Kinder-, Jugend- und Familiendiagnostik (KJFD), KölnGoogle Scholar
  27. Durand K, Gallay M, Seigneuric A, Robichon F, Baudouin JY (2007) The development of facial emotion recognition: the role of configural information. J Exp Child Psychol 97(1):14–27. doi: 10.1016/j.jecp.2006.12.001 PubMedCrossRefGoogle Scholar
  28. Dyck MJ, Piek JP, Hay D, Smith L, Hallmayer J (2006) Are abilities abnormally interdependent in children with autism? J Clin Child Adolesc Psychol 35(1):20–33. doi: 10.1207/s15374424jccp3501_3 PubMedCrossRefGoogle Scholar
  29. Flowe HD (2012) Do characteristics of faces that convey trustworthiness and dominance underlie perceptions of criminality? PLoS ONE 7:e37253PubMedCentralPubMedCrossRefGoogle Scholar
  30. Gepner B, Deruelle C, Grynfeltt S (2001) Motion and emotion: a novel approach to the study of face processing by young autistic children. J Autism Dev Disord 31(1):37–45PubMedCrossRefGoogle Scholar
  31. Greimel E, Schulte-Rüther M, Fink GR, Piefke M, Herpertz-Dahlmann B, Konrad K (2010) Development of neural correlates of empathy from childhood to early adulthood: an fMRI study in boys and adult men. J Neural Transm 117:781–791PubMedCrossRefGoogle Scholar
  32. Guyer AE, Monk CS, McClure-Tone EB, Nelson EE, Roberson-Nay R, Adler AD, Fromm SJ, Leibenluft E, Pine DS, Ernst M (2008) A developmental examination of amygdala response to facial expressions. J Cogn Neurosci 20(9):1565–1582PubMedCentralPubMedCrossRefGoogle Scholar
  33. Harms M, Martin A, Wallace G (2010) Facial emotion recognition in autism spectrum disorders: a review of behavioral and neuroimaging studies. Neuropsychol Rev 20(3):290–322PubMedCrossRefGoogle Scholar
  34. Herba CP (2004) Annotation: development of facial expression recognition from childhood to adolescence: behavioural and neurological perspectives. J Child Psychol Psychiat 45(7):1185–1198PubMedCrossRefGoogle Scholar
  35. Hobson RP (1986) The autistic child´s appraisal of expressions of emotion. J Child Psychol Psychiat 27:321–342Google Scholar
  36. Hobson RP, Ouston J, Lee A (1988) What is in a face? The case of autism. Br J Psychol 79:441–453PubMedCrossRefGoogle Scholar
  37. Humphreys K, Minshew N, Leonard GL, Behrmann M (2011) A fine-grained analysis of facial expression processing in high-functioning adults with autism. Neuropsychologia 45:685–695CrossRefGoogle Scholar
  38. Kaufman J, Birmaher B, Brent D, Rao U, Flynn C, Moreci P, Williamson D, Ryan N (1997) Schedule for AFFECTIVE disorders and schizophrenia for school-age children-present and lifetime version (K-SADS-PL): initial reliability and validity data. J Am Acad Child Adolesc Psychiatry 36:980–988PubMedCrossRefGoogle Scholar
  39. Kenworthy L, Yerys BE, Anthony LG, Wallace GL (2008) Understanding executive control in autism spectrum disorders in the lab and in the real world. Neuropsychol Rev 18:320–338PubMedCentralPubMedCrossRefGoogle Scholar
  40. Kirchner J, Hatri A, Heekeren H, Dziobek I (2011) Autistic symptomatology, face processing abilities, and eye fixation patterns. J Autism Dev Disord 41(2):158–167PubMedCrossRefGoogle Scholar
  41. Klin A, Sparrow SS, de Bildt A, Cicchetti DV, Cohen DJ, Volkmar FR (1999) A normed study of face recognition in autism and related disorders. J Autism Dev Disord 29:499–508PubMedCrossRefGoogle Scholar
  42. Kolb B, Wilson B, Taylor L (1992) Developmental changes in the recognition and comprehension of facial expression: implications for frontal lobe function. Brain Cogn 20:74–84PubMedCrossRefGoogle Scholar
  43. Krebs J, Biswas A, Pascalis O, Kamp-Becker I, Remschmidt H, Schwarzer G (2011) Face processing in children with AUTISM spectrum disorder: independent or interactive processing of facial identity and facial expression? J Autism Dev Disord 41(6):796–804PubMedCrossRefGoogle Scholar
  44. Kuusikko S, Haapsamo H, Jansson-Verkasalo E, Hurtig T, Mattila ML, Ebeling H, Jussila K, Boelte S, Moilanen I (2009) Emotion recognition in children and adolescents with autism spectrum disorders. J Autism Dev Disord 39(6):938–945PubMedCrossRefGoogle Scholar
  45. Lahaie A, Mottron L, Arguin M, Berthiaume C, Jemel B, Saumier D (2006) Face perception in high-functioning autistic adults: evidence for superior processing of face parts, not for a configural face-processing deficit. Neuropsychology 20:30–41PubMedCrossRefGoogle Scholar
  46. Langdell T (1978) Recognition of faces: an approach to the study of autism. J Child Psychol Psychiat 19:255–268PubMedCrossRefGoogle Scholar
  47. LeCouteur A, Rutter M, Lord C, Rios P, Robertson S, Holdgrafer M, McLennan J (1989) Autism diagnostic interview: a standardized investigator-based instrument. J Autism Dev Disord 19(3):363–387CrossRefGoogle Scholar
  48. Lee JE, Bigler ED, Alexander AL, Lazar M, DuBray MB, Chung MK, Johnson M, Morgan J, Miller JN, McMahon WM, Lu J, Jeong EK, Lainhart JE (2007) Diffusion tensor imaging of white matter in the superior temporal gyrus and temporal stem in autism. Neurosci Lett 424(2):127–132. doi: 10.1016/j.neulet.2007.07.042 PubMedCrossRefGoogle Scholar
  49. Lord C, Risi S, Lambrecht L, Cook EH, Leventhal B, DiLavore PC, Pickels A, Rutter M (2000) The ADOS-G (autism diagnostic observation schedule-generic): a standard measure of social-communication deficits associated with autism spectrum disorders. J Autism Dev Disord 30:205–223PubMedCrossRefGoogle Scholar
  50. Mondloch CJ, Le Grand R, Maurer D (2002) Configural face processing develops more slowly than featural face processing. Perception 31:553–566PubMedCrossRefGoogle Scholar
  51. Monk CS, McClure EB, Nelson EE, Zarahn E, Bilder RM, Leibenluft E, Charney DS, Ernst M, Pine DS (2003) Adolescent immaturity in attention-related brain engagement to emotional facial expressions. Neuroimage 20:420–428PubMedCrossRefGoogle Scholar
  52. Murphy K, Barkley RA (1995) Preliminary normative data on DSM-IV criteria for adults. ADHD Report 3:6–7Google Scholar
  53. Neumann D, Spezio ML, Piven J, Adolphs R (2006) Looking you in the mouth: abnormal gaze in autism resulting from impaired top-down modulation of visual attention. Soc Cogn Affect Neurosci 1(3):194–202PubMedCentralPubMedCrossRefGoogle Scholar
  54. O’Hearn K, Schroer E, Minshew N, Luna B (2010) Lack of developmental improvement on a face memory task during adolescence in autism. Neuropsychologia 48(13):3955–3960. doi: 10.1016/j.neuropsychologia.2010.08.024 PubMedCentralPubMedCrossRefGoogle Scholar
  55. O’Connor K, Hamm JP, Kirk IJ (2005) The neurophysiological correlates of face processing in adults and children with Asperger’s syndrome. Brain Cogn 59(1):82–95. doi: 10.1016/j.bandc.2005.05.004 PubMedCrossRefGoogle Scholar
  56. Organization WH (1993) The ICD-10 classification of mental and behavioural disorders: diagnostic criteria for research. World Health Organization, GenevaGoogle Scholar
  57. Peelen MV, Glaser B, Vuilleumier P, Eliez S (2009) Differential development of selectivity for faces and bodies in the fusiform gyrus. Dev Sci 12(6):F16–F25PubMedCrossRefGoogle Scholar
  58. Raznahan A, Toro R, Daly E, Robertson D, Murphy C, Deeley Q, Bolton PF, Paus T, Murphy DGM (2010) Cortical anatomy in autism spectrum disorder: an in vivo MRI study on the effect of age. Cereb Cortex 20(6):1332–1340PubMedCrossRefGoogle Scholar
  59. Rossion BG (2002) How does the brain process upright and inverted faces? Behav Cogn Neurosci Rev 2002:63–75CrossRefGoogle Scholar
  60. Ruehl D, Boelte S, Feineis-Matthews S, Poustka F (2004) ADOS. Diagnostische beobachtungsskala fuer autistische stoerungen, Hans HuberGoogle Scholar
  61. Rump KM, Giovannelli JL, Minshew NJ, Strauss MS (2009) The development of emotion recognition in individuals with autism. Child Dev 80(5):1434–1447PubMedCentralPubMedCrossRefGoogle Scholar
  62. Rutter M, Bailey A, Lord C (2003) Social communication questionnaire (SCQ). Western Psychological Services, Los AngelesGoogle Scholar
  63. Schultz RT (2005) Developmental deficits in social perception in autism: the role of the amygdala and fusiform face area. Int J Dev Neurosci 23:125–141PubMedCrossRefGoogle Scholar
  64. Tantam D, Monoghan L, Nicholson H, Stirling J (1989) Autistic children’s ability to interpret faces: a research note. J Child Psychol Psychiat 30:623–630PubMedCrossRefGoogle Scholar
  65. Thomas LA, De Bellis MD, Graham R, LaBar KS (2007) Development of emotional facial recognition in late childhood and adolescence. Dev Sci 10:547–558PubMedCrossRefGoogle Scholar
  66. Uono S, Sato W, Toichi M (2011) The specific impairment of fearful expression recognition and its atypical development in pervasive developmental disorder. Soc Neurosci 6:452–463PubMedCrossRefGoogle Scholar
  67. Walker-Andrews AS (1997) Infantsï perception of expressive behaviors: differentiation of multimodal information. Psychol Bull 121:437–456Google Scholar
  68. Wallace GL, Dankner N, Kenworthy L, Giedd JN, Martin A (2010) Age-related temporal and parietal cortical thinning in autism spectrum disorders. Brain 133(12):3745–3754PubMedCentralPubMedCrossRefGoogle Scholar
  69. Wang AT, Lee SS, Sigman M, Dapretto M (2006) Developmental changes in the neural basis of interpreting communicative intent. Soc Cogn Affect Neurosci 1:107–121PubMedCentralPubMedCrossRefGoogle Scholar
  70. Wechsler D (1991) Manual for the Wechsler Intelligence Scale for Children, 3rd edn. Psychological Corporation, San AntonioGoogle Scholar
  71. Wechsler D (1997) Wechsler Adult Intelligence Scale-III manualGoogle Scholar
  72. Weigelt S, Koldewyn K, Kanwisher N (2012) Face identity recognition in autism spectrum disorders: a review of behavioral studies. Neurosci Biobehav Rev 36(3):1060–1084PubMedCrossRefGoogle Scholar
  73. Wolf JM, Tanaka JW, Klaiman C, Cockburn J, Herlihy L, Brown C, South M, McPartland J, Kaiser MD, Phillips R, Schultz RT (2008) Specific impairment of face-processing abilities in children with autism spectrum disorder using the Let’s Face It! skills battery. Autism Res 1(6):329–340PubMedCrossRefGoogle Scholar
  74. Wright B, Clarke N, Jordan JO, Young AW, Clarke P, Miles J, Nation K, Clarke L, Williams C (2008) Emotion recognition in faces and the use of visual context Vo in young people with high-functioning autism spectrum disorders. Autism 12(6):607–626PubMedCrossRefGoogle Scholar
  75. Young AW, Hellawell D, Hay DC (1987) Configural information in face perception. Perception 16:747–759PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Wien 2014

Authors and Affiliations

  • Ellen Greimel
    • 1
    • 2
    • 3
    Email author
  • Martin Schulte-Rüther
    • 1
  • Inge Kamp-Becker
    • 4
  • Helmut Remschmidt
    • 4
  • Beate Herpertz-Dahlmann
    • 2
  • Kerstin Konrad
    • 1
  1. 1.Child Neuropsychology Section, Department of Child and Adolescent Psychiatry, Psychosomatics and PsychotherapyUniversity Hospital of the RWTH AachenAachenGermany
  2. 2.Department of Child and Adolescent Psychiatry, Psychosomatics and PsychotherapyUniversity Hospital of the RWTH AachenAachenGermany
  3. 3.Department of Child and Adolescent Psychiatry, Psychosomatics and PsychotherapyUniversity Hospital MunichMunichGermany
  4. 4.Department of Child and Adolescent PsychiatryUniversity Hospital Giessen and MarburgCampus MarburgGermany

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