Emotion recognition problems are frequently reported in individuals with an autism spectrum disorder (ASD). However, this research area is characterized by inconsistent findings, with atypical emotion processing strategies possibly contributing to existing contradictions. In addition, an attenuated saliency of the eyes region is often demonstrated in ASD during face identity processing. We wanted to compare reliance on mouth versus eyes information in children with and without ASD, using hybrid facial expressions. A group of six-to-eight-year-old boys with ASD and an age- and intelligence-matched typically developing (TD) group without intellectual disability performed an emotion labelling task with hybrid facial expressions. Five static expressions were used: one neutral expression and four emotional expressions, namely, anger, fear, happiness, and sadness. Hybrid faces were created, consisting of an emotional face half (upper or lower face region) with the other face half showing a neutral expression. Results showed no emotion recognition problem in ASD. Moreover, we provided evidence for the existence of top- and bottom-emotions in children: correct identification of expressions mainly depends on information in the eyes (so-called top-emotions: happiness) or in the mouth region (so-called bottom-emotions: sadness, anger, and fear). No stronger reliance on mouth information was found in children with ASD. 1. Introduction Facial expressions inform us about the feelings and state of mind of others and enable us to adjust our behavior and to react appropriately. Therefore, the ability to interpret facial expressions accurately and to derive socially relevant information from them is considered a fundamental requirement for typical reciprocal social interactions and communication [1]. Autism spectrum disorders (ASD) are pervasive developmental disorders characterized by quantitative and qualitative deficits in reciprocal social interactions and communication and by the presence of restricted and repetitive behavior patterns, interests, and activities [2]. Difficulties in recognizing, identifying, and understanding the meaning of emotions are often considered as one of the trademarks of their social problems. Different procedures have been used to examine emotion processing abilities in children and adults with ASD, with or without intellectual disability: sorting, (cross-modal) matching, and labeling tasks (for a literature review and a meta-analysis on this topic, see [3, 4], resp.). Each of these procedures has revealed problems with affect processing
References
[1]
I. Nachson, “On the modularity of face recognition: the riddle of domain specificity,” Journal of Clinical and Experimental Neuropsychology, vol. 17, no. 2, pp. 256–275, 1995.
[2]
American Psychiatric Association, Diagnostic and Statistical Manual of Mental Disorders, Washington, DC, USA, 4th edition, 2000.
[3]
M. B. Harms, A. Martin, and G. L. Wallace, “Facial emotion recognition in autism spectrum disorders: a review of behavioral and neuroimaging studies,” Neuropsychology Review, vol. 20, no. 3, pp. 290–322, 2010.
[4]
M. Uljarevic and A. Hamilton, “Recognition of emotions in autism: a formal meta-analysis,” Journal of Autism and Developmental Disorders, vol. 43, no. 7, pp. 1517–1526, 2013.
[5]
D. Tantam, L. Monaghan, H. Nicholson, and J. Stirling, “Autistic children's ability to interpret faces: a research note,” Journal of Child Psychology and Psychiatry and Allied Disciplines, vol. 30, no. 4, pp. 623–630, 1989.
[6]
G. Celani, M. W. Battacchi, and L. Arcidiacono, “The understanding of the emotional meaning of facial expressions in people with autism,” Journal of Autism and Developmental Disorders, vol. 29, no. 1, pp. 57–66, 1999.
[7]
M. J. Law Smith, B. Montagne, D. I. Perrett, M. Gill, and L. Gallagher, “Detecting subtle facial emotion recognition deficits in high-functioning Autism using dynamic stimuli of varying intensities,” Neuropsychologia, vol. 48, no. 9, pp. 2777–2781, 2010.
[8]
R. P. Hobson, “The autistic child's appraisal of expressions of emotion: a further study,” Journal of Child Psychology and Psychiatry and Allied Disciplines, vol. 27, no. 5, pp. 671–680, 1986.
[9]
S. Kuusikko, H. Haapsamo, E. Jansson-Verkasalo et al., “Emotion recognition in children and adolescents with autism spectrum disorders,” Journal of Autism and Developmental Disorders, vol. 39, no. 6, pp. 938–945, 2009.
[10]
M. Prior, B. Dahlstrom, and T.-L. Squires, “Autistic children's knowledge of thinking and feeling states in other people,” Journal of Child Psychology and Psychiatry and Allied Disciplines, vol. 31, no. 4, pp. 587–601, 1990.
[11]
J.-P. Teunisse and B. De Gelder, “Face processing in adolescents with autistic disorder: the inversion and composite effects,” Brain and Cognition, vol. 52, no. 3, pp. 285–294, 2003.
[12]
J. L. Tracy, R. W. Robins, R. A. Schriber, and M. Solomon, “Is emotion recognition impaired in individuals with autism spectrum disorders?” Journal of Autism and Developmental Disorders, vol. 41, no. 1, pp. 102–109, 2011.
[13]
B. Wright, N. Clarke, J. Jordan et al., “Emotion recognition in faces and the use of visual context Vo in young people with high-functioning autism spectrum disorders,” Autism, vol. 12, no. 6, pp. 607–626, 2008.
[14]
K. Evers, I. Noens, J. Steyaert, and J. Wagemans, “Combining strengths and weaknesses in visual perception of children with an autism spectrum disorder: perceptual matching of facial expressions,” Research in Autism Spectrum Disorders, vol. 5, no. 4, pp. 1327–1342, 2011.
[15]
G. L. Wallace, L. K. Case, M. B. Harms, J. A. Silvers, L. Kenworthy, and A. Martin, “Diminished sensitivity to sad facial expressions in high functioning autism spectrum disorders is associated with symptomatology and adaptive functioning,” Journal of Autism and Developmental Disorders, vol. 41, no. 11, pp. 1475–1486, 2011.
[16]
S. Baron-Cohen, S. Wheelwright, and T. Jolliffe, “Is there a “language of the eyes”? Evidence from normal adults, and adults with autism or Asperger Syndrome,” Visual Cognition, vol. 4, no. 3, pp. 311–331, 1997.
[17]
D. Da Fonseca, A. Santos, D. Bastard-Rosset, C. Rondan, F. Poinso, and C. Deruelle, “Can children with autistic spectrum disorders extract emotions out of contextual cues?” Research in Autism Spectrum Disorders, vol. 3, no. 1, pp. 50–56, 2009.
[18]
L. Speer, A. Cook, W. McMahon, and E. Clark, “Face processing in children with autism: effects of stimulus contents and type,” Autism, vol. 11, no. 3, pp. 265–277, 2007.
[19]
M. Behrmann, G. Avidan, G. L. Leonard et al., “Configural processing in autism and its relationship to face processing,” Neuropsychologia, vol. 44, no. 1, pp. 110–129, 2006.
[20]
S. Weigelt, K. Koldewyn, and N. Kanwisher, “Face identity recognition in autism spectrum disorders: a review of behavioral studies,” Neuroscience and Biobehavioral Reviews, vol. 36, no. 3, pp. 1060–1084, 2012.
[21]
T. Langdell, “Recognition of faces: an approach to the study of autism,” Journal of Child Psychology and Psychiatry and Allied Disciplines, vol. 19, no. 3, pp. 255–268, 1978.
[22]
D. M. Riby, G. Doherty-Sneddon, and V. Bruce, “The eyes or the mouth? Feature salience and unfamiliar face processing in Williams syndrome and autism,” Quarterly Journal of Experimental Psychology, vol. 62, no. 1, pp. 189–203, 2009.
[23]
R. M. Joseph, K. Ehrman, R. McNally, and B. Keehn, “Affective response to eye contact and face recognition ability in children with ASD,” Journal of the International Neuropsychological Society, vol. 14, no. 6, pp. 947–955, 2008.
[24]
K. Chawarska and F. Shic, “Looking but not seeing: atypical visual scanning and recognition of faces in 2 and 4-Year-old children with Autism spectrum disorder,” Journal of Autism and Developmental Disorders, vol. 39, no. 12, pp. 1663–1672, 2009.
[25]
W. Jones, K. Carr, and A. Klin, “Absence of preferential looking to the eyes of approaching adults predicts level of social disability in 2-year-old toddlers with autism spectrum disorder,” Archives of General Psychiatry, vol. 65, no. 8, pp. 946–954, 2008.
[26]
R. M. Joseph and J. Tanaka, “Holistic and part-based face recognition in children with autism,” Journal of Child Psychology and Psychiatry and Allied Disciplines, vol. 44, no. 4, pp. 529–542, 2003.
[27]
A. Klin, W. Jones, R. Schultz, F. Volkmar, and D. Cohen, “Visual fixation patterns during viewing of naturalistic social situations as predictors of social competence in individuals with autism,” Archives of General Psychiatry, vol. 59, no. 9, pp. 809–816, 2002.
[28]
B. Gepner and F. Féron, “Autism: a world changing too fast for a mis-wired brain?” Neuroscience and Biobehavioral Reviews, vol. 33, no. 8, pp. 1227–1242, 2009.
[29]
K. Pelphrey, J. Goldstein, S. Reznick, J. Piven, T. Allison, and G. McCarthy, “The influence of observed gaze shift context and timing upon activity within the superior temporal sulcus,” Journal of Cognitive Neuroscience, p. 69, 2002.
[30]
J. N. Van Der Geest, C. Kemner, G. Camfferman, M. N. Verbaten, and H. van Engeland, “Looking at images with human figures: comparison between autistic and normal children,” Journal of Autism and Developmental Disorders, vol. 32, no. 2, pp. 69–75, 2002.
[31]
V. Bruce and A. Young, “Understanding face recognition,” The British journal of psychology, vol. 77, pp. 305–327, 1986.
[32]
J. V. Haxby, E. A. Hoffman, and M. I. Gobbini, “The distributed human neural system for face perception,” Trends in Cognitive Sciences, vol. 4, no. 6, pp. 223–233, 2000.
[33]
R. Adolphs, D. Tranel, H. Damasio, and A. Damasio, “Impared recognition of emotion in facial expressions following bilateral damage to the human amygdala,” Nature, vol. 372, no. 6507, pp. 669–672, 1994.
[34]
R. Bruyer, C. Laterre, X. Seron et al., “A case of prosopagnosia with some preserved covert remembrance of familiar faces,” Brain and Cognition, vol. 2, no. 3, pp. 257–284, 1983.
[35]
T. F. Gross, “The perception of four basic emotions in human and nonhuman faces by children with autism and other developmental disabilities,” Journal of Abnormal Child Psychology, vol. 32, no. 5, pp. 469–480, 2004.
[36]
K. Rice, J. M. Moriuchi, W. Jones, and A. Klin, “Parsing heterogeneity in autism spectrum disorders: visual scanning of dynamic social scenes in school-aged children,” Journal of the American Academy of Child and Adolescent Psychiatry, vol. 51, no. 3, pp. 238–248, 2012.
[37]
M. D. Rutherford and A. M. Towns, “Scan path differences and similarities during emotion perception in those with and without autism spectrum disorders,” Journal of Autism and Developmental Disorders, vol. 38, no. 7, pp. 1371–1381, 2008.
[38]
A. J. Calder, A. M. Burton, P. Miller, A. W. Young, and S. Akamatsu, “A principal component analysis of facial expressions,” Vision Research, vol. 41, no. 9, pp. 1179–1208, 2001.
[39]
H. Eisenbarth and G. W. Alpers, “Happy mouth and sad eyes: scanning emotional facial expressions,” Emotion, vol. 11, no. 4, pp. 860–865, 2011.
[40]
M. L. Smith, G. W. Cottrell, F. Gosselin, and P. G. Schyns, “Transmitting and decoding facial expressions,” Psychological Science, vol. 16, no. 3, pp. 184–189, 2005.
[41]
E. Scheller, C. Büchel, and M. Gamer, “Diagnostic features of emotional expressions are processed preferentially,” PLoS ONE, vol. 7, no. 7, Article ID e41792, 2012.
[42]
C. Lord, S. Risi, L. Lambrecht et al., “The Autism Diagnostic Observation Schedule-Generic: a standard measure of social and communication deficits associated with the spectrum of autism,” Journal of Autism and Developmental Disorders, vol. 30, no. 3, pp. 205–223, 2000.
[43]
D. Wechsler, Wechsler Intelligence Scale for Children, The Psychological Corporation, London, UK, 3rd edition, 1992.
[44]
P. J. Tellegen, J. A. Laros, and M. Winkel, SON-R 2 1/2-7 Niet-Verbale Intelligentietest, Hogrefe, Amsterdam, The Netherlands, 2003.
[45]
J. Grégoire, L’Evaluation clinique de l’intelligence de l’enfant: Théorie et pratique du WISC-III, Mardaga, Sprimont, Belgium, 2000.
[46]
M. N. Dailey, G. W. Cottrell, and J. Reilly, “California Facial Expressions (CAFE),” Computer Science and Engineering Departement, UCSD, La Jolla, Calif, USA, 2001, http://www.cs.ucsd.edu/users/gary/CAFE/.
[47]
P. Ekman and W. V. Friesen, The Facial Action Coding System (FACS): A Technique for the Measurement of Facial Action, Consulting Psychologists Press, Palo Alto, Calif, USA, 1978.
[48]
E. Pellicano and G. Rhodes, “Holistic processing of faces in preschool children and adults,” Psychological Science, vol. 14, no. 6, pp. 618–622, 2003.
[49]
S. Carey and R. Diamond, “Are faces perceived as configurations? More by adults than by children?” Visual Cognition, vol. 1, no. 2/3, pp. 253–274, 1994.
[50]
F. Happé and U. Frith, “The weak coherence account: detail-focused cognitive style in autism spectrum disorders,” Journal of Autism and Developmental Disorders, vol. 36, no. 1, pp. 5–25, 2006.
[51]
L. Mottron, M. Dawson, I. Soulières, B. Hubert, and J. Burack, “Enhanced perceptual functioning in autism: an update, and eight principles of autistic perception,” Journal of Autism and Developmental Disorders, vol. 36, no. 1, pp. 27–43, 2006.
[52]
C. F. Norbury, J. Brock, L. Cragg, S. Einav, H. Griffiths, and K. Nation, “Eye-movement patterns are associated with communicative competence in autistic spectrum disorders,” Journal of Child Psychology and Psychiatry and Allied Disciplines, vol. 50, no. 7, pp. 834–842, 2009.
