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Deficits in facial, body movement and vocal emotional processing in autism spectrum disorders

Published online by Cambridge University Press:  27 January 2010

R. C. M. Philip ,
H. C. Whalley ,
A. C. Stanfield ,
R. Sprengelmeyer ,
I. M. Santos ,
A. W. Young ,
A. P. Atkinson ,
A. J. Calder ,
E. C. Johnstone  and
S. M. Lawrie
...Show all authors
R. C. M. Philip*
Affiliation:
Division of Psychiatry, University of Edinburgh, UK
H. C. Whalley
Affiliation:
Division of Psychiatry, University of Edinburgh, UK
A. C. Stanfield
Affiliation:
Division of Psychiatry, University of Edinburgh, UK
R. Sprengelmeyer
Affiliation:
School of Psychology, University of St Andrews, UK
I. M. Santos
Affiliation:
Department of Educational Sciences, University of Aveiro, Portugal
A. W. Young
Affiliation:
Department of Psychology, University of York, UK
A. P. Atkinson
Affiliation:
Department of Psychology, University of Durham, UK
A. J. Calder
Affiliation:
MRC Cognition and Brain Sciences Unit, University of Cambridge, UK
E. C. Johnstone
Affiliation:
Division of Psychiatry, University of Edinburgh, UK
S. M. Lawrie
Affiliation:
Division of Psychiatry, University of Edinburgh, UK
J. Hall
Affiliation:
Division of Psychiatry, University of Edinburgh, UK
*
*Address for correspondence: Dr R. C. M. Philip, Division of Psychiatry, University of Edinburgh, Kennedy Tower, Royal Edinburgh Hospital, EdinburghEH10 5HF, UK. (Email: [email protected])
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Abstract

Background

Previous behavioural and neuroimaging studies of emotion processing in autistic spectrum disorder (ASD) have focused on the use of facial stimuli. To date, however, no studies have examined emotion processing in autism across a broad range of social signals.

Method

This study addressed this issue by investigating emotion processing in a group of 23 adults with ASD and 23 age- and gender-matched controls. Recognition of basic emotions (‘happiness’, ‘sadness’, ‘anger’, disgust' and ‘fear’) was assessed from facial, body movement and vocal stimuli. The ability to make social judgements (such as approachability) from facial stimuli was also investigated.

Results

Significant deficits in emotion recognition were found in the ASD group relative to the control group across all stimulus domains (faces, body movements and voices). These deficits were seen across a range of emotions. The ASD group were also impaired in making social judgements compared to the control group and this correlated with impairments in basic emotion recognition.

Conclusions

This study demonstrates that there are significant and broad-ranging deficits in emotion processing in ASD present across a range of stimulus domains and in the auditory and visual modality; they cannot therefore be accounted for simply in terms of impairments in face processing or in the visual modality alone. These results identify a core deficit affecting the processing of a wide range of emotional information in ASD, which contributes to the impairments in social function seen in people with this condition.

Keywords

Autismemotionfacegesturevocal
Type
Original Articles
Information
Psychological Medicine , Volume 40 , Issue 11 , November 2010 , pp. 1919 - 1929
Copyright
Copyright © Cambridge University Press 2010

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References

Adolphs, R, Sears, L, Piven, J (2001). Abnormal processing of social information from faces in autism. Journal of Cognitive Neuroscience 13, 232–240.CrossRefGoogle ScholarPubMed
Ashwin, C, Baron-Cohen, S, Wheelwright, S, O'Riordan, M, Bullmore, ET (2007). Differential activation of the amygdala and the ‘social brain’ during fearful face-processing in Asperger syndrome. Neuropsychologia 45, 2–14.CrossRefGoogle ScholarPubMed
Atkinson, AP, Dittrich, WH, Gemmell, AJ, Young, AW (2004). Emotion perception from dynamic and static body expressions in point-light and full-light displays. Perception 33, 717–746.CrossRefGoogle ScholarPubMed
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. Journal of Child Psychology and Psychiatry 38, 813–822.CrossRefGoogle ScholarPubMed
Baron-Cohen, S, Richler, J, Bisarya, D, Gurunathan, N, Wheelwright, S (2003). The systemizing quotient: an investigation of adults with Asperger syndrome or high-functioning autism, and normal sex differences. Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences 358, 361–374.CrossRefGoogle ScholarPubMed
Baron-Cohen, S, Ring, HA, Wheelwright, S, Bullmore, ET, Brammer, MJ, Simmons, A, Williams, SCR (1999). Social intelligence in the normal and autistic brain: an fMRI study. European Journal of Neuroscience 11, 1891–1898.CrossRefGoogle Scholar
Baron-Cohen, S, Wheelwright, S (2004). The empathy quotient: an investigation of adults with Asperger syndrome or high functioning autism, and normal sex differences. Journal of Autism and Developmental Disorders 34, 163–175.CrossRefGoogle ScholarPubMed
Baron-Cohen, S, Wheelwright, S, Hill, J, Raste, Y, Plumb, I (2001 a). The ‘Reading the Mind in the Eyes’ Test revised version: a study with normal adults, and adults with Asperger syndrome or high-functioning autism. Journal of Child Psychology and Psychiatry, and Allied Disciplines 42, 241–251.CrossRefGoogle ScholarPubMed
Baron-Cohen, S, Wheelwright, S, Skinner, R, Martin, J, Clubley, E (2001 b). The Autism-Spectrum Quotient (AQ): evidence from Asperger syndrome/high-functioning autism, males and females, scientists and mathematicians. Journal of Autism and Developmental Disorders 31, 5–17.CrossRefGoogle ScholarPubMed
Benton, AL, Hamsher, KS, Varney, N (1983). Contributions to Neuropsychological Assessment: A Clinical Manual. Oxford University Press: Oxford.Google Scholar
Blake, R, Turner, LM, Smoski, MJ, Pozdol, SL, Stone, WL (2003). Visual recognition of biological motion is impaired in children with autism. Psychological Science 14, 151–157.CrossRefGoogle ScholarPubMed
Calder, AJ, Keane, J, Lawrence, AD, Manes, F (2004). Impaired recognition of anger following damage to the ventral striatum. Brain 127, 1958–1969.CrossRefGoogle Scholar
Castelli, F, Frith, C, Happe, F, Frith, U (2002). Autism, Asperger syndrome and brain mechanisms for the attribution of mental states to animated shapes. Brain 125, 1839–1849.CrossRefGoogle ScholarPubMed
Celani, G, Battacchi, MW, Arcidiacono, L (1999). The understanding of the emotional meaning of facial expressions in people with autism. Journal of Autism and Developmental Disorders 29, 57–66.CrossRefGoogle ScholarPubMed
Critchley, HD, Daly, EM, Bullmore, ET, Williams, SCR, Van Amelsvoort, T, Robertson, DM, Rowe, A, Phillips, M, McAlonan, G, Howlin, P, Murphy, DGM (2000). The functional neuroanatomy of social behaviour: changes in cerebral blood flow when people with autistic disorder process facial expressions. Brain 123, 2203–2212.CrossRefGoogle ScholarPubMed
Dalton, KM, Nacewicz, BM, Johnstone, T, Schaefer, HS, Gernsbacher, MA, Goldsmith, HH, Alexander, AL, Davidson, RJ (2005). Gaze fixation and the neural circuitry of face processing in autism. Nature Neuroscience 8, 519–526.CrossRefGoogle ScholarPubMed
Deeley, Q, Daly, EM, Surguladze, S, Page, L, Toal, F, Robertson, D, Curran, S, Giampietro, V, Seal, M, Brammer, MJ, Andrew, C, Murphy, K, Phillips, ML, Murphy, DGM (2007). An event related functional magnetic resonance imaging study of facial emotion processing in Asperger syndrome. Biological Psychiatry 62, 207–217.CrossRefGoogle ScholarPubMed
Ekman, P, Friesen, WV (1976). Pictures of Facial Affect. Consulting Psychologists Press: Palo Alto, CA.Google Scholar
Frith, U (2001). Mind blindness and the brain in autism. Neuron 32, 969–979.CrossRefGoogle ScholarPubMed
Hall, GBC, Szechtman, H, Nahmias, C (2003). Enhanced salience and emotion recognition in autism: a PET study. American Journal of Psychiatry 160, 1439–1441.CrossRefGoogle ScholarPubMed
Hall, J, Harris, JM, Sprengelmeyer, R, Sprengelmeyer, A, Young, AW, Santos, IM, Johnstone, EC, Lawrie, SM (2004). Social cognition and face processing in schizophrenia. British Journal of Psychiatry 185, 169–170.CrossRefGoogle ScholarPubMed
Happe, F, Ehlers, S, Fletcher, P, Frith, U, Johansson, M, Gillberg, C, Dolan, R, Frackowiak, R, Frith, C (1996). ‘Theory of mind’ in the brain. Evidence from a PET scan study of Asperger syndrome. Neuroreport 8, 197–201.CrossRefGoogle ScholarPubMed
Hobson, RP, Ouston, J, Lee, A (1988). What's in a face? The case of autism. British Journal of Psychology 79, 441.CrossRefGoogle Scholar
Howard, MA, Cowell, PE, Boucher, J, Broks, P, Mayes, A, Farrant, A, Roberts, N (2000). Convergent neuroanatomical and behavioural evidence of an amygdala hypothesis of autism. Neuroreport 11, 2931–2935.CrossRefGoogle ScholarPubMed
Hubert, B, Wicker, B, Moore, D, Monfardini, E, Duverger, H, Fonséca, D, Deruelle, C (2007). Brief report: recognition of emotional and non-emotional biological motion in individuals with autistic spectrum disorders. Journal of Autism and Developmental Disorders 37, 1386–92.CrossRefGoogle ScholarPubMed
Klin, A, Jones, W, Schultz, R, Volkmar, F, Cohen, D (2002). Visual fixation patterns during viewing of naturalistic social situations as predictors of social competence in individuals with autism. Archives of General Psychiatry 59, 809–816.CrossRefGoogle ScholarPubMed
Koshino, H, Kana, RK, Keller, TA, Cherkassky, VL, Minshew, NJ, Just, MA (2008). fMRI investigation of working memory for faces in autism: visual coding and underconnectivity with frontal areas. Cerebral Cortex 18, 289–300.CrossRefGoogle ScholarPubMed
Lord, C, Risi, S, Lambrecht, L, Cook, EH, Leventhal, BL, DiLavore, PC, Pickles, A, Rutter, M (2000). 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 30, 205–223.CrossRefGoogle ScholarPubMed
Matsumoto, D, Ekman, P (1988). Japanese and Caucasian Facial Expressions of Emotion (JACFEE) and Neutral Faces (JACNeuF). Department of Psychology, San Francisco State University: San Francisco, CA.Google Scholar
Mazefsky, C, Oswald, D (2007). Emotion perception in Asperger's syndrome and high-functioning autism: the importance of diagnostic criteria and cue intensity. Journal of Autism and Developmental Disorders 37, 1086–1095.CrossRefGoogle ScholarPubMed
Moore, DG, Hobson, RP, Lee, A (1997). Components of person perception: an investigation with autistic, non-autistic retarded and typically developing children and adolescents. British Journal of Developmental Psychology 15, 401–423.CrossRefGoogle Scholar
Murray, I, Arnott, J (1993). Toward the simulation of emotion in synthetic speech: a review of the literature on the human vocal emotion. Journal of the Acoustical Society of America 93, 1097–1108.CrossRefGoogle ScholarPubMed
O'Connor, K (2007). Brief report: impaired identification of discrepancies between expressive faces and voices in adults with Asperger's syndrome. Journal of Autism and Developmental Disorders 37, 2008–2013.CrossRefGoogle ScholarPubMed
Ogai, M, Matsumoto, H, Suzuki, K, Ozawa, F, Fukuda, R, Uchiyama, I, Suckling, J, Isoda, H, Mori, N, Takei, N (2003). fMRI study of recognition of facial expressions in high-functioning autistic patients. Neuroreport 14, 559–563.CrossRefGoogle ScholarPubMed
Pelphrey, KA, Sasson, NJ, Reznick, JS, Paul, G, Goldman, BD, Piven, J (2002). Visual scanning of faces in autism. Journal of Autism and Developmental Disorders 32, 249–261.CrossRefGoogle ScholarPubMed
Piggot, J, Kwon, H, Mobbs, D, Blasey, C, Lotspeich, L, Menon, V, Bookheimer, S, Reiss, AL (2004). Emotional attribution in high-functioning individuals with autistic spectrum disorder: a functional imaging study. Journal of the American Academy of Child and Adolescent Psychiatry 43, 473–480.CrossRefGoogle ScholarPubMed
Rutherford, MD, Baron-Cohen, S, Wheelwright, S (2002). Reading the mind in the voice: a study with normal adults and adults with Asperger syndrome and high functioning autism. Journal of Autism and Developmental Disorders 32, 189–194.CrossRefGoogle Scholar
Santos, IM (2003). Perception of social characteristics from faces. Ph.D. thesis, University of York, UK.Google Scholar
Santos, IM, Young, AW (2008). Effects of inversion and negation on social inferences from faces. Perception 37, 1061–1078.CrossRefGoogle ScholarPubMed
Sasson, N (2006). The development of face processing in autism. Journal of Autism and Developmental Disorders 36, 381–394.CrossRefGoogle ScholarPubMed
Spezio, ML, Adolphs, R, Hurley, RSE, Piven, J (2007). Analysis of face gaze in autism using ‘Bubbles’. Neuropsychologia 45, 144–151.CrossRefGoogle ScholarPubMed
Wang, AT, Dapretto, M, Hariri, AR, Sigman, M, Bookheimer, SY (2004). Neural correlates of facial affect processing in children and adolescents with autism spectrum disorder. Journal of the American Academy of Child and Adolescent Psychiatry 43, 481–490.CrossRefGoogle ScholarPubMed
Young, AW, Perrett, DI, Calder, AJ, Sprengelmeyer, R, Ekman, P (2002). Facial Expressions of Emotion: Stimuli and Tests (FEEST). Thames Valley Test Company: Bury St Edmunds.Google Scholar
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