Discriminating between facial expressions of anger and fear by individuals with high-functioning autism spectrum disorder

Abstract

This study examined the effects of facial color on emotion recognition in individuals with high-functioning autism spectrum disorder compared to typically developing individuals. A total of 34 participants with high-functioning autism spectrum disorder and 39 typically developing individuals underwent two cognitive facial expression tasks using images altered to have a reddish color representing anger. Task 1 required participants to categorize images as either fear or anger as the emotion corresponding to the image, while Task 2 required ranking the images along a continuum from anger to fear. Results showed that individuals with high-functioning autism spectrum disorder exhibited a facial color effect similar to typically developing participants but had lower accuracy in recognizing facial emotions. Interestingly, the color effect was less pronounced in Japanese individuals with autism spectrum disorder when viewing faces of the same race, but more pronounced for unfamiliar European faces. This suggests that individuals with high-functioning autism spectrum disorder may develop compensatory strategies for recognizing facial expressions, and that cultural and racial factors influence emotion perception in individuals with autism spectrum disorder.

Keywords

facial expression facial recognition autism spectrum disorder race factors anger

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References

Adams

F. M.

Osgood

C. E.

(1973). A cross-cultural study of the affective meanings of color. Journal of Cross-Cultural Psychology, 4, 135–156. https://doi.org/10.1177/002202217300400201

American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders (5th ed.). American Psychiatric Publishing.

Amestoy

Guillaud

Bouvard

M. P.

Cazalets

J. R.

(2015). Developmental changes in face visual scanning in autism spectrum disorder as assessed by data-based analysis. Frontiers in Psychology, 6, 989. https://doi.org/10.3389/fpsyg.2015.00989

Annaz

Karmiloff-Smith

Johnson

M. H.

Thomas

M. S.

(2009). A cross-syndrome study of the development of holistic face recognition in children with autism, Down syndrome, and Williams syndrome. Journal of Experimental Child Psychology, 102, 456–486. https://doi.org/10.1016/j.jecp.2008.11.005

Åsberg Johnels

Hovey

Zürcher

Hippolyte

Lemonnier

Gillberg

Hadjikhani

(2017). Autism and emotional face-viewing. Autism Research, 10, 901–910. https://doi.org/10.1002/aur.1730

Baio

Wiggins

Christensen

D. L.

Maenner

M. J.

Daniels

Warren

Kurzius-Spencer

Zahorodny

Rosenberg

C. R.

White

Durkin

M. S.

(2018). Prevalence of autism spectrum disorder among children aged 8 years: Autism and developmental disabilities monitoring network, 11 sites, United States, 2010. MMWR Surveillance Summaries, 67, 1–23. https://doi.org/10.15585%2Fmmwr.ss6706a1

Baron-Cohen

Wheelwright

Skinner

Martin

Clubley

(2001). 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. https://doi.org/10.1023/a:1005653411471

Benitez-Quiroz

C. F.

Srinivasan

Martinez

A. M.

(2018). Facial color is an efficient mechanism to visually transmit emotion. Proceedings of the National Academy of Sciences of the United States of America, 115, 3581–3586. https://doi.org/10.1073/pnas.1716084115

Benitez-Quiroz

C. F.

Srinivasan

Martinez

A. M.

(2019). Discriminant functional learning of color features for the recognition of facial action units and their intensities. IEEE Transactions on Pattern Analysis and Machine Intelligence, 41, 2835–2845. https://doi.org/10.1109/TPAMI.2018.2868952

10.

Bosc

Dubini

Polin

(1997). Development and validation of a social functioning scale, the Social Adaptation Self-evaluation Scale. European Neuropsychopharmacology, 7, S57–S73. https://doi.org/10.1016/s0924-977x(97)00420-3

11.

Chien

S. H.-L.

Wang

L.-H.

Chen

C.-C.

Chen

T.-Y.

Chen

H.-S.

(2014). Autistic children do not exhibit an own-race advantage as compared to typically developing children. Research in Autism Spectrum Disorders, 8, 1544–1551. https://doi.org/10.1016/j.rasd.2014.08.005

12.

Corbett

B. A.

White

Lerner

Preacher

K. J.

Klemencic

M. E.

Simmons

G. L.

Pilkington

Gable

Gioia

Key

A. P.

(2023). Peers, play, and performance to build social salience in autistic youth: A multisite randomized clinical trial. Journal of Consulting and Clinical Psychology, 91, 411–425. https://doi.org/10.1037/ccp0000821

13.

Crespi

Badcock

(2008). Psychosis and autism as diametrical disorders of the social brain. Behavioral and Brain Sciences, 31, 241–261; discussion 261–320. https://doi.org/10.1017/S0140525X08004214

14.

Demetriou

E. A.

Song

C. Y.

Park

S. H.

Pepper

K. L.

Naismith

S. L.

Hermens

D. F.

Hickie

I. B.

Thomas

E. E.

Norton

White

Guastella

A. J.

(2018). Autism, early psychosis, and social anxiety disorder: A transdiagnostic examination of executive function cognitive circuitry and contribution to disability. Translational Psychiatry, 8, 200. https://doi.org/10.1038/s41398-018-0193-8

15.

De Wit

T. C. J.

Falck-Ytter

von Hofsten

(2008). Young children with autism spectrum disorder look differently at positive versus negative emotional faces. Research in Autism Spectrum Disorders, 2, 651–659. https://doi.org/10.1016/j.rasd.2008.01.004

16.

Doernberg

Hollander

(2016). Neurodevelopmental disorders (ASD and ADHD): DSM-5, ICD-10, and ICD-11. CNS Spectrums, 21, 295–299. https://doi.org/10.1017/S1092852916000262

17.

Drummond

P. D.

(1994). The effect of anger and pleasure on facial blood flow. Australian Journal of Psychology, 46, 95–99. https://doi.org/10.1080/00049539408259479

18.

Drummond

P. D.

Quah

S. H.

(2001). The effect of expressing anger on cardiovascular reactivity and facial blood flow in Chinese and Caucasians. Psychophysiology, 38, 190–196. https://doi.org/10.1111/1469-8986.3820190

19.

Tao

Martinez

A M.

(2014). Compound facial expressions of emotion. Proceedings of the National Academy of Sciences. Biological Sciences, 111, E1454–E1462. https://doi.org/10.1073/pnas.1322355111

20.

Elfenbein

H. A.

Ambady

(2002). On the universality and cultural specificity of emotion recognition: A meta-analysis. Psychological Bulletin, 128, 203–235. https://doi.org/10.1037/0033-2909.128.2.203

21.

Frank

Schulze

Hellweg

Koehne

Roepke

(2018). Impaired detection and differentiation of briefly presented facial emotions in adults with high-functioning autism and Asperger syndrome. Behaviour Research and Therapy, 104, 7–13. https://doi.org/10.1016/j.brat.2018.02.005

22.

Goto

Ueda

Yoshimura

Kakihara

Kaji

Yamada

Shinkai

Nakajima

Iwata

Higuchi

Nakamura

(2005). Reliability and validity of Japanese version of Social Adaptation Self-evaluation Scale (SASS). Seishin Igaku [Psychiatry], 47, 483–489. https://doi.org/10.11477/mf.1405100063

23.

Guy

Habak

Wilson

H. R.

Mottron

Bertone

(2017). Face perception develops similarly across viewpoint in children and adolescents with and without autism spectrum disorder. Journal of Vision, 17, 38. https://doi.org/10.1167/17.1.38

24.

Hadad

B. S.

Schwartz

Binur

(2019). Reduced perceptual specialization in autism: Evidence from the other-race face effect. Journal of Experimental Psychology: General, 148, 588–594. https://doi.org/10.1037/xge0000550

25.

Hanley

Riby

D. M.

Derges

M. J.

Douligeri

Philyaw

Ikeda

Monden

Shimoizumi

Yamagata

Hirai

(2020). Does culture shape face perception in autism? Cross-cultural evidence of the own-race advantage from the UK and Japan. Developmental Science, 23, e12942. https://doi.org/10.1111/desc.12942

26.

Harms

M. B.

Martin

Wallace

G. L.

(2010). Facial emotion recognition in autism spectrum disorders: A review of behavioral and neuroimaging studies. Neuropsychology Review, 20, 290–322. https://doi.org/10.1007/s11065-010-9138-6

27.

Hayward

W. G.

Favelle

S. K.

Oxner

Chu

M. H.

Lam

S. M.

(2017). The other-race effect in face learning: Using naturalistic images to investigate face ethnicity effects in a learning paradigm. Quarterly Journal of Experimental Psychology, 70, 890–896. https://doi.org/10.1080/17470218.2016.1146781

28.

Horry

Wright

D. B.

Tredoux

C. G.

(2010). Recognition and context memory for faces from own and other ethnic groups: A remember-know investigation. Memory & Cognition, 38, 134–141. https://doi.org/10.3758/MC.38.2.134

29.

Howard

M. A.

Cowell

P. E.

Boucher

Broks

Mayes

Farrant

Roberts

(2000). Convergent neuroanatomical and behavioural evidence of an amygdala hypothesis of autism. Neuroreport, 11, 2931–2935. https://doi.org/10.1097/00001756-200009110-00020

30.

Howlin

Moss

(2012). Adults with autism spectrum disorders. The Canadian Journal of Psychiatry, 57, 275–283. https://doi.org/10.1177/070674371205700502

31.

Hugenberg

Young

S. G.

Bernstein

M. J.

Sacco

D. F.

(2010). The categorization-individuation model: An integrative account of the other-race recognition deficit. Psychological Review, 117, 1168–1187. https://doi.org/10.1037/a0020463

32.

Hull

Petrides

K. V.

Allison

Smith

Baron-Cohen

Lai

M. C.

Mandy

(2017). “Putting on my best normal": Social camouflaging in adults with autism spectrum conditions. Journal of Autism and Developmental Disorders, 47, 2519–2534. https://doi.org/10.1007/s10803-017-3166-5

33.

Humphreys

Minshew

Leonard

G. L.

Behrmann

(2007). A fine-grained analysis of facial expression processing in high-functioning adults with autism. Neuropsychologia, 45, 685–695. https://doi.org/10.1016/j.neuropsychologia.2006.08.003

34.

Ishihara

(1966). Ishihara's tests for colour-blindness/by Shinobu Ishihara. The series of plates designed as tests for colour-blindness. Isshinkai.

35.

Kinney

A. R.

Middleton

Graham

J. E.

(2021). A Bayesian analysis of non-significant rehabilitation findings: Evaluating the evidence in favour of truly absent treatment effects. Annals of Physical & Rehabilitation Medicine, 64, 101425. https://doi.org/10.1016/j.rehab.2020.07.008

36.

Kleberg

J. L.

Nyström

Bölte

Falck-Ytter

(2019). Sex differences in social attention in infants at risk for autism. Journal of Autism and Developmental Disorders, 49, 1342–1351. https://doi.org/10.1007/s10803-018-3799-z

37.

Kuusikko-Gauffin

Jansson-Verkasalo

Carter

Pollock-Wurman

Jussila

Mattila

M.-L.

Rahko

Ebeling

Pauls

Moilanen

(2011). Face memory and object recognition in children with high-functioning autism or Asperger syndrome and in their parents. Research in Autism Spectrum Disorders, 5, 622–628. https://doi.org/10.1016/j.rasd.2010.07.007

38.

Lahera

Herrera

Fernández

Bardón

De Los Ángeles

Fernández-Liria

(2014). Familiarity and face emotion recognition in patients with schizophrenia. Comprehensive Psychiatry, 55, 199–205. https://doi.org/10.1016/j.comppsych.2013.06.006

39.

Lai

M. C.

Lombardo

M. V.

Baron-Cohen

(2014). Autism. The Lancet, 383, 896–910. https://doi.org/10.1016/S0140-6736(13)61539-1

40.

Latimier

Kovarski

Peyre

Fernandez

L. G.

Gras

Leboyer

Zalla

(2019). Trustworthiness and dominance personality traits’ judgments in adults with autism spectrum disorder. Journal of Autism and Developmental Disorders, 49, 4535–4546. https://doi.org/10.1007/s10803-019-04163-1

41.

Liu

T. L.

Wang

P. W.

Yang

Y. C.

Hsiao

R. C.

Y. Y.

Shyi

G. C.

Yen

C. F.

(2019). Deficits in facial emotion recognition and implicit attitudes toward emotion among adolescents with high functioning autism spectrum disorder. Comprehensive Psychiatry, 90, 7–13. https://doi.org/10.1016/j.comppsych.2018.12.010

42.

Livingston

L. A.

Shah

Milner

Happé

(2020). Quantifying compensatory strategies in adults with and without diagnosed autism. Molecular Autism, 11, 15. https://doi.org/10.1186/s13229-019-0308-y

43.

Lord

Elsabbagh

Baird

Veenstra-Vanderweele

(2018). Autism spectrum disorder. The Lancet, 392, 508–520. https://doi.org/10.1016/S0140-6736(18)31129-2

44.

Lord

Jones

R. M.

(2012). Annual research review: Re-thinking the classification of autism spectrum disorders. Journal of Child Psychology and Psychiatry, 53, 490–509. https://doi.org/10.1111/j.1469-7610.2012.02547.x

45.

Mazefsky

C. A.

White

S. W.

(2014). Emotion regulation: Concepts & practice in autism spectrum disorder. Child & Adolescent Psychiatric Clinics of North America, 23, 15–24. https://doi.org/10.1016/j.chc.2013.07.002

46.

Montagne

Kessels

R. P.

De Haan

E. H.

Perrett

D. I.

(2007). The emotion recognition task: A paradigm to measure the perception of facial emotional expressions at different intensities. Perceptual and Motor Skills, 104, 589–598. https://doi.org/10.2466/pms.104.2.589-598

47.

Montoya

Campos

J. J.

Schandry

(2005). See red? Turn pale? Unveiling emotions through cardiovascular and hemodynamic changes. The Spanish Journal of Psychology, 8, 79–85. https://doi.org/10.1017/s1138741600004984

48.

Nakajima

Minami

Nakauchi

(2017). Interaction between facial expression and color. Scientific Reports, 7, 41019. https://doi.org/10.1038/srep41019

49.

Peromaa

Olkkonen

(2019). Red color facilitates the detection of facial anger—But how much? PLoS One, 14, e0215610. https://doi.org/10.1371/journal.pone.0215610

50.

Prins

Kingdom

F. A. A.

(2018). Applying the model-comparison approach to test specific research hypotheses in psychophysical research using the Palamedes toolbox. Frontiers in Psychology, 9, 1250. https://doi.org/10.3389/fpsyg.2018.01250

51.

Psychlops Wiki. (2023). Psychlops Wiki—Front page (http://psychlops.osdn.jp/ja/) (accessed 11 April, 2023)

52.

The Psychological Corporation. (1997). WAIS-III and WMS-III technical manual. The Psychological Corporation.

53.

R Core Team. (2022). R: A language and environment for statistical computing. R Foundation for Statistical Computing. Retrieved April 11, 2023, from https://www.R-project.org/

54.

Sachse

Schlitt

Hainz

Ciaramidaro

Walter

Poustka

Bölte

Freitag

C. M.

(2014). Facial emotion recognition in paranoid schizophrenia and autism spectrum disorder. Schizophrenia Research, 159, 509–514. https://doi.org/10.1016/j.schres.2014.08.030

55.

Schulte-Ruther

Greimel

Piefke

Kamp-Becker

Remschmidt

Fink

G. R.

Herpertz-Dahlmann

Konrad

(2014). Age-dependent changes in the neural substrates of empathy in autism spectrum disorder. Social Cognitive and Affective Neuroscience, 9, 1118–1126. https://doi.org/10.1093/scan/nst088

56.

Shah

Bird

Cook

(2016). Face processing in autism: Reduced integration of cross-feature dynamics. Cortex, 75, 113–119. https://doi.org/10.1016/j.cortex.2015.11.019

57.

Shanok

N. A.

Jones

N. A.

Lucas

N. N.

(2019). The nature of facial emotion recognition impairments in children on the autism Spectrum. Child Psychiatry & Human Development, 50, 661–667. https://doi.org/10.1007/s10578-019-00870-z

58.

Snow

Ingeholm

J. E.

Levy

I. F.

Caravella

R. A.

Case

L. K.

Wallace

G. L.

Martin

(2011). Impaired visual scanning and memory for faces in high-functioning autism spectrum disorders: It's not just the eyes. Journal of the International Neuropsychological Society, 17, 1021–1029. https://doi.org/10.1017/S1355617711000981

59.

Song

Hakoda

(2018). Selective impairment of basic emotion recognition in people with autism: Discrimination thresholds for recognition of facial expressions of varying intensities. Journal of Autism and Developmental Disorders, 48, 1886–1894. https://doi.org/10.1007/s10803-017-3428-2

60.

Stephen

I. D.

Law Smith

M. J.

Stirrat

M. R.

Perrett

D. I.

(2009). Facial skin coloration affects perceived health of human faces. International Journal of Primatology, 30, 845–857. https://doi.org/10.1007/s10764-009-9380-z

61.

Stephen

I. D.

Oldham

F. H.

Perrett

D. I.

Barton

R. A.

(2012). Redness enhances perceived aggression, dominance and attractiveness in men’s faces. Evolutionary Psychology, 10, 562–572. https://doi.org/10.1177/147470491201000312

62.

Tan

K. W.

Stephen

I. D.

(2013). Colour detection thresholds in faces and colour patches. Perception, 42, 733–741. https://doi.org/10.1068/p7499

63.

Thorstenson

C. A.

Pazda

A. D.

Elliot

A. J.

(2020). Social perception of facial color appearance for human trichromatic versus dichromatic color vision. Personality and Social Psychology Bulletin, 46, 51–63. https://doi.org/10.1177/0146167219841641

64.

Thorstenson

C. A.

Pazda

A. D.

Lichtenfeld

(2020). Facial blushing influences perceived embarrassment and related social functional evaluations. Cognition & Emotion, 34, 413–426. https://doi.org/10.1080/02699931.2019.1634004

65.

Thorstenson

C. A.

Pazda

A. D.

Yong

S. G.

Elliot

A. J.

(2019). Face color facilitates the disambiguation of confusing emotion expressions: Toward a social functional account of face color in emotion communication. Emotion, 19, 799–807. https://doi.org/10.1037/emo0000485

66.

Tsang

(2018). Eye-tracking study on facial emotion recognition tasks in individuals with high-functioning autism spectrum disorders. Autism: The International Journal of Research and Practice, 22, 161–170. https://doi.org/10.1177/1362361316667830

67.

Uljarevic

Hamilton

(2013). Recognition of emotions in autism: A formal meta-analysis. Journal of Autism and Developmental Disorders, 43, 1517–1526. https://doi.org/10.1007/s10803-012-1695-5

68.

Wakabayashi

Tojo

Baron-Cohen

Wheelwright

(2004). The autism-spectrum quotient (AQ) Japanese wheelwright version: Evidence from high-functioning clinical group and normal adults. Shinrigaku Kenkyu [The Japanese Journal of Psychology], 75, 78–84. https://doi.org/10.4992/jjpsy.75.78

69.

Wakui

Thoma

De Fockert

J. W.

(2016). View-sensitive ERP repetition effects indicate automatic holistic processing of spatially unattended objects. Neuropsychologia, 89, 426–436. https://doi.org/10.1016/j.neuropsychologia.2016.07.024

70.

Wallace

G. L.

Case

L. K.

Harms

M. B.

Silvers

J. A.

Kenworthy

Martin

(2011). 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, 41, 1475–1486. https://doi.org/10.1007/s10803-010-1170-0

71.

Wallace

Coleman

Bailey

(2008). An investigation of basic facial expression recognition in autism spectrum disorders. Cognition and Emotion, 22, 1353–1380. https://doi.org/10.1080/02699930701782153

72.

Walsh

J. A.

Creighton

S. E.

Rutherford

M. D.

(2016). Emotion perception or social cognitive complexity: What drives face processing deficits in autism spectrum disorder? Journal of Autism and Developmental Disorders, 46, 615–623. https://doi.org/10.1007/s10803-015-2606-3

73.

Whitaker

Jones

C. R. G.

Wilkins

A. J.

Roberson

(2016). Judging the intensity of emotional expression in faces: The effects of colored tints on individuals with autism spectrum disorder. Autism Research, 9, 450–459. https://doi.org/10.1002/aur.1506

74.

Wieckowski

A. T.

White

S. W.

(2017). Eye-gaze analysis of facial emotion recognition and expression in adolescents with ASD. Journal of Clinical Child & Adolescent Psychology, 46, 110–124. https://doi.org/10.1080/15374416.2016.1204924

75.

Williams

D. L.

Goldstein

Minshew

N. J.

(2005). Impaired memory for faces and social scenes in autism: Clinical implications of memory dysfunction. Archives of Clinical Neuropsychology, 20, 1–15. https://doi.org/10.1016/j.acn.2002.08.001

76.

Wilson

C. E.

Palermo

Burton

A. M.

Brock

(2011). Recognition of own- and other-race faces in autism spectrum disorders. Quarterly Journal of Experimental Psychology, 64, 1939–1954. https://doi.org/10.1080/17470218.2011.603052

77.

World Health Organization. (2018). ICD-11 for mortality and morbidity statistics. Retrieved April 11, 2023, from https://icd.who.int/browse11/l-m/en

78.

Yamada

Yokoyama

Matsumura

Mitani

Kaneko

Nakagome

(2012). Fish consumption is positively associated with social functioning: A cross-sectional study in male Japanese workers. Psychiatry Research, 200, 1038–1040. https://doi.org/10.1016/j.psychres.2012.04.023

79.

Yeung

M. K.

Lee

T. L.

Chan

A. S.

(2020). Impaired recognition of negative facial expressions is partly related to facial perception deficits in adolescents with high-functioning autism spectrum disorder. Journal of Autism and Developmental Disorders, 50, 1596–1606. https://doi.org/10.1007/s10803-019-03915-3

80.

Quinn

P. C.

Fan

Huang

Lee

Pascalis

(2016). Children with autism spectrum disorder scan own-race faces differently from other-race faces. Journal of Experimental Child Psychology, 141, 177–186. https://doi.org/10.1016/j.jecp.2015.09.011