Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.
ADVANCED SEARCH
Log in
Top
Journal of Neurodevelopmental Disorders
Published in: Journal of Neurodevelopmental Disorders 1/2012

Open Access 01-12-2012 | Research

Abnormal social reward processing in autism as indexed by pupillary responses to happy faces

Authors: Leigh Sepeta, Naotsugu Tsuchiya, Mari S Davies, Marian Sigman, Susan Y Bookheimer, Mirella Dapretto

Published in: Journal of Neurodevelopmental Disorders | Issue 1/2012

Login to get access

Abstract

Background

Individuals with Autism Spectrum Disorders (ASD) typically show impaired eye contact during social interactions. From a young age, they look less at faces than typically developing (TD) children and tend to avoid direct gaze. However, the reason for this behavior remains controversial; ASD children might avoid eye contact because they perceive the eyes as aversive or because they do not find social engagement through mutual gaze rewarding.

Methods

We monitored pupillary diameter as a measure of autonomic response in children with ASD (n = 20, mean age = 12.4) and TD controls (n = 18, mean age = 13.7) while they looked at faces displaying different emotions. Each face displayed happy, fearful, angry or neutral emotions with the gaze either directed to or averted from the subjects.

Results

Overall, children with ASD and TD controls showed similar pupillary responses; however, they differed significantly in their sensitivity to gaze direction for happy faces. Specifically, pupillary diameter increased among TD children when viewing happy faces with direct gaze as compared to those with averted gaze, whereas children with ASD did not show such sensitivity to gaze direction. We found no group differences in fixation that could explain the differential pupillary responses. There was no effect of gaze direction on pupil diameter for negative affect or neutral faces among either the TD or ASD group.

Conclusions

We interpret the increased pupillary diameter to happy faces with direct gaze in TD children to reflect the intrinsic reward value of a smiling face looking directly at an individual. The lack of this effect in children with ASD is consistent with the hypothesis that individuals with ASD may have reduced sensitivity to the reward value of social stimuli.
Appendix
Available only for authorised users
Literature
1.
Association AP: Diagnostic and statistical manual of mental disorders. 1994, Washington: Author, 4
2.
Osterling J, Dawson G: Early recognition of children with autism: a study of first birthday home videotapes. J Autism Dev Disord. 1994, 24: 247-257. 10.1007/BF02172225.CrossRefPubMed
3.
Langdell T: Recognition of faces: an approach to the study of autism. J Child Psychol Psychiat. 1977, 19: 255-268.CrossRef
4.
Schultz RT, Gauthier I, Klin A, Fulbright RK, Anderson AW, Volkmar F, Skudlarski P, Lacadie C, Cohen DJ, Gore JC: Abnormal ventral temporal cortical activity during face discrimination among individuals with autism and Asperger syndrome. Arch Gen Psychiatry. 2000, 57: 331-340. 10.1001/archpsyc.57.4.331.CrossRefPubMed
5.
Weeks SJ, Hobson RP: The salience of facial expression for autistic children. J Child Psychol Psychiatry. 1987, 28: 137-151. 10.1111/j.1469-7610.1987.tb00658.x.CrossRefPubMed
6.
Dalton KM, Nacewicz BM, Johnstone T, Schaefer HS, Gernsbacher MA, Goldsmith HH, Alexander AL, Davidson RJ: Gaze fixation and the neural circuitry of face processing in autism. Nat Neurosci. 2005, 8: 519-526.PubMedCentralPubMed
7.
Klin A, Jones W, Schultz R, Volkmar F, Cohen D: Visual fixation patterns during viewing of naturalistic social situations as predictors of social competence in individuals with autism. Arch Gen Psychiatry. 2002, 59: 809-816. 10.1001/archpsyc.59.9.809.CrossRefPubMed
8.
Neumann D, Spezio ML, Piven J, Adolphs R: Looking you in the mouth: abnormal gaze in autism resulting from impaired top-down modulation of visual attention. Scan. 2006, 1: 194-202.PubMedCentralPubMed
9.
Pelphrey KA, Sasson NJ, Reznick JS, Paul G, Goldman BD, Piven J: Visual scanning of faces in autism. J Autism Dev Disord. 2002, 32: 249-261. 10.1023/A:1016374617369.CrossRefPubMed
10.
Spezio ML, Adolphs R, Hurley RS, Piven J: Analysis of face gaze in autism using “Bubbles”. Neuropsychologia. 2007, 45: 144-151. 10.1016/j.neuropsychologia.2006.04.027.CrossRefPubMed
11.
Kylliainen A, Hietanen JK: Skin conductance responses to another person’s gaze in children with autism. J Autism Dev Disord. 2006, 36: 517-525. 10.1007/s10803-006-0091-4.CrossRefPubMed
12.
Dawson G, Carver L, Meltzoff AN, Panagiotides H, McPartland J, Webb SJ: Neural correlates of face and object recognition in young children with autism spectrum disorder, developmental delay, and typical development. Child Dev. 2002, 73: 700-717. 10.1111/1467-8624.00433.PubMedCentralCrossRefPubMed
13.
Dawson G, Webb SJ, McPartland J: Understanding the nature of face processing impairment in autism: insights from behavioral and electrophysiological studies. Dev Neuropsychol. 2005, 27: 403-424. 10.1207/s15326942dn2703_6.CrossRefPubMed
14.
Phillips ML, Bullmore ET, Howard R, Woodruff PW, Wright IC, Williams SC, Simmons A, Andrew C, Brammer M, David AS: Investigation of facial recognition memory and happy and sad facial expression perception: an fMRI study. Psychiatry Res. 1998, 83: 127-138. 10.1016/S0925-4927(98)00036-5.CrossRefPubMed
15.
O’Doherty J, Winston J, Critchley H, Perrett D, Burt DM, Dolan RJ: Beauty in a smile: the role of medial orbitofrontal cortex in facial attractiveness. Neuropsychologia. 2003, 41: 147-155. 10.1016/S0028-3932(02)00145-8.CrossRefPubMed
16.
Kampe KK, Frith CD, Dolan RJ, Frith U: Reward value of attractiveness and gaze. Nature. 2001, 413: 589-10.1038/35098149.CrossRefPubMed
17.
Beatty J: Task-evoked pupillary responses, processing load, and the structure of processing resources. Psychol Bull. 1982, 91: 276-292.CrossRefPubMed
18.
Hess EH, Polt JM: Pupil size as related to interest value of visual stimuli. Science. 1960, 132: 349-350. 10.1126/science.132.3423.349.CrossRefPubMed
19.
Steinhauer SR, Hakerem G: The pupillary response in cognitive psychophysiology and Schizophrenia. 1992, New York: NY Academy of Science Press
20.
Bradley MM, Miccoli L, Escrig MA, Lang PJ: The pupil as a measure of emotional arousal and autonomic activation. Psychophysiology. 2008, 45: 602-607. 10.1111/j.1469-8986.2008.00654.x.PubMedCentralCrossRefPubMed
21.
O’Doherty JP, Buchanan TW, Seymour B, Dolan RJ: Predictive neural coding of reward preference involves dissociable responses in human ventral midbrain and ventral striatum. Neuron. 2006, 49: 157-166. 10.1016/j.neuron.2005.11.014.CrossRefPubMed
22.
Steinhauer SR, Boller F, Zubin J, Pearlman S: Pupillary dilation to emotional visual stimuli revisited. Psychophysiology. 1983, 20: 472-
23.
Silk JS, Dahl RE, Ryan ND, Forbes EE, Axelson DA, Birmaher B, Siegle GJ: Pupillary reactivity to emotional information in child and adolescent depression: links to clinical and ecological measures. Am J Psychiatry. 2007, 164: 1873-1880. 10.1176/appi.ajp.2007.06111816.PubMedCentralCrossRefPubMed
24.
Silk JS, Stroud LR, Siegle GJ, Dahl RE, Lee KH, Nelson EE: Peer acceptance and rejection through the eyes of youth: pupillary, eyetracking and ecological data from the Chatroom Interact task. Soc Cogn Affect Neurosci. 2012, 7: 93-105. 10.1093/scan/nsr044.PubMedCentralCrossRefPubMed
25.
Hess EH, Seltzer AL, Shlien JM: Pupil response of hetero- and homosexual males to pictures of men and women: a pilot study. J Abnorm Psychol. 1965, 70: 165-168.CrossRefPubMed
26.
Garrett JC, Harrison DW, Kelly PL: Pupillometric assessment of arousal to sexual stimuli: novelty effects or preference?. Arch Sex Behav. 1989, 18: 191-201. 10.1007/BF01543194.CrossRefPubMed
27.
Dabbs JM: Testosterone and pupillary response to auditory sexual stimuli. Physiol Behav. 1997, 62: 909-912. 10.1016/S0031-9384(97)00268-0.CrossRefPubMed
28.
Bijleveld E, Custers R, Aarts H: The unconscious eye opener: pupil dilation reveals strategic recruitment of resources upon presentation of subliminal reward cues. Psychol Sci. 2009, 20: 1313-1315. 10.1111/j.1467-9280.2009.02443.x.CrossRefPubMed
29.
Chae Y, Lee JC, Park KM, Kang OS, Park HJ, Lee H: Subjective and autonomic responses to smoking-related visual cues. J Physiol Sci. 2008, 58: 139-145. 10.2170/physiolsci.RP014207.CrossRefPubMed
30.
Wang Z, Faith M, Patterson F, Tang K, Kerrin K, Wileyto EP, Detre JA, Lerman C: Neural substrates of abstinence-induced cigarette cravings in chronic smokers. J Neurosci. 2007, 27: 14035-14040. 10.1523/JNEUROSCI.2966-07.2007.PubMedCentralCrossRefPubMed
31.
Satterthwaite TD, Green L, Myerson J, Parker J, Ramaratnam M, Buckner RL: Dissociable but inter-related systems of cognitive control and reward during decision making: evidence from pupillometry and event-related fMRI. NeuroImage. 2007, 37: 1017-1031. 10.1016/j.neuroimage.2007.04.066.CrossRefPubMed
32.
Anderson CJ, Colombo J, Jill Shaddy D: Visual scanning and pupillary responses in young children with Autism Spectrum Disorder. J Clin Exp Neuropsychol. 2006, 28: 1238-1256. 10.1080/13803390500376790.CrossRefPubMed
33.
Falck-Ytter T: Face inversion effects in autism: a combined looking time and pupillometric study. Autism Res. 2008, 1: 297-306. 10.1002/aur.45.CrossRefPubMed
34.
Senju A, Csibra G: Gaze following in human infants depends on communicative signals. Curr Biol. 2008, 18: 668-671. 10.1016/j.cub.2008.03.059.CrossRefPubMed
35.
George N, Driver J, Dolan RJ: Seen gaze-direction modulates fusiform activity and its coupling with other brain areas during face processing. NeuroImage. 2001, 13: 1102-1112.CrossRefPubMed
36.
Davies MS, Dapretto M, Sigman M, Sepeta L, Bookheimer S: Neural bases of gaze and emotion processing in children with autism. Brain and Behav. 2011, 1: 1-11.CrossRef
37.
Lord C, Risi S, Lambrecht L, Cook EH, Leventhal BL, DiLavore PC, Pickles A, Rutter M: The autism diagnostic observation schedule-generic: a standard measure of social and communication deficits associated with the spectrum of autism. J Autism Dev Disord. 2000, 30: 205-223. 10.1023/A:1005592401947.CrossRefPubMed
38.
Lord C, Rutter M, Le Couteur A: Autism diagnostic interview-revised: a revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. J Autism Dev Disord. 1994, 24: 659-685. 10.1007/BF02172145.CrossRefPubMed
39.
Tottenham N, Tanaka J, Leon AC, McCarry T, Nurse M, Hare TA, Marcus DJ, Westerlund A, Casey BJ, Nelson CA: The NimStim set of facial expressions: judgments from untrained research participants. Psychiatry Res. in press
40.
Wang AT, Dapretto M, Hariri AR, Sigman M, Bookheimer SY: Neural correlates of facial affect processing in children and adolescents with autism spectrum disorder. J Am Acad Child Adolesc Psychiatry. 2004, 43: 481-490. 10.1097/00004583-200404000-00015.CrossRefPubMed
41.
Efron B, Tibshirani RJ: An Introduction to the Bootstrap. 1998, Boca Raton: CRC Press, 1
42.
Barbur JL: Learning from the pupil - studies of basic mechanisms and clinical applications. 2004, Cambridge: MIT Press
43.
O’Doherty JP, Dayan P, Friston K, Critchley H, Dolan RJ: Temporal difference models and reward-related learning in the human brain. Neuron. 2003, 38: 329-337. 10.1016/S0896-6273(03)00169-7.CrossRefPubMed
44.
Scott-Van Zeeland AA, Dapretto M, Ghahremani DG, Poldrack RA, Bookheimer SY: Reward processing in autism. Autism Res. 2010, 3: 53-67.PubMedCentralPubMed
45.
Joseph RM, Ehrman K, McNally R, Keehn B: Affective response to eye contact and face recognition ability in children with ASD. J Int Neuropsychol Soc. 2008, 14: 947-955. 10.1017/S1355617708081344.CrossRefPubMed
46.
Farzin F, Rivera SM, Hessl D: Brief report: Visual processing of faces in individuals with fragile X syndrome: an eye tracking study. J Autism Dev Disord. 2009, 39: 946-952. 10.1007/s10803-009-0744-1.PubMedCentralCrossRefPubMed
47.
Lee BT, Seok JH, Lee BC, Cho SW, Yoon BJ, Lee KU, Chae JH, Choi IG, Ham BJ: Neural correlates of affective processing in response to sad and angry facial stimuli in patients with major depressive disorder. Prog Neuropsychopharmacol Biol Psychiatry. 2008, 32: 778-785. 10.1016/j.pnpbp.2007.12.009.CrossRefPubMed
48.
Thomas KM, Drevets WC, Whalen PJ, Eccard CH, Dahl RE, Ryan ND, Casey BJ: Amygdala response to facial expressions in children and adults. Biol Psychiatry. 2001, 49: 309-316. 10.1016/S0006-3223(00)01066-0.CrossRefPubMed
49.
Dayan P, Yu AJ: Phasic norepinephrine: a neural interrupt signal for unexpected events. Network. 2006, 17: 335-350. 10.1080/09548980601004024.CrossRefPubMed
50.
Bouret S, Sara SJ: Reward expectation, orientation of attention and locus coeruleus-medial frontal cortex interplay during learning. Eur J Neurosci. 2004, 20: 791-802. 10.1111/j.1460-9568.2004.03526.x.CrossRefPubMed
51.
Gredeback G, Melinder A: Infants’ understanding of everyday social interactions: a dual process account. Cognition. 2010, 114: 197-206. 10.1016/j.cognition.2009.09.004.CrossRefPubMed
52.
van der Gaag C, Minderaa RB, Keysers C: The BOLD signal in the amygdala does not differentiate between dynamic facial expressions. Soc Cogn Affect Neurosci. 2007, 2: 93-103. 10.1093/scan/nsm002.PubMedCentralCrossRefPubMed
53.
Kesler-West ML, Andersen AH, Smith CD, Avison MJ, Davis CE, Kryscio RJ, Blonder LX: Neural substrates of facial emotion processing using fMRI. Brain Res Cogn Brain Res. 2001, 11: 213-226. 10.1016/S0926-6410(00)00073-2.CrossRefPubMed
Metadata
Title
Abnormal social reward processing in autism as indexed by pupillary responses to happy faces
Authors
Leigh Sepeta
Naotsugu Tsuchiya
Mari S Davies
Marian Sigman
Susan Y Bookheimer
Mirella Dapretto
Publication date
01-12-2012
Publisher
BioMed Central
Published in
Journal of Neurodevelopmental Disorders / Issue 1/2012
Print ISSN: 1866-1947
Electronic ISSN: 1866-1955
DOI
https://doi.org/10.1186/1866-1955-4-17

Other articles of this Issue 1/2012

Journal of Neurodevelopmental Disorders 1/2012 Go to the issue

Research

Reduced social preferences in autism: evidence from charitable donations

Research

Fragile X syndrome: a pilot proton magnetic resonance spectroscopy study in premutation carriers

Editorial

Journal of Neurodevelopmental Disorders is now a fully open access journal

Research

Adolescents with prenatal cocaine exposure show subtle alterations in striatal surface morphology and frontal cortical volumes

Research

Long-term alterations of striatal parvalbumin interneurons in a rat model of early exposure to alcohol

Research

Impaired multiple object tracking in children with chromosome 22q11.2 deletion syndrome