| Journal of Neurodevelopmental Disorders | |
| Abnormal social reward processing in autism as indexed by pupillary responses to happy faces | |
| Mirella Dapretto2  Susan Y Bookheimer2  Marian Sigman2  Mari S Davies1  Naotsugu Tsuchiya3  Leigh Sepeta4  | |
| [1] Department of Neurology, Child and Adolescent Assessment Division, Sports Concussion Institute Health Services Research group, University of California Los Angeles, Los Angeles, CA, 90095, USA;Department of Psychiatry and Biobehavioral Sciences, David Geffen School of Medicine, University of California Los Angeles, Los Angeles, CA, 90095, USA;Japan Science and Technology Agency, Tokyo, Japan;Children’s National Medical Center, Washington, DC, 20010, USA | |
| 关键词: Reward processing; Pupillary response; Autism; | |
| Others : 811815 DOI : 10.1186/1866-1955-4-17 |
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| received in 2012-02-03, accepted in 2012-06-07, 发布年份 2012 | |
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【 摘 要 】
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.
【 授权许可】
2012 Sepeta et al.; licensee BioMed Central Ltd.
【 预 览 】
| Files | Size | Format | View |
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| 20140709072853995.pdf | 969KB | ||
| Figure 3. | 9KB | Image | |
| Figure 2. | 45KB | Image | |
| Figure 1. | 37KB | Image |
【 图 表 】
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【 参考文献 】
- [1]Association AP: Diagnostic and statistical manual of mental disorders. 4th edition. Washington: Author; 1994.
- [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.
- [3]Langdell T: Recognition of faces: an approach to the study of autism. J Child Psychol Psychiat 1977, 19:255-268.
- [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.
- [5]Weeks SJ, Hobson RP: The salience of facial expression for autistic children. J Child Psychol Psychiatry 1987, 28:137-151.
- [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.
- [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.
- [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.
- [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]Spezio ML, Adolphs R, Hurley RS, Piven J: Analysis of face gaze in autism using “Bubbles”. Neuropsychologia 2007, 45:144-151.
- [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.
- [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.
- [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.
- [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.
- [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.
- [16]Kampe KK, Frith CD, Dolan RJ, Frith U: Reward value of attractiveness and gaze. Nature 2001, 413:589.
- [17]Beatty J: Task-evoked pupillary responses, processing load, and the structure of processing resources. Psychol Bull 1982, 91:276-292.
- [18]Hess EH, Polt JM: Pupil size as related to interest value of visual stimuli. Science 1960, 132:349-350.
- [19]Steinhauer SR, Hakerem G: The pupillary response in cognitive psychophysiology and Schizophrenia. New York: NY Academy of Science Press; 1992.
- [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.
- [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.
- [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.
- [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.
- [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.
- [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.
- [27]Dabbs JM Jr: Testosterone and pupillary response to auditory sexual stimuli. Physiol Behav 1997, 62:909-912.
- [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.
- [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.
- [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.
- [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.
- [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.
- [33]Falck-Ytter T: Face inversion effects in autism: a combined looking time and pupillometric study. Autism Res 2008, 1:297-306.
- [34]Senju A, Csibra G: Gaze following in human infants depends on communicative signals. Curr Biol 2008, 18:668-671.
- [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.
- [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.
- [37]Lord C, Risi S, Lambrecht L, Cook EH Jr, 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.
- [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.
- [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 Resin 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.
- [41]Efron B, Tibshirani RJ: An Introduction to the Bootstrap. 1st edition. Boca Raton: CRC Press; 1998.
- [42]Barbur JL: Learning from the pupil - studies of basic mechanisms and clinical applications. Cambridge: MIT Press; 2004.
- [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.
- [44]Scott-Van Zeeland AA, Dapretto M, Ghahremani DG, Poldrack RA, Bookheimer SY: Reward processing in autism. Autism Res 2010, 3:53-67.
- [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.
- [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.
- [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.
- [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.
- [49]Dayan P, Yu AJ: Phasic norepinephrine: a neural interrupt signal for unexpected events. Network 2006, 17:335-350.
- [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.
- [51]Gredeback G, Melinder A: Infants’ understanding of everyday social interactions: a dual process account. Cognition 2010, 114:197-206.
- [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.
- [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.
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