Joint attention – the ability to coordinate attention with a social partner – is critical for social communication, learning and the regulation of interpersonal relationships. Infants and young children with autism demonstrate impairments in both initiating and responding to joint attention bids in naturalistic settings. However, little is known about joint attention abilities in adults with autism. Here, we tested 17 autistic adults and 17 age- and nonverbal intelligence quotient–matched controls using an interactive eye-tracking paradigm in which participants initiated and responded to joint attention bids with an on-screen avatar. Compared to control participants, autistic adults completed fewer trials successfully. They were also slower to respond to joint attention bids in the first block of testing but performed as well as controls in the second block. There were no group differences in responding to spatial cues on a non-social task with similar attention and oculomotor demands. These experimental results were mirrored in the subjective reports given by participants, with some commenting that they initially found it challenging to communicate using eye gaze, but were able to develop strategies that allowed them to achieve joint attention. Our study indicates that for many autistic individuals, subtle difficulties using eye-gaze information persist well into adulthood.
AdamsonLBBakemanRDecknerDFet al. (2009) Joint engagement and the emergence of language in children with autism and Down syndrome. Journal of Autism and Developmental Disorders39(1): 84–96.
2.
American Psychiatric Association (2000) Diagnostic and Statistical Manual of Mental Disorders. 4th ed.Washington, DC: American Psychiatric Association.
3.
American Psychiatric Association (2013) Diagnostic and Statistical Manual of Mental Disorders. 5th ed.Washington, DC: American Psychiatric Association.
4.
BakemanRAdamsonLB (1984) Coordinating attention to people and objects in mother-infant and peer-infant interactions. Child Development55(4): 1278–1289.
5.
Baron-CohenS (1995) Mindblindness. Cambridge, MA: MIT Press.
6.
Baron-CohenS (2008) Autism, hypersystemizing, and truth. Quarterly Journal of Experimental Psychology61(1): 64–75.
7.
BatesEBenigniLBrethertonIet al. (1979) The Emergence of Symbols: Cognition and Communication in Infancy. New York: Academic Press.
8.
BaylissAPMurphyENaughtinCKet al. (2013) Gaze leading: initiating simulated joint attention influences eye movements and choice behavior. Journal of Experimental Psychology: General142(1): 76–92. Available at: http://doi.org/10.1037/a0029286
9.
BöcklerATimmermansBSebanzNet al. (2014) Effects of observing eye contact on gaze following in high-functioning autism. Journal of Autism and Developmental Disorders44(7): 1651–1658.
10.
BrockJ (2011) Commentary: complementary approaches to the developmental cognitive neuroscience of autism – reflections on Pelphrey et al. (2011). Journal of Child Psychology and Psychiatry52(6): 645–646.
11.
BruinsmaYKoegelRLKoegelLK (2004) Joint attention and children with autism: a review of the literature. Mental Retardation and Developmental Disabilities Research Reviews10(3): 169–175.
12.
CaruanaNBrockJWoolgarA (2015) A frontotemporoparietal network common to initiating and responding to joint attention bids. Neuroimage108: 34–46.
13.
CaruanaNMcArthurGWoolgar (2016) Detecting communicative intent in a computerised test of joint attention. PeerJ Preprints4: e2410v1. Available at: https://doi.org/10.7287/peerj.preprints.2410v1
14.
CaryMS (1978) The role of gaze in the initiation of conversation. Social Psychology41(3): 269–271.
15.
CharmanT (2003) Why is joint attention a pivotal skill in autism?Philosophical Transactions of the Royal Society of London Series B: Biological Sciences358: 315–324.
16.
CharmanTSwettenhamJBaron-CohenSet al. (1997) Infants with autism: an investigation of empathy, pretend play, joint attention, and imitation. Developmental Psychology33(5): 781–789.
17.
ChevallierCKohlsGTroianiVet al. (2012) The social motivation theory of autism. Trends in Cognitive Sciences16: 231–239.
18.
CourgeonMRautureauGMartinJ-Cet al. (2014) Joint attention simulation using eye-tracking and virtual humans. IEEE Transactions on Affective Computing5(3): 238–250.
19.
DawsonGTothKAbbottRet al. (2004) Early social attention impairments in autism: social orienting, joint attention, and attention to distress. Developmental Psychology40(2): 271–283.
20.
DidehbaniNAllenTKandalaftMet al. (2016) Virtual reality social cognition training for children with high functioning autism. Computers in Human Behavior62: 703–711. Available at: http://dx.doi.org/10.1016/j.chb.2016.04.033
21.
EmeryNJ (2000) The eyes have it: the neuroethology, function and evolution of social gaze. Neuroscience and Biobehavioral Reviews24(6): 581–604.
22.
FriesenCKingstoneA (1998) The eyes have it! Reflexive orienting is triggered by nonpredictive gaze. Psychonomic Bulletin & Review5(3): 490–495.
23.
HobsonJHobsonP (2007) Identification: the missing link between joint attention and imitation?Development and Psychopathology19(02): 411–431.
KimKMundyP (2012) Joint attention, social-cognition, and recognition memory in adults. Frontiers in Human Neuroscience6. Available at: http://doi.org/10.3389/fnhum.2012.00172
26.
KuusikkoSPollock-WurmanRJussilaKet al. (2008) Social anxiety in high-functioning children and adolescents with autism and Asperger syndrome. Journal of Autism and Developmental Disorders38: 1697–1709.
27.
LawrenceMA (2013) ez: easy analysis and visualization of factorial experiments. R package version 4.2–2. Available at: http://CRAN.R-project.org/package=ez
28.
LeekamS (2015) Social cognitive impairment and autism: what are we trying to explain?Philosophical Transactions of the Royal Society of London Series B: Biological Sciences371(1686): 20150082.
29.
LordCRisiSLambrechtLet al. (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 Disorders30(3): 205–223.
30.
LovelandKALandrySH (1986) Joint attention and language in autism and developmental language delay. Journal of Autism and Developmental Disorders16(3): 335–349.
31.
MundyPSigmanMKasariC (1990) A longitudinal study of joint attention and language development in autistic children. Journal of Autism and Developmental Disorders20(1): 115–128.
32.
MundyPSigmanMKasariC (1994) Joint attention, developmental level, and symptom presentation in autism. Development and Psychopathology6(03): 389–401.
33.
MundyPSigmanMUngererJet al. (1986) Defining the social deficits of autism: the contribution of non-verbal communication measures. Journal of Child Psychology and Psychiatry27(5): 657–669.
34.
MurrayDSCreagheadNAManning-CourtneyPet al. (2008) The relationship between joint attention and language in children with autism spectrum disorders. Focus on Autism and Other Developmental Disabilities23(1): 5–14.
35.
NationKPennyS (2008) Sensitivity to eye gaze in autism: is it normal? Is it automatic? Is it social?Development and Psychopathology20(1): 79–97.
36.
OsterlingJDawsonG (1994) Early recognition of children with autism: a study of first birthday home videotapes. Journal of Autism and Developmental Disorders24(3): 247–257.
37.
OsterlingJDawsonGMunsonJA (2002) Early recognition of 1-year-old infants with autism spectrum disorder versus mental retardation. Development and Psychopathology14(2): 239–251.
38.
PelphreyKAShultzSHudacCMet al. (2011) Research review: constraining heterogeneity: the social brain and its development in autism spectrum disorder. Journal of Child Psychology and Psychiatry52(6): 631–644.
39.
PfeifferUJVogeleyKSchilbachL (2013) From gaze cueing to dual eyetracking: novel approaches to investigate the neural correlates of gaze in social interaction. Neuroscience and Biobehavioral Reviews37(10): 2516–2528.
40.
PhillipsWBaron-CohenSRutterM (1992) The role of eye contact in goal detection: evidence from normal infants and children with autism or mental handicap. Development and Psychopathology4(3): 375–383.
41.
RitvoRARitvoERGuthrieDet al. (2011) The Ritvo Autism Asperger Diagnostic Scale-Revised (RAADS-R): a scale to assist the diagnosis of autism spectrum disorder in adults: an international validation study. Journal of Autism and Developmental Disorders41: 1076–1089.
42.
ScaifeMBrunerJS (1975) The capacity for joint visual attention in the infant. Nature253(5489): 265–266.
43.
SchilbachLWilmsMEickhoffSBet al. (2010) Minds made for sharing: initiating joint attention recruits reward-related neurocircuitry. Journal of Cognitive Neuroscience22(12): 2702–2715. Available at: http://doi.org/10.1162/jocn.2009.21401
44.
SenjuAJohnsonMH (2009) The eye contact effect: mechanisms and development. Trends in Cognitive Sciences13(3): 127–134. Available at: http://dx.doi.org/10.1016/j.tics.2008.11.009
45.
SigmanMRuskinE (1999) Continuity and change in the social competence of children with autism, Down syndrome and developmental delays. Monographs of the Society for Research in Child Development64(1): 1–114.
SR Research (2004) Experiment Builder (version 1.10.165). Ottawa, ON, Canada: SR Research.
48.
StoneWLOusleyOYLittlefordCD (1997) Motor imitation in young children with autism: what’s the object?Journal of Abnormal Child Psychology25: 475–485.
49.
SvenssonE (2001) Guidelines to statistical evaluation of data from rating scales and questionnaires. Journal of Rehabilitation Medicine33(1): 47–48.
50.
TomaselloM (1995) Joint attention as social cognition. In: MooreCDunhamPJ (eds) Joint Attention: Its Origins and Role in Development. Hillsdale, NJ: Lawrence Erlbaum Associates, pp.1–14.
51.
WelchBL (1947) The generalization of ‘student’s’ problem when several different population variances are involved. Biometrika34: 28–35.
52.
WheelwrightSBaron-CohenSGoldenfeldNet al. (2006) Predicting Autism Spectrum Quotient (AQ) from the Systemizing Quotient-Revised (SQ-R) and Empathy Quotient (EQ). Brain Research1079(1): 47–56. Available at: http://dx.doi.org/10.1016/j.brainres.2006.01.012
53.
WongCKasariC (2012) Play and joint attention of children with autism in the preschool special education classroom. Journal of Autism and Developmental Disorders42(10): 2152–2161.
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