A Statistical Physics Perspective to Understand Social Visual Attention in Autism Spectrum Disorder

Abstract

This study investigated social visual attention in children with Autism Spectrum Disorder (ASD) and with typical development (TD) in the light of Brockmann and Geisel’s model of visual attention. The probability distribution of gaze movements and clustering of gaze points, registered with eye-tracking technology, was studied during a free visual exploration of a gaze stimulus. A data-driven analysis of the distribution of eye movements was chosen to overcome any possible methodological problems related to the subjective expectations of the experimenters about the informative contents of the image in addition to a computational model to simulate group differences. Analysis of the eye-tracking data indicated that the scanpaths of children with TD and ASD were characterized by eye movements geometrically equivalent to Lévy flights. Children with ASD showed a higher frequency of long saccadic amplitudes compared with controls. A clustering analysis revealed a greater dispersion of eye movements for these children. Modeling of the results indicated higher values of the model parameter modulating the dispersion of eye movements for children with ASD. Together, the experimental results and the model point to a greater dispersion of gaze points in ASD.

Keywords

eye-tracking ASD Lévy flight social visual attention

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References

Al-Rahayfeh

Faezipour

(2013) Eye tracking and head movement detection a state-of-art survey. IEEE Journal of Translational Engineering in Health and Medicine 1: 1–12.

American Psychiatric Association (2000) Diagnostic and Statistical Manual of Mental Disorders (4th ed., text rev.), Washington, DC: Author.

Armano

Javarone

M. A.

(2013) Clustering dataset by complex networks analysis. Complex Adaptive System Modeling 1: 1–10.

Barton

J. J.

Radcliffe

Cherkasova

M. V.

Edelman

Intriligator

J. M.

(2006) Information processing during face recognition: The effects of familiarity, inversion, and morphing on scanning fixations. Perception 35: 1089–1105.

Bayliss

A. P.

di Pellegrino

Tipper

S. P.

(2005) Sex differences in eye gaze and symbolic cueing of attention. The Quarterly Journal of Experiemntal Psychology 58: 631–650.

Belik

V. V.

Brockmann

(2007) Accelerating random walks by disorder. New Journal of Physics 9: 1–8.

Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society. Series B (Methodological), 57, 289–300.

Benjamini, Y., & Yekutieli, D. (2001). The control of the false discovery rate in multiple testing under dependency. Annals of Statistics, 29, 1165-1188.

Birmingham

Bischof

W. F.

Kingstone

(2009) Saliency does not account for fixations to eyes within social scenes. Vision Research 49: 2992–3000.

10.

Boccignone

Ferraro

(2004) Modelling gaze shift as a constrained random walk. Physica A: Statistical Mechanics and its Applications 331: 207–218.

11.

Bojko

(2013) Eye Tracking the User Experience—A Practical Guide to Research, New York: Rosenfeld Media.

12.

Borji

Itti

(2013) State-of-the-art in visual attention modeling. IEEE Transactions on pattern analysis and machine intelligence 35: 185–207.

13.

Brockmann

Geisel

(2000) The ecology of gaze shifts. Neurocomputing 643: 32–33.

14.

Bruce

N. D. B.

Tsotsos

J. K.

(2009) Saliency based on information maximization. Advances in Neural Information Processing Systems 18: 155–162.

15.

Butterworth

Jarrett

(1991) What minds have in common is space: Spatial mechanisms serving joint visual attention in infancy. British Journal of Developmental Psychology 9: 55–72.

16.

Caldara

Miellet

(2011) iMap: A novel method for statistical fixation mapping of eye movement data. Behavior Research Methods 43: 864–878.

17.

Chawarska

Klin

Volkmar

(2003) Automatic attention cueing through eye movement in 2-year-old children with autism. Child Development 74: 1108–1122.

18.

Cook

Barbalat

Blakemore

S. J.

(2012) Top-down modulation of the perception of other people in schizophrenia and autism. Frontiers in Human Neuroscience. Article 175.

19.

Csibra

Gergely

(2006) Social learning and social cognition: The case for pedagogy. In: Munakata

Johnson

M. H.

(eds) Processes of change in brain and cognitive development. Attention and performance Vol. XXI, Oxford, UK: Oxford University Press, pp. 249–274.

20.

Dawson

(2008) Early behavioral intervention, brain plasticity, and the prevention of autism spectrum disorder. Development and Psychopathology 20: 775–803.

21.

Dawson

Meltzoff

A. N.

Osterling

Rinaldi

(1998) Neuropsychological correlates of early symptoms of autism. Child Development 69: 1276–1285.

22.

Dawson

Osterling

Rinaldi

Carver

McPartland

(2001) Brief report: Recognition memory and stimulus-reward associations: Indirect support for the role of ventromedial prefrontal dysfunction in autism. Journal of Autism and Developmental Disorders 31: 337–341.

23.

Dawson

Toth

Abbott

Osterling

Munson

Estes

Liaw

(2004) Early social attention impairments in autism: Social orienting, joint attention, and attention to distress. Developmental Psychology 40: 271–283.

24.

D’Entremont

Hains

S. M. J.

Muir

D. W.

(1997) A demonstration of gaze following in 3- to 6-month-olds. Infant Behavior and Development 20: 569–572.

25.

Doherty-Sneddon

Riby

D. M.

Whittle

(2012) Gaze aversion as a cognitive load management strategy in autism spectrum disorder and William syndrome. Journal of Child Psychology and Psychiatry 53: 420–430.

26.

Driver

Davis

Ricciardelli

Kidd

Maxwell

Baron-Cohen

(1999) Gaze perception triggers reflexive visuospatial orienting. Visual Cognition 6: 509–540.

27.

Falck-Ytter

Bölte

Gredebäck

(2013) Eye tracking in early autism research. Journal of Neurodevelopmental Disorders 5: 28.

28.

Falck-Ytter

von Hofsten

(2011) How special is social looking in ASD: A review. Progress in Brain Research 189: 209–222.

29.

Fecteau

J. H.

Munoz

D. P.

(2006) Salience, relevance, and spiking neurons: a priority map for target selection. Trends in Cognitive Science 10: 382–390.

30.

Fletcher-Watson

Leekam

S. R.

Benson

Frank

M. C.

Findlay

J. M.

(2009) Eye-movements reveal attention to social information in autism spectrum disorders. Neuropsychologia 47: 248–257.

31.

Gilchrist

I. D.

Harvey

(2006) Evidence for a systematic component within scan paths in visual search. Visual cognition 14: 704–715.

32.

Hadjikhani

Chabris

C. F.

Joseph

R. M.

Clark

McGrath

Aharon

Tager-Flusberg

(2003) Early visual cortex organization in autism: An fMRI study. Neuroreport 15: 267–270.

33.

Henderson

J. M.

Williams

C. C.

Falk

R. J.

(2005) Eye movements are functional during face learning. Memory & Cognition 33: 98–106.

34.

Hoehl

Reid

Mooney

Striano

(2008) What are you looking at? Infants’ neural processing of an adult’s object-directed eye gaze. Developmental Science 11: 10–16.

35.

Hoehl

Parise

Palumbo

Reid

Handl

Striano

(2009) Looking at eye gaze processing and its neural correlates in infancy—Implications for social development and autism. Child Development 80: 968–985.

36.

Hood

B. M.

Willen

J. D.

Driver

(1998) Adults’ eyes trigger shifts of visual attention in human infants. Psychological Science 9: 131–134.

37.

Hooge

I. T.

Erkelens

C. J.

(1998) Adjustment of fixation duration in visual search. Vision Research 38: 1295–1302.

38.

Itti

Koch

(2001) Computational modeling of visual attention. Natural Revies of Neuroscience 2: 194–203.

39.

Karmiloff-Smith

(1998) Development itself is the key to understanding developmental disorders. Trends in Cognitive Sciences 2: 389–398.

40.

Koehler

Guo

Zhang

Eckstein

(2014) What do saliency models predict? Journal of Vision 14: 1–28.

41.

Klin

Jones

Schultz

Volkmar

Cohen

(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.

42.

Kylliäinen

Hietanen

J. K.

(2004) Attention orienting by another’s gaze direction in children with autism. Journal of Child Psychology and Psychiatry 45: 435–444.

43.

Leekam

Baron-Cohen

Perrett

Milders

Brown

(1997) Eye direction detection: A dissociation between geometric and joint attention skills in autism. British Journal of Developmental Psychology 15: 77–95.

44.

Leekam

Hunnisett

Moore

(1998) Targets and cues: Gaze-following in children with autism. Journal of Child Psychology and Psychiatry and Allied Disciplines 39: 951–962.

45.

Leekam

S. R.

(2005) Why do children with autism have a joint attention impairment? In: Eilan

Hoerl

McCormack

Roessler

(eds) Joint attention: Perspectives from philosophy and psychology, Oxford (UK): Oxford University Press, pp. 205–229.

46.

Lord

Rutter

DiLavore

P. C.

Risi

(1999) Autism diagnostic observation schedule (ADOS), Los Angeles, CA: Western Psychological Services.

47.

Morimoto

C. H.

Mimica

(2005) Eye gaze tracking techniques for interactive applications. Computer Vision Image Understanding, Special Issue on Eye Detection and Tracking 98: 4–24.

48.

Mottron

Dawson

Soulières

Hubert

Burack

(2006) Enhanced perceptual functioning in autism: An update, and eight principles of autistic perception. Journal of Autism and Developmental Disorders 36: 27–43.

49.

Mundy

(1995) Joint attention and social-emotional approach behavior in children with autism. Development and Psychopathology 7: 63–82.

50.

Mundy

(2011) The social behavior of autism: A parallel and distributed information processing perspective. In: Amaral

D. G.

Dawson

Geschwind

D. H.

(eds) Autism spectrum disorders, New York: Oxford University Press, pp. 149–171.

51.

Mundy

Burnette

(2005) Joint attention and neurodevelopmental models of autism. In: Volkmar

F. R.

Paul

Klin

Cohen

(eds) Handbook of autism and pervasive developmental disorders. Diagnosis, development, neurobiology, and behaviour, 3rd ed. Vol. 1. Hoboken, NJ: John Wiley, pp. 650–681.

52.

Nation

Penny

(2008) Sensitivity to eye gaze in autism: Is it normal? Is it automatic? Is it social? Development and Psychopathology 20: 79–97.

53.

Neumann

Spezio

M. L.

Piven

Adolphs

(2006) Looking you in the mouth: Abnormal gaze in autism resulting from impaired top-down modulation of visual attention. Social Cognitive and Affective Neuroscience 1: 194–202.

54.

Noris

Nadel

Barker

Hadjikhani

Billard

(2012) Investigating gaze of children with ASD in naturalistic settings. Plos One 7: e44144.

55.

Noton

Stark

(1971) Scanpaths in eye movements during pattern perception. Science 171: 308–311.

56.

Orban de Xivry

J. J.

Ramon

Lefevre

Rossion

(2008) Reduced fixation on the upper area of personally familiar faces following acquired prosopagnosia. Journal of Neuropsychology 2: 245–268.

57.

Pellicano

(2012) The development of executive functioning in Autism. Autism Research and Treatment 2012. Article ID 146132, 8 pp.

58.

Pigott

T. D.

(2001) A review of methods for missing data. Educational Research and Evaluation 7: 353–383.

59.

Sasson

N. J.

Touchston

E. W.

(2014) Visual attention to competing social and object image by preschool children with autism spectrum disorder. Journal of Autism and Developmental Disorders 44: 584–592.

60.

Scaife

Bruner

J. S.

(1975) The capacity for joint visual attention in the infant. Nature 253: 265–266.

61.

Schultz

R. T.

(2005) Developmental deficits in social perception in autism: The role of the amygdala and fusiform face area. International Journal of Developmental Neuroscience 23: 125–141.

62.

Serences

J. T.

Yantis

(2006) Selective visual attention and perceptual coherence. Trends in Cognitive Science 10: 38–45.

63.

Simmons

D. R.

Robertson

A. E.

McKay

L. S.

Toal

McAleer

Pollick

F. E.

(2009) Vision in autism spectrum disorders. Vision Research 49: 2705–2739.

64.

Tobii Eye Tracking White Paper—An introduction to eye tracking and Tobii Eye Trackers. (2010). Tobii Technology. Retrieved from www.tobii.com.

65.

Tomasello

(1999) The cultural origins of human cognition, Cambridge: Harvard University Press.

66.

Wass

S. V.

Jones

E. J. H.

Gliga

Smith

T. J.

Charman

Johson

M. H.

(2015) the BASIS Team. Shorter spontaneous fixation durations in infants with later emerging autism. Scientific Reports 5: 8284.

67.

Yarbus

A. L.

(1967) Eye movements and vision, New York: Plenum Press.

68.

Zhu

(2007) Novel eye gaze tracking techniques under natural head movement. IEEE Transactions on Biomedical Engineering 54: 2246–2260.