Early Visual Foraging in Relationship to Familial Risk for Autism and Hyperactivity/Inattention

Abstract

Objective: Information foraging is atypical in both autism spectrum disorders (ASDs) and ADHD; however, while ASD is associated with restricted exploration and preference for sameness, ADHD is characterized by hyperactivity and increased novelty seeking. Here, we ask whether similar biases are present in visual foraging in younger siblings of children with a diagnosis of ASD with or without additional high levels of hyperactivity and inattention. Method: Fifty-four low-risk controls (LR) and 50 high-risk siblings (HR) took part in an eye-tracking study at 8 and 14 months and at 3 years of age. Results: At 8 months, siblings of children with ASD and low levels of hyperactivity/inattention (HR/ASD-HI) were more likely to return to previously visited areas in the visual scene than were LR and siblings of children with ASD and high levels of hyperactivity/inattention (HR/ASD+HI). Conclusion: We show that visual foraging is atypical in infants at-risk for ASD. We also reveal a paradoxical effect, in that additional family risk for ADHD core symptoms mitigates the effect of ASD risk on visual information foraging.

Keywords

infants ASD visual attention eye-tracking

Get full access to this article

View all access options for this article.

References

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

Biederman

Spencer

(1999). Attention-deficit/hyperactivity disorder (ADHD) as a noradrenergic disorder. Biological Psychiatry, 46, 1234-1242.

Blaser

Eglington

Carter

A. S.

Kaldy

(2014). Pupillometry reveals a mechanism for the autism spectrum disorder (ASD) advantage in visual tasks. Scientific Reports, 4, Article 4301.

Bornstein

M. H.

Hahn

C. S.

Suwalsky

J. T.

(2013). Physically developed and exploratory young infants contribute to their own long-term academic achievement. Psychological science, 24(10), 1906.

Bronson

(1991). Infant differences in the rate of visual encoding. Child Development, 62, 44-54.

Carballo

J. J.

Rodríguez-Blanco

García-Nieto

Baca-García

(2014). Screening for the ADHD phenotype using the Strengths and Difficulties Questionnaire in a clinical sample of newly referred children and adolescents. Journal of Attention Disorders. Advance online publication. doi:10.1177/1087054714561858

Chen

Burton

Greenberger

Dmitrieva

(1999). Population migration and the variation of dopamine D4 receptor (DRD4) allele frequencies around the globe. Evolution & Human Behavior, 20, 309-324.

Cohen

J. D.

McClure

S. M.

A. J.

(2007). Should I stay or should I go? How the human brain manages the trade-off between exploitation and exploration. Philosophical Transactions of the Royal Society B: Biological Sciences, 362, 933-942.

Costa

V. D.

Tran

V. L.

Turchi

Averbeck

B. B.

(2014). Dopamine modulates novelty seeking behavior during decision making. Behavioral Neuroscience, 128, 556-566.

10.

deKlerk

C. C.

Gliga

Charman

Johnson

M. H.

(2014). Face engagement during infancy predicts later face recognition ability in younger siblings of children with autism. Developmental Science, 17, 596-611.

11.

Dunnett

C. W.

(1955). A multiple comparison procedure for comparing several treatments with a control. Journal of the American Statistical Association, 50, 1096-1121.

12.

Elison

J. T.

Sasson

N. J.

Turner-Brown

L. M.

Dichter

G. S.

Bodfish

J. W.

(2012). Age trends in visual exploration of social and nonsocial information in children with autism. Research in Autism Spectrum Disorders, 6, 842-851.

13.

Elsabbagh

Gliga

Pickles

Hudry

Charman

Johnson

M. H.

, & the BASIS Team. (2013). The development of face orienting mechanisms in infants at-risk for autism. Behavioural Brain Research, 251, 147-154.

14.

Fischer

Graupner

S. T.

Velichkovsky

B. M.

Pannasch

(2013). Attentional dynamics during free picture viewing: Evidence from oculomotor behavior and electrocortical activity. Frontiers in Systems Neuroscience, 7, Article 17.

15.

Frank

M. J.

Doll

B. B.

Oas-Terpstra

Moreno

(2009). Prefrontal and striatal dopaminergic genes predict individual differences in exploration and exploitation. Nature Neuroscience, 12, 1062-1068.

16.

Gliga

Bedford

Charman

Johnson

M. H.

, & the BASIS Team. (2015). Enhanced visual search in infancy predicts emerging autism symptoms. Current Biology, 25, 1727-1730.

17.

Goldin

R. L.

Matson

J. L.

Tureck

Cervantes

P. E.

Jang

(2013). A comparison of tantrum behavior profiles in children with ASD, ADHD and comorbid ASD and ADHD. Research in Developmental Disabilities, 34, 2669-2675.

18.

Hills

T. T.

Todd

P. M.

Goldstone

R. L.

(2008). Search in external and internal spaces evidence for generalized cognitive search processes. Psychological Science, 19, 802-808.

19.

Jensen

P. S.

Mrazek

Knapp

P. K.

Steinberg

Pfeffer

Schowalter

Shapiro

(1997). Evolution and revolution in child psychiatry: ADHD as a disorder of adaptation. Journal of the American Academy of Child & Adolescent Psychiatry, 36, 1672-1681.

20.

Jepma

Nieuwenhuis

(2011). Pupil diameter predicts changes in the exploration–exploitation trade-off: Evidence for the adaptive gain theory. Journal of Cognitive Neuroscience, 23, 1587-1596.

21.

Johnson

M. H.

(2012). Executive function and developmental disorders: The flip side of the coin. Trends in Cognitive Sciences, 16, 454-457.

22.

Johnson

M. H.

Gliga

Jones

Charman

(2015). Annual research review: Infant development, autism, and ADHD—Early pathways to emerging disorders. Journal of Child Psychology and Psychiatry, 56, 228-247.

23.

Johnson

M. H.

Jones

Gliga

(2015). Brain adaptation and alternative developmental trajectories. Development and Psychopathology, 27, 425-442.

24.

Kacelnik

Houston

A. I.

Krebs

J. R.

(1981). Optimal foraging and territorial defense in the great tit (Parus major). Behavioral Ecology and Sociobiology, 8, 35-40.

25.

Krebs

J. R.

Kacelnik

Taylor

(1978). Test of optimal sampling by foraging great tits. Nature, 275, 27-31.

26.

Kriete

Noelle

D. C.

(2015). Dopamine and the development of executive dysfunction in autism spectrum disorders. PLoS ONE, 10(3), e0121605.

27.

Larsson

Chang

D’Onofrio

B. M.

Lichtenstein

(2014). The heritability of clinically diagnosed attention deficit hyperactivity disorder across the lifespan. Psychological Medicine, 44, 2223-2229.

28.

Lord

Rutter

Le Couteur

(1994). Autism Diagnostic Interview-Revised: a revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. Journal of autism and developmental disorders, 24(5), 659-685.

29.

Lord

Risi

Lambrecht

Cook

E. H.

Jr. Leventhal

B. L.

DiLavore

P. C.

Rutter

(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 Disorders, 30, 205-223.

30.

Matthews

L. J.

Butler

P. M.

(2011). Novelty-seeking DRD4 polymorphisms are associated with human migration distance out-of-Africa after controlling for neutral population gene structure. American Journal of Physical Anthropology, 145, 382-389.

31.

Messinger

Young

G. S.

Ozonoff

Dobkins

Carter

Zwaigenbaum

Sigman

(2013). Beyond autism: A Baby Siblings Research Consortium study of high-risk children at three years of age. Journal of the American Academy of Child & Adolescent Psychiatry, 52, 300-308.

32.

Mullen

(1995). Mullen Scales of Early Learning (AGS ed.). Bloomington, MN: Pearson Assessments.

33.

Ozonoff

Young

G. S.

Carter

Messinger

Yirmiya

Zwaigenbaum

Stone

W. L.

(2011). Recurrence risk for autism spectrum disorders: A Baby Siblings Research Consortium study. Pediatrics, 128, e488-e495.

34.

Pannasch

Helmert

J. R.

Roth

Herbold

A. K.

Walter

(2008). Visual fixation durations and saccade amplitudes: Shifting relationship in a variety of conditions. Journal of Eye Movement Research, 2(2), Article 4.

35.

Pellicano

Smith

A. D.

Cristino

Hood

B. M.

Briscoe

Gilchrist

I. D.

(2011). Children with autism are neither systematic nor optimal foragers. Proceedings of the National Academy of Sciences, 108, 421-426.

36.

Pierce

Courchesne

(2001). Evidence for a cerebellar role in reduced exploration and stereotyped behavior in autism. Biological Psychiatry, 49, 655-664.

37.

Risko

E. F.

Anderson

N. C.

Lanthier

Kingstone

(2012). Curious eyes: Individual differences in personality predict eye movement behavior in scene-viewing. Cognition, 122, 86-90.

38.

Rommelse

N. N.

Geurts

H. M.

Franke

Buitelaar

J. K.

Hartman

C. A.

(2011). A review on cognitive and brain endophenotypes that may be common in autism spectrum disorder and attention-deficit/hyperactivity disorder and facilitate the search for pleiotropic genes. Neuroscience & Biobehavioral Reviews, 35, 1363-1396.

39.

Russell

Rodgers

L. R.

Ukoumunne

O. C.

Ford

(2014). Prevalence of parent-reported ASD and ADHD in the UK: Findings from the Millennium Cohort Study. Journal of Autism and Developmental Disorders, 44, 31-40.

40.

Rutter

Bailey

Lord

(2003). The Social Communication Questionnaire (SCQ). Torrance, CA: Western Psychological Services.

41.

Salgado

C. A.

Bau

C. H.

Grevet

E. H.

Fischer

A. G.

Victor

M. M.

Kalil

K. L.

Belmonte-de-Abreu

(2008). Inattention and hyperactivity dimensions of ADHD are associated with different personality profiles. Psychopathology, 42, 108-112.

42.

Schlesinger

Amso

(2013). Image free-viewing as intrinsically-motivated exploration: estimating the learnability of center-of-gaze image samples in infants and adults. Frontiers in psychology. Epub ahead of print 31 October 2015. DOI: 10.3389/fpsyg.2013.00802.

43.

Solanto

M. V.

(2002). Dopamine dysfunction in AD/HD: Integrating clinical and basic neuroscience research. Behavioural Brain Research, 130, 65-71.

44.

Tye

Mercure

Ashwood

K. L.

Azadi

Asherson

Johnson

M. H.

McLoughlin

(2013). Neurophysiological responses to faces and gaze direction differentiate children with ASD, ADHD and ASD+ADHD. Developmental Cognitive Neuroscience, 5, 71-85.

45.

Ullebø

A. K.

Posserud

M. B.

Heiervang

Gillberg

Obel

(2011). Screening for the attention deficit hyperactivity disorder phenotype using the Strength and Difficulties Questionnaire. European Child & Adolescent Psychiatry, 20, 451-458.

46.

Williams

Taylor

(2006). The evolution of hyperactivity, impulsivity and cognitive diversity. Journal of the Royal Society Interface, 3, 399-413.

47.

World Health Organization. (1993). The ICD-10 classification of mental and behavioural disorders: Diagnostic criteria for research. Geneva, Switzerland: Author.

48.

Yerys

B. E.

Wallace

G. L.

Sokoloff

J. L.

Shook

D. A.

James

J. D.

Kenworthy

(2009). Attention deficit/hyperactivity disorder symptoms moderate cognition and behavior in children with autism spectrum disorders. Autism Research, 2, 322-333.