Skip to main content
SpringerLink
Log in

Paternal Autistic Traits are Predictive of Infants Visual Attention

  • Original Paper
  • Published:
Journal of Autism and Developmental Disorders Aims and scope Submit manuscript

Abstract

Since subthreshold autistic social impairments aggregate in family members, and since attentional dysfunctions appear to be one of the earliest cognitive markers of children with autism, we investigated in the general population the relationship between infants’ attentional functioning and the autistic traits measured in their parents. Orienting and alerting attention systems were measured in 8-month-old infants using a spatial cueing paradigm. Results showed that only paternal autistic traits were linked to their children’s: (1) attentional disengagement; (2) rapid attentional orienting and (3) alerting. Our findings suggest that an early dysfunction of orienting and alerting systems might alter the developmental trajectory of future ability in social cognition and communication.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Almeida, R. A., Dickinson, J. E., Maybery, M. T., Badcock, J. C., & Badcock, D. R. (2010). A new step towards understanding embedded figures test performance in the autism spectrum: The radial frequency search task. Neuropsychologia, 48(2), 374–381.

    Article  PubMed  Google Scholar 

  • Amaral, D. G., Schumann, C. M., & Nordahl, C. W. (2008). Neuroanatomy of autism. Trends in Neurosciences, 31(3), 137–145.

    Article  PubMed  Google Scholar 

  • American Psychiatric Association. (1994). Task force on DSM-IV. DSM-IV: Diagnostic and statistical manual of mental disorders.

  • Ames, C., & Fletcher-Watson, S. (2010). A review of methods in the study of attention in autism. Developmental Review, 30(1), 52–73.

    Article  Google Scholar 

  • Baron-Cohen, S., Lombardo, M. V., Auyeung, B., Ashwin, E., Chakrabarti, B., & Knickmeyer, R. (2011). Why are autism spectrum conditions more prevalent in males? PLoS Biology, 9(6), e1001081.

    Article  PubMed Central  PubMed  Google Scholar 

  • Baron-Cohen, S., Wheelwright, S., Skinner, R., Martin, J., & Clubley, E. (2001). The autism–spectrum quotient (AQ): Evidence from asperger syndrome/high-functioning autism, males and females, scientists and mathematicians. Journal of Autism and Developmental Disorders, 31(1), 5–17.

    Article  PubMed  Google Scholar 

  • Bayliss, A. P., & Kritikos, A. (2011). Brief report: Perceptual load and the autism spectrum in typically developed individuals. Journal of Autism and Developmental Disorders, 41(11), 1573–1578.

    Article  PubMed  Google Scholar 

  • Belmonte, M. K., Gomot, M., & Baron-Cohen, S. (2010). Visual attention in autism families: ‘unaffected’ sibs share atypical frontal activation. Journal of Child Psychology and Psychiatry, 51(3), 259–276.

    Article  PubMed  Google Scholar 

  • Bishop, D. V. M., Maybery, M., Maley, A., Wong, D., Hill, W., & Hallmayer, J. (2004). Using self-report to identify the broad phenotype in parents of children with autistic spectrum disorders: A study using the autism–spectrum quotient. Journal of Child Psychology and Psychiatry, 45(8), 1431–1436.

    Article  PubMed  Google Scholar 

  • Bolton, P., Pickles, A., Murphy, M., & Rutter, M. (1998). Autism, affective and other psychiatric disorders: Patterns of familial aggregation. Psychological Medicine, 28(2), 385–395.

    Article  PubMed  Google Scholar 

  • Bruneau, N., Bonnet-Brilhault, F., Gomot, M., Adrien, J., & Barthélémy, C. (2003). Cortical auditory processing and communication in children with autism: Electrophysiological/behavioral relations. International Journal of Psychophysiology, 51(1), 17–25.

    Article  PubMed  Google Scholar 

  • Butterworth, G., & Grover, L. (1990). Joint visual attention, manual pointing, and pre-verbal communication in human infancy. In M. Jeannerod (Ed.), Attention and performance XIII (pp. 605–624). Hillside, NJ: Erlbaum.

    Google Scholar 

  • Butterworth, G., & Jarrett, N. (1991). What minds have in common is space: Spatial mechanisms serving joint attention in infancy. British Journal of Developmental Psychology, 9, 55–72.

    Article  Google Scholar 

  • Callejas, A., Lupianez, J., & Tudela, P. (2004). The three attentional networks: On their independence and interactions. Brain and Cognition, 54, 225–227.

    Article  PubMed  Google Scholar 

  • Carpenter, M., Nagell, K., & Tomasello, M. (1998). Social cognition, joint attention, and communicative competence from 9 to 15 months of age. Monographs of the Society for Research in Child Development, 63(4), 1–143.

    Google Scholar 

  • Chawarska, K., Macari, S., & Shic, F. (2013). Decreased spontaneous attention to social scenes in 6-month-old infants later diagnosed with autism spectrum disorders. Biological Psychiatry, 74, 195–203.

    Article  PubMed  Google Scholar 

  • Ciesielski, K., Courchesne, E., & Elmasian, R. (1990). Effects of focused selective attention tasks on event-related potentials in autistic and normal individuals. Electroencephalography and Clinical Neurophysiology, 75(3), 207–220.

    Article  PubMed  Google Scholar 

  • Constantino, J. N., & Todd, R. D. (2003). Autistic traits in the general population: A twin study. Archives of General Psychiatry, 60(5), 524–530.

    Article  PubMed  Google Scholar 

  • Constantino, J. N., & Todd, R. D. (2005). Intergenerational transmission of subthreshold autistic traits in the general population. Biological Psychiatry, 57(6), 655–660.

    Article  PubMed  Google Scholar 

  • Corbetta, M., & Shulman, G. L. (2002). Control of goal-directed and stimulus-driven attention in the brain. Nature Review Neuroscience, 3, 201–215.

    Article  Google Scholar 

  • Corbetta, M., & Shulman, G. L. (2011). Spatial neglect and attention networks. Annual Review of Neuroscience, 34, 569–599.

    Article  PubMed Central  PubMed  Google Scholar 

  • Courchesne, E., Lincoln, A. J., Kilman, B. A., & Galambos, R. (1985). Event-related brain potential correlates of the processing of novel visual and auditory information in autism. Journal of Autism and Developmental Disorders, 15(1), 55–76.

    Article  PubMed  Google Scholar 

  • Courchesne, E., Townsend, J., Akshoomoff, N. A., Saitoh, O., Yeung-Courchesne, R., Lincoln, A. J., et al. (1994). Impairment in shifting attention in autistic and cerebellar patients. Behavioral Neuroscience, 108(5), 848–865.

    Article  PubMed  Google Scholar 

  • Dakin, S., & Frith, U. (2005). Vagaries of visual perception in autism. Neuron, 48(3), 497–507.

    Article  PubMed  Google Scholar 

  • Dawson, G., & Lewy, A. (1989). Arousal, attention, and the socioemotional impairments of individuals with autism. In G. Dawson (Ed.), Autism: Nature, diagnosis, and treatment (pp. 49–74). New York: Guilford Press.

    Google Scholar 

  • Dawson, G., Webb, S., Schellenberg, G. D., Dager, S., Friedman, S., Aylward, E., et al. (2002). Defining the broader phenotype of autism: Genetic, brain, and behavioral perspectives. Development and Psychopathology, 14(3), 581–611.

    Article  PubMed  Google Scholar 

  • Dawson, G., Webb, S. J., Wijsman, E., Schellenberg, G., Estes, A., Munson, J., et al. (2005). Neurocognitive and electrophysiological evidence of altered face processing in parents of children with autism: Implications for a model of abnormal development of social brain circuitry in autism. Development and Psychopathology, 17(3), 679–697.

    Article  PubMed  Google Scholar 

  • Elsabbagh, M., Fernandes, J., Jane Webb, S., Dawson, G., Charman, T., & Johnson, M. H. (2013). Disengagement of visual attention in infancy is associated with emerging autism in toddlerhood. Biological Psychiatry, 74, 189–194.

    Article  PubMed Central  PubMed  Google Scholar 

  • Elsabbagh, M., & Johnson, M. H. (2010). Getting answers from babies about autism. Trends in Cognitive Sciences, 14(2), 81–87.

    Article  PubMed  Google Scholar 

  • Elsabbagh, M., Volein, A., Holmboe, K., Tucker, L., Csibra, G., Baron-Cohen, S., et al. (2009). Visual orienting in the early broader autism phenotype: Disengagement and facilitation. Journal of Child Psychology and Psychiatry, 50(5), 637–642.

    Article  PubMed Central  PubMed  Google Scholar 

  • Fischer, B., & Breitmeyer, B. (1987). Mechanisms of visual attention revealed by saccadic eye movements. Neuropsychologia, 25(1), 73–83.

    Article  PubMed  Google Scholar 

  • Gold, M. S., & Gold, J. R. (1975). Autism and attention: Theoretical considerations and a pilot study using set reaction time. Child Psychiatry and Human Development, 6, 68–80.

    Article  PubMed  Google Scholar 

  • Grinter, E. J., Maybery, M. T., Van Beek, P. L., Pellicano, E., Badcock, J. C., & Badcock, D. R. (2009). Global visual processing and self-rated autistic-like traits. Journal of Autism and Developmental Disorders, 39(9), 1278–1290.

    Article  PubMed  Google Scholar 

  • Hood, B. (1995). Shifts of visual attention in the human infant: A neuroscientific approach. Advances in Infancy Research, 9, 163–216.

    Google Scholar 

  • Hutman, T. (2013). From attention to interaction: The emergence of autism during infancy. Biological Psychiatry, 74, 162–163.

    Article  PubMed  Google Scholar 

  • Johnson, M. H. (2011). Interactive specialization: A domain-general framework for human functional brain development? Developmental Cognitive Neuroscience, 1(1), 7–21.

    Article  PubMed  Google Scholar 

  • Johnson, M. H., Posner, M. I., & Rothbart, M. K. (1991). Components of visual orienting in early infancy: Contingency learning, anticipatory looking, and disengaging. Journal of Cognitive Neuroscience, 3(4), 335–344.

    Article  PubMed  Google Scholar 

  • Johnson, M. H., & Tucker, L. A. (1996). The development and temporal dynamics of spatial orienting in infants. Journal of Experimental Child Psychology, 63(1), 171–188.

    Article  PubMed  Google Scholar 

  • Joseph, R. M., Keehn, B., Connolly, C., Wolfe, J. M., & Horowitz, T. S. (2009). Why is visual search superior in autism spectrum disorder? Developmental Science, 12(6), 1083–1096.

    Article  PubMed  Google Scholar 

  • Karmiloff-Smith, A. (1998). Development itself is the key to understanding developmental disorders. Trends in Cognitive Sciences, 2(10), 389–398.

    Article  PubMed  Google Scholar 

  • Keehn, B., Lincoln, A. J., Müller, R. A., & Townsend, J. (2010). Attentional networks in children and adolescents with autism spectrum disorder. Journal of Child Psychology and Psychiatry, 51(11), 1251–1259.

    Article  PubMed Central  PubMed  Google Scholar 

  • Keehn, B., Müller, R., & Townsend, J. (2013). Atypical attentional networks and the emergence of autism. Neuroscience and Biobehavioral Reviews, 37, 164–183.

    Article  PubMed Central  PubMed  Google Scholar 

  • Klin, A., Jones, W., Schultz, R., Volkmar, F., & Cohen, D. (2002). Visual fixation patterns during viewing of naturalistic social situations as predictors of social competence in individuals with autism. Archives of General Psychiatry, 59(9), 809–816.

    Article  PubMed  Google Scholar 

  • Koldewyn, K., Whitney, D., & Rivera, S. M. (2010). The psychophysics of visual motion and global form processing in autism. Brain, 133(2), 599–610.

    Article  PubMed Central  PubMed  Google Scholar 

  • Landry, R., & Bryson, S. E. (2004). Impaired disengagement of attention in young children with autism. Journal of Child Psychology and Psychiatry, 45(6), 1115–1122.

    Article  PubMed  Google Scholar 

  • Mann, T. A., & Walker, P. (2003). Autism and a deficit in broadening the spread of visual attention. Journal of Child Psychology and Psychiatry, 44(2), 274–284.

    Article  PubMed  Google Scholar 

  • McCleery, J. P., Akshoomoff, N., Dobkins, K. R., & Carver, L. J. (2009). Atypical face versus object processing and hemispheric asymmetries in 10-month-old infants at risk for autism. Biological Psychiatry, 66(10), 950–957.

    Article  PubMed Central  PubMed  Google Scholar 

  • Mottron, L., Dawson, M., Soulieres, I., Hubert, B., & Burack, J. (2006). Enhanced perceptual functioning in autism: An update, and eight principles of autistic perception. Journal of Autism and Developmental Disorders, 36(1), 27–43.

    Article  PubMed  Google Scholar 

  • Mundy, P. (2003). Annotation: The neural basis of social impairments in autism—The role of the dorsal medial–frontal cortex and anterior cingulate system. Journal of Child Psychology and Psychiatry, 44(6), 793–809.

    Article  PubMed  Google Scholar 

  • Mundy, P., & Newell, L. (2007). Attention, joint attention, and social cognition. Current Directions in Psychological Science, 16(5), 269–274.

    Article  PubMed Central  PubMed  Google Scholar 

  • Orekhova, E. V., Stroganova, T., Prokofiev, A., Nygren, G., Gillberg, C., & Elam, M. (2009). The right hemisphere fails to respond to temporal novelty in autism: Evidence from an ERP study. Clinical Neurophysiology, 120(3), 520–529.

    Article  PubMed  Google Scholar 

  • Parner, E. T., Baron-Cohen, S., Lauritsen, M. B., Jørgensen, M., Schieve, L. A., Yeargin-Allsopp, M., et al. (2012). Parental age and autism spectrum disorders. Annals of Epidemiology, 22(3), 143–150.

    Article  PubMed  Google Scholar 

  • Pellicano, E., & Burr, D. (2012). When the world becomes ‘too real’: A bayesian explanation of autistic perception. Trends in Cognitive Sciences, 16(10), 504–510.

    Article  PubMed  Google Scholar 

  • Petersen, S. E., & Posner, M. I. (2012). The attention system of the human brain: 20 years after. Annual Review of Neuroscience, 35, 73–89.

    Article  PubMed Central  PubMed  Google Scholar 

  • Posner, M. I. (1980). Orienting of attention. Quarterly Journal of Experimental Psychology, 32(1), 3–25.

    Article  PubMed  Google Scholar 

  • Posner, M. I., & Petersen, S. E. (1990). The attention system of the human brain. Annual Review of Neuroscience, 13, 25–42.

    Article  PubMed  Google Scholar 

  • Richards, J. E. (1997). Peripheral stimulus localization by infants: Attention, age and individual differences in heart rate variability. Journal of Experimental Psychology: Human Perception and Performance, 23(3), 667–680.

    PubMed  Google Scholar 

  • Richards, J. E. (2001). Attention in young infants: A developmental psychophysiological perspective. In C. A. Nelson & M. Luciana (Eds.), Handbook of developmental cognitive neuroscience (pp. 321–338). Cambridge, MA: MIT Press.

    Google Scholar 

  • Richards, J. E. (2003). Attention affects the recognition of briefly presented visual stimuli in infants: An ERP study. Developmental Science, 6(3), 312–328.

    Article  PubMed Central  PubMed  Google Scholar 

  • Richards, J. E. (2005). Localizing cortical sources of event-related potentials in infants’ covert orienting. Developmental Science, 8(3), 255–278.

    Article  PubMed Central  PubMed  Google Scholar 

  • Ronconi, L., Basso, D., Gori, S., & Facoetti, A. (2013b). TMS on right frontal eye fields induces an inflexible focus of attention. Cerebral Cortex. doi: 10.1093/cercor/bhs319.

  • Ronconi, L., Gori, S., Giora, E., Ruffino, M., Molteni, M., & Facoetti, A. (2013a). Deeper attentional masking by lateral objects in children with autism. Brain and Cognition, 82(2), 213–218.

    Article  PubMed  Google Scholar 

  • Ronconi, L., Gori, S., Ruffino, M., Franceschini, S., Urbani, B., Molteni, M., et al. (2012). Decreased coherent motion discrimination in autism spectrum disorder: The role of attentional zoom-out deficit. PLoS ONE, 7(11), e49019. doi:10.1371/journal.pone.0049019.

    Article  PubMed Central  PubMed  Google Scholar 

  • Ronconi, L., Gori, S., Ruffino, M., Molteni, M., & Facoetti, A. (2013a). Zoom-out attentional impairment in children with autism spectrum disorder. Cortex doi: 10.1016/j.cortex.2012.03.005.

  • Saalmann, Y. B., Pigarev, I. N., & Vidyasagar, T. R. (2007). Neural mechanisms of visual attention: How top–down feedback highlights relevant locations. Science, 316(5831), 1612–1615.

    Article  PubMed  Google Scholar 

  • Sacrey, L. R., Bryson, S. E., & Zwaigenbaum, L. (2013). Prospective examination of visual attention during play in infants at high-risk for autism spectrum disorder: A longitudinal study from 6 to 36 months of age. Behavioural Brain Research, 256, 441–450.

    Article  PubMed  Google Scholar 

  • Sucksmith, E., Roth, I., & Hoekstra, R. (2011). Autistic traits below the clinical threshold: Re-examining the broader autism phenotype in the 21st century. Neuropsychology Review, 21(4), 360–389.

    Article  PubMed  Google Scholar 

  • Sutherland, A., & Crewther, D. P. (2010). Magnocellular visual evoked potential delay with high autism spectrum quotient yields a neural mechanism for altered perception. Brain, 133(7), 2089–2097.

    Article  PubMed  Google Scholar 

  • Townsend, J., Courchesne, E., & Egaas, B. (1996). Slowed orienting of covert visual–spatial attention in autism: Specific deficits associated with cerebellar and parietal abnormality. Development and Psychopathology, 8(3), 563–584.

    Article  Google Scholar 

  • Wainwright-Sharp, J. A., & Bryson, S. E. (1993). Visual orienting deficits in high-functioning people with autism. Journal of Autism and Developmental Disorders, 23(1), 1–13.

    Article  PubMed  Google Scholar 

  • Wass, S., Porayska-Pomsta, K., & Johnson, M. H. (2011). Training attentional control in infancy. Current Biology, 21, 1543–1547.

    Article  PubMed Central  PubMed  Google Scholar 

  • Zwaigenbaum, L., Bryson, S., Rogers, T., Roberts, W., Brian, J., & Szatmari, P. (2005). Behavioral manifestations of autism in the first year of life. International Journal of Developmental Neuroscience, 23(2), 143–152.

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This research project was supported by two grants: one from Università di Padova Progetti di Ricerca di Ateneo 2011 (code CPDA113109/11) and one from Progetti di Eccellenza CARIPARO (rep. no. 1873/2012). The authors are deeply indebted to the infants who took part in the study and to their parents. We also thank Caterina Masiero for her technical help.

Conflict of interest

None.

Author information

Author notes

  1. Laura Franchin

    Present address: Department of Psychology and Cognitive Science, University of Trento, Trento, Italy

Authors and Affiliations

  1. Developmental and Cognitive Neuroscience Lab, Department of General Psychology, University of Padua, Padua, Italy

    Luca Ronconi, Andrea Facoetti & Roberta Bettoni

  2. Developmental Neuropsychology Unit, Scientific Institute “E. Medea”, Bosisio Parini, Italy

    Andrea Facoetti

  3. Department of Psychology, University of Milano-Bicocca, Milan, Italy

    Hermann Bulf

  4. Infant Cognitive Lab, Department of Developmental and Socialization Psychology, University of Padua, Padua, Italy

    Laura Franchin & Eloisa Valenza

  5. Interdepartmental Center for Cognitive Science (CISC), Università degli Studi di Padova, Via Venezia 8, 35131, Padua, Italy

    Eloisa Valenza

  6. Dipartimento di Psicologia dello Sviluppo e della Socializzazione, Università degli Studi di Padova, Via Venezia 8, 35131, Padua, Italy

    Eloisa Valenza

Authors
  1. Luca Ronconi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Andrea Facoetti
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hermann Bulf
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Laura Franchin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Roberta Bettoni
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Eloisa Valenza
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Eloisa Valenza.

Additional information

Luca Ronconi, Andrea Facoetti and Hermann Bulf have contributed equally to this work and have co-first authorship.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ronconi, L., Facoetti, A., Bulf, H. et al. Paternal Autistic Traits are Predictive of Infants Visual Attention. J Autism Dev Disord 44, 1556–1564 (2014). https://doi.org/10.1007/s10803-013-2018-1

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10803-013-2018-1

Keywords

Search

Navigation