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Development of attention from birth to 5 months in infants at risk for autism spectrum disorder

Published online by Cambridge University Press:  23 April 2019

Jessica Bradshaw Open the ORCID record for Jessica Bradshaw [Opens in a new window] ,
Ami Klin ,
Lindsey Evans ,
Cheryl Klaiman ,
Celine Saulnier  and
Courtney McCracken
Jessica Bradshaw*
Affiliation:
Department of Psychology, University of South Carolina, Columbia, SC, USA
Ami Klin
Affiliation:
Marcus Autism Center, Children's Healthcare of Atlanta, Atlanta, GA, USA Department of Pediatrics, Emory University School of Medicine, Atlanta, GA, USA
Lindsey Evans
Affiliation:
Department of Psychology, Illinois Institute of Technology, Chicago, IL, USA
Cheryl Klaiman
Affiliation:
Marcus Autism Center, Children's Healthcare of Atlanta, Atlanta, GA, USA Department of Pediatrics, Emory University School of Medicine, Atlanta, GA, USA
Celine Saulnier
Affiliation:
Department of Pediatrics, Emory University School of Medicine, Atlanta, GA, USA
Courtney McCracken
Affiliation:
Emory-Children's-Georgia Tech Pediatric Research Alliance, Atlanta, USA
*
Author for correspondence: Jessica Bradshaw, Department of Psychology, University of South Carolina, 1512 Pendleton St., Barnwell College, Suite 220, Columbia, SC29208; E-mail: jbradshaw@sc.edu.
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Abstract

Social-communication skills emerge within the context of rich social interactions, facilitated by an infant's capacity to attend to people and objects in the environment. Disruption in this early neurobehavioral process may decrease the frequency and quality of social interactions and learning opportunities, potentially leading to downstream deleterious effects on social development. This study examined early attention in infant siblings of children with autism spectrum disorder (ASD) who are at risk for social and communication delays. Visual and auditory attention was mapped from age 1 week to 5 months in infants at familial risk for ASD (high risk; N = 41) and low-risk typically developing infants (low risk; N = 39). At 12 months, a subset of participants (N = 40) was administered assessments of social communication and nonverbal cognitive skills. Results revealed that high-risk infants performed lower on attention tasks at 2 and 3 months of age compared to low-risk infants. A significant association between overall attention at 3 months and developmental outcome at 12 months was observed for both groups. These results provide evidence for early vulnerabilities in visual attention for infants at risk for ASD during a period of important neurodevelopmental transition (between 2 and 3 months) when attention has significant implications for social communication and cognitive development.

Keywords

visual attentionautism spectrum disorderinfancysocial communicationneonate
Type
Regular Articles
Information
Development and Psychopathology , Volume 32 , Issue 2 , May 2020 , pp. 491 - 501
Copyright
Copyright © Cambridge University Press 2019

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References

American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders (5th ed.). Arlington, VA: Author.Google Scholar
Atkinson, J., & Braddick, O. (2012). Visual attention in the first years: Typical development and developmental disorders. Developmental Medicine and Child Neurology, 54, 589–595. doi:10.1111/j.1469-8749.2012.04294.xCrossRefGoogle ScholarPubMed
Brazelton, T. B., & Nugent, J. (2011). The Neonatal Behavioral Assessment Scale (4th ed.). London: MacKeith Press.Google Scholar
Carpenter, S., Evans, L., Beacham, C., Klaiman, C., & Bradshaw, J. (2017). Longitudinal examination of head control in infants at high and low risk for autism spectrum disorder from two to six months. Paper presented at the International Meeting for Autism Research, San Fransisco, CA.Google Scholar
Chawarska, K., Klin, A., Paul, R., & Volkmar, F. (2007). Autism spectrum disorder in the second year: Stability and change in syndrome expression. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 48, 128–138. doi:10.1111/j.1469-7610.2006.01685.xCrossRefGoogle ScholarPubMed
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. doi:10.1016/j.biopsych.2012.11.022CrossRefGoogle ScholarPubMed
Colombo, J., Mitchell, D. W., Coldren, J. T., & Freeseman, L. J. (1991). Individual differences in infant visual attention: Are short lookers faster processors or feature processors? Child Development, 62, 1247–1257. doi:10.1111/j.1467-8624.1991.tb01603.xCrossRefGoogle ScholarPubMed
Constantino, J. N. (2012). Social Responsiveness Scale (2nd ed.). Los Angeles: Western Psychological Services.Google Scholar
Di Giorgio, E., Frasnelli, E., Rosa Salva, O., Luisa Scattoni, M., Puopolo, M., Tosoni, D., … Vallortigara, G. (2016). Difference in visual social predispositions between newborns at low- and high-risk for autism. Scientific Reports, 6, 26395. doi:10.1038/srep26395CrossRefGoogle ScholarPubMed
Elsabbagh, M., Fernandes, J., Jane Webb, S., Dawson, G., Charman, T., Johnson, M. H., & British Autism Study of Infant Siblings Team. (2013). Disengagement of visual attention in infancy is associated with emerging autism in toddlerhood. Biological Psychiatry, 74, 189–194. doi:10.1016/j.biopsych.2012.11.030CrossRefGoogle ScholarPubMed
Elsabbagh, M., Holmboe, K., Gliga, T., Mercure, E., Hudry, K., Charman, T., … BASIS Team. (2011). Social and attention factors during infancy and the later emergence of autism characteristics. Progress in Brain Research, 189, 195–207. doi:10.1016/B978-0-444-53884-0.00025-7CrossRefGoogle ScholarPubMed
Emde, R. N., & Harmon, R. J. (1972). Endogenous and exogenous smiling systems in early infancy. Journal of the American Academy of Child Psychiatry, 11, 177–200. doi:10.1016/S0002-7138(10)60071-4CrossRefGoogle ScholarPubMed
Frick, J. E., Colombo, J., & Allen, J. R. (2000). Temporal sequence of global-local processing in 3-month-old infants. Infancy, 1, 375–386. doi:10.1207/S15327078IN0103_6CrossRefGoogle Scholar
Gredebäck, G., Fikke, L., & Melinder, A. (2010). The development of joint visual attention: A longitudinal study of gaze following during interactions with mothers and strangers. Developmental Science, 13, 839–848. doi:10.1111/j.1467-7687.2009.00945.xCrossRefGoogle ScholarPubMed
Guthrie, W., Swineford, L. B., Nottke, C., & Wetherby, A. M. (2013). Early diagnosis of autism spectrum disorder: Stability and change in clinical diagnosis and symptom presentation. Journal of Child Psychology and Psychiatry, 54, 582–590.CrossRefGoogle ScholarPubMed
Halit, H., de Haan, M., & Johnson, M. (2003). Cortical specialisation for face processing: Face-sensitive event-related potential components in 3- and 12-month-old infants. NeuroImage, 19, 1180–1193. doi:10.1016/S1053-8119(03)00076-4CrossRefGoogle ScholarPubMed
Hazlett, H. C., Gu, H., Munsell, B. C., Kim, S. H., Styner, M., Wolff, J. J., … Statistical Analysis. (2017). Early brain development in infants at high risk for autism spectrum disorder. Nature, 542, 348–351. doi:10.1038/nature21369CrossRefGoogle ScholarPubMed
Hunnius, S., & Bekkering, H. (2014). What are you doing? How active and observational experience shape infants’ action understanding. Philosophical Transactions of the Royal Society B: Biological Sciences, 369, 20130490–20130490. doi:10.1098/rstb.2013.0490CrossRefGoogle ScholarPubMed
Hunnius, S., Geuze, R. H., & van Geert, P. (2006). Associations between the developmental trajectories of visual scanning and disengagement of attention in infants. Infant Behavior and Development, 29, 108–125. doi:10.1016/J.INFBEH.2005.08.007CrossRefGoogle ScholarPubMed
Iverson, J. M. (2010). Developing language in a developing body: The relationship between motor development and language development. Journal of Child Language, 37, 229. doi:10.1017/S0305000909990432CrossRefGoogle Scholar
Johnson, M. H. (1990). Cortical maturation and the development of visual attention in early infancy. Journal of Cognitive Neuroscience, 2(2), 81–95. doi:10.1162/jocn.1990.2.2.81CrossRefGoogle ScholarPubMed
Johnson, M. H. (2005). Subcortical face processing. Nature Reviews Neuroscience, 6, 766–774. doi:10.1038/nrn1766CrossRefGoogle ScholarPubMed
Johnson, M. H. (2014). Autism: Demise of the innate social orienting hypothesis. Current Biology, 24, R30–R31. doi:10.1016/j.cub.2013.11.021CrossRefGoogle ScholarPubMed
Johnson, M. H., Griffin, R., Csibra, G., Halit, H., Farroni, T., De Haan, M., … Richards, J. (2005). The emergence of the social brain network: Evidence from typical and atypical development. Development and Psychopathology, 17, 599–619. doi:10.1017/S0954579405050297CrossRefGoogle ScholarPubMed
Jones, E., Gliga, T., Bedford, R., Charman, T., & Johnson, M. (2014). Developmental pathways to autism: A review of prospective studies of infants at risk. Neuroscience & Biobehavioral Reviews, 39, 1–33. doi:10.1016/j.neubiorev.2013.12.001CrossRefGoogle ScholarPubMed
Jones, E., Venema, K., Earl, R., Lowy, R., Barnes, K., Estes, A., … Webb, S. J. (2016). Reduced engagement with social stimuli in 6-month-old infants with later autism spectrum disorder: A longitudinal prospective study of infants at high familial risk. Journal of Neurodevelopmental Disorders, 8, 7. doi:10.1186/s11689-016-9139-8CrossRefGoogle ScholarPubMed
Jones, W., & Klin, A. (2013). Attention to eyes is present but in decline in 2–6-month-old infants later diagnosed with autism. Nature, 504, 427–431. doi:10.1038/nature12715CrossRefGoogle ScholarPubMed
Kanakogi, Y., & Itakura, S. (2011). Developmental correspondence between action prediction and motor ability in early infancy. Nature Communications, 2, 341. doi:10.1038/ncomms1342CrossRefGoogle ScholarPubMed
Klin, A., Shultz, S., & Jones, W. (2015). Social visual engagement in infants and toddlers with autism: Early developmental transitions and a model of pathogenesis. Neuroscience & Biobehavioral Reviews, 50, 189–203. doi:10.1016/j.neubiorev.2014.10.006CrossRefGoogle Scholar
Lavelli, M., & Fogel, A. (2005). Developmental changes in the relationship between the infant's attention and emotion during early face-to-face communication: The 2-month transition. Developmental Psychology, 41, 265–280. doi:10.1037/0012-1649.41.1.265CrossRefGoogle ScholarPubMed
LeBarton, E. S., & Iverson, J. M. (2013). Fine motor skill predicts expressive language in infant siblings of children with autism. Developmental Science, 16, 815–827. doi:10.1111/desc.12069Google ScholarPubMed
Lester, B. M., Andreozzi-Fontaine, L., Tronick, E., & Bigsby, R. (2014). Assessment and evaluation of the high risk neonate: The NICU Network Neurobehavioral Scale. Journal of Visualized Experiments, 90. doi:10.3791/3368Google Scholar
Lester, B. M., & Tronick, E. Z. (2005). NICU Network Neurobehavioral Scale (NNNS) Manual. Baltimore, MD: Brookes.Google Scholar
Libertus, K., & Needham, A. (2011). Reaching experience increases face preference in 3-month-old infants. Developmental Science, 14, 1355–1364. doi:10.1111/j.1467-7687.2011.01084.xCrossRefGoogle ScholarPubMed
Lloyd-Fox, S., Wu, R., Richards, J. E., Elwell, C. E., & Johnson, M. H. (2015). Cortical activation to action perception is associated with action production abilities in young infants. Cerebral Cortex, 25, 289–297. doi:10.1093/cercor/bht207CrossRefGoogle ScholarPubMed
Lord, C., Risi, S., Lambrecht, L., Cook, E. H., Leventhal, B., DiLavore, P., … Rutter, M. (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.CrossRefGoogle ScholarPubMed
Lord, C., Rutter, M., DiLavore, P., Risi, S., Gotham, K., & Bishop, S. (2012). Autism Diagnostic Observation Schedule: ADOS-2. Torrance, CA: Western Psychological Services.Google Scholar
Messinger, D., Young, G. S., Ozonoff, S., Dobkins, K., Carter, A., Zwaigenbaum, L., … Sigman, M. (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. doi:10.1016/j.jaac.2012.12.011CrossRefGoogle Scholar
Morton, J., & Johnson, M. H. (1991). CONSPEC and CONLERN: A two-process theory of infant face recognition. Psychological Review, 98, 164–181.CrossRefGoogle ScholarPubMed
Mous, S. E., Jiang, A., Agrawal, A., & Constantino, J. N. (2017). Attention and motor deficits index non-specific background liabilities that predict autism recurrence in siblings. Journal of Neurodevelopmental Disorders, 9, 32. doi:10.1186/s11689-017-9212-yCrossRefGoogle ScholarPubMed
Mullen, E. M. (1995). Mullen Scales of Early Learning: AGS edition. Circle Pines, MN: American Guidance Service.Google Scholar
Mundy, P., Sullivan, L., & Mastergeorge, A. M. (2009). A parallel and distributed-processing model of joint attention, social cognition and autism. Autism Research, 2, 2–21. doi:10.1002/aur.61CrossRefGoogle ScholarPubMed
Nakano, T., & Nakatani, K. (2014). Cortical networks for face perception in two-month-old infants. Proceedings of the Royal Society Part B: Biological Sciences, 281, 20141468. doi:10.1098/rspb.2014.1468CrossRefGoogle ScholarPubMed
Needham, A., Barrett, T., & Peterman, K. (2002). A pick-me-up for infants’ exploratory skills: Early simulated experiences reaching for objects using “sticky mittens” enhances young infants’ object exploration skills. Infant Behavior and Development, 25, 279–295. doi:10.1016/S0163-6383(02)00097-8CrossRefGoogle Scholar
Noble, Y., & Boyd, R. (2012). Neonatal assessments for the preterm infant up to 4 months corrected age: A systematic review. Developmental Medicine & Child Neurology, 54, 129–139. doi:10.1111/j.1469-8749.2010.03903.xCrossRefGoogle ScholarPubMed
Ozonoff, S., Young, G. S., Belding, A., Hill, M., Hill, A., Hutman, T., … Iosif, A.-M. (2014). The broader autism phenotype in infancy: When does it emerge? Journal of the American Academy of Child & Adolescent Psychiatry, 53, 398–407. doi:10.1016/j.jaac.2013.12.020CrossRefGoogle ScholarPubMed
Ozonoff, S., Young, G. S., Carter, A., Messinger, D., Yirmiya, N., Zwaigenbaum, L., … Stone, W. L. (2011). Recurrence risk for autism spectrum disorders: A baby siblings research consortium study. Pediatrics, 128, e488–e495.Google ScholarPubMed
Ozonoff, S., Young, G. S., Landa, R. J., Brian, J., Bryson, S., Charman, T., … Iosif, A.-M. (2015). Diagnostic stability in young children at risk for autism spectrum disorder: A baby siblings research consortium study. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 56, 988–998. doi:10.1111/jcpp.12421CrossRefGoogle ScholarPubMed
Perra, O., & Gattis, M. (2010). The control of social attention from 1 to 4 months. British Journal of Developmental Psychology, 28, 891–908. doi:10.1348/026151010X487014CrossRefGoogle ScholarPubMed
Perra, O., & Gattis, M. (2012). Attention engagement in early infancy. Infant Behavior and Development, 35, 635–644. doi:10.1016/J.INFBEH.2012.06.004CrossRefGoogle ScholarPubMed
Richards, J. E., Reynolds, G. D., & Courage, M. L. (2010). The neural bases of infant attention. Current Directions in Psychological Science, 19, 41–46. doi:10.1177/0963721409360003CrossRefGoogle ScholarPubMed
Rochat, P. (1989). Object manipulation and exploration in 2- to 5-month-old infants. Developmental Psychology, 25, 871–884. doi:10.1037/0012-1649.25.6.871CrossRefGoogle Scholar
Rochat, P. (1993). Hand-mouth coordination in the newborn: Morphology, determinants, and early development of a basic act. Advances in Psychology, 97, 265–288. doi:10.1016/S0166-4115(08)60956-5CrossRefGoogle Scholar
Rochat, P. R. (2001). Social contingency detection and infant development. Bulletin of the Menninger Clinic; Summer, 65, 347–360.CrossRefGoogle ScholarPubMed
Ross-Sheehy, S., Perone, S., Macek, K. L., & Eschman, B. (2017). Visual orienting and attention deficits in 5- and 10-month-old preterm infants. Infant Behavior and Development, 46, 80–90. doi:10.1016/j.infbeh.2016.12.004CrossRefGoogle ScholarPubMed
Ruff, H. A., Saltarelli, L. M., Capozzoli, M., & Dubiner, K. (1992). The differentiation of activity in infants’ exploration of objects. Developmental Psychology, 28, 851–861.CrossRefGoogle Scholar
Rutter, M., Bailey, A., & Lord, C. (2003). Social Communication Questionnaire (SCQ). Torrance, CA: Western Psychological Services.Google Scholar
Salley, B., Sheinkopf, S. J., Neal-Beevers, A. R., Tenenbaum, E. J., Miller-Loncar, C. L., Tronick, E., … Lester, B. M. (2016). Infants’ early visual attention and social engagement as developmental precursors to joint attention. Developmental Psychology, 52, 1721–1731. doi:10.1037/dev0000205CrossRefGoogle ScholarPubMed
Senju, A., & Johnson, M. H. (2009). The eye contact effect: Mechanisms and development. Trends in Cognitive Sciences, 13, 127–134. doi:10.1016/j.tics.2008.11.009CrossRefGoogle ScholarPubMed
Senju, A., & Tomalski, P. (2015). The two-process theory of face processing: Modifications based on two decades of data from infants and adults. Neuroscience & Biobehavioral Reviews, 50, 169–179. doi:10.1016/j.neubiorev.2014.10.009Google Scholar
Shic, F., Macari, S., & Chawarska, K. (2014). Speech disturbs face scanning in 6-month-old infants who develop autism spectrum disorder. Biological Psychiatry, 75, 231–237. doi:10.1016/j.biopsych.2013.07.009CrossRefGoogle ScholarPubMed
Shultz, S., Klin, A., & Jones, W. (2018). Neonatal transitions in social behavior and their implications for autism. Trends in Cognitive Sciences, 22, 452–469. doi:10.1016/j.tics.2018.02.012CrossRefGoogle ScholarPubMed
Soska, K. C., Adolph, K. E., & Johnson, S. P. (2010). Systems in development: Motor skill acquisition facilitates three-dimensional object completion. Developmental Psychology, 46, 129–138. doi:10.1037/a0014618CrossRefGoogle ScholarPubMed
Striano, T., Stahl, D., Cleveland, A., & Hoehl, S. (2007). Sensitivity to triadic attention between 6 weeks and 3 months of age. Infant Behavior and Development, 30, 529–534. doi:10.1016/J.INFBEH.2006.12.010CrossRefGoogle ScholarPubMed
Tronick, E., & Lester, B. M. (2013). Grandchild of the NBAS: The NICU Network Neurobehavioral Scale (NNNS): A review of the research using the NNNS. Journal of Child and Adolescent Psychiatric Nursing, 26, 193–203. doi:10.1111/jcap.12042CrossRefGoogle ScholarPubMed
von Hofsten, C. (2004). An action perspective on motor development. Trends in Cognitive Sciences, 8, 266–272. doi:10.1016/j.tics.2004.04.002CrossRefGoogle ScholarPubMed
von Hofsten, C., & Rosander, K. (1996). The development of gaze control and predictive tracking in young infants. Vision Research, 36, 81–96.CrossRefGoogle ScholarPubMed
Wetherby, A. M., & Prizant, B. M. (2002). Communication and Symbolic Behavior Scales: Developmental profile. Baltimore, MD: Brookes.Google ScholarPubMed
Wolf, M.-J., Koldewijn, K., Beelen, A., Smit, B., Hedlund, R., & Groot, I. (2007). Neurobehavioral and developmental profile of very low birthweight preterm infants in early infancy. Acta Paediatrica, 91, 930–938. doi:10.1111/j.1651-2227.2002.tb02858.xCrossRefGoogle Scholar