Abstract
Infants show shifting patterns of visual engagement to faces over the first years of life. To explore the adaptive implications of this engagement, we collected eye-tracking measures on cross-sectional samples of 10–25-month-old typically developing toddlers (TD;N = 28) and those with autism spectrum disorder (ASD;N = 54). Concurrent language assessments were conducted and relationships between visual engagement and expressive and receptive language were analyzed between groups, and within ASD subgroups. TD and ASD toddlers exhibited greater mouth- than eye-looking, with TD exhibiting higher levels of mouth-looking than ASD. Mouth-looking was positively associated with expressive language in TD toddlers, and in ASD toddlers who had acquired first words. Mouth-looking was unrelated to expressive language in ASD toddlers who had not yet acquired first words.
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Notes
Nonverbal developmental quotient = {[(Fine Motor Age Equivalent Score + Visual Reception Age Equivalent Score)/2]/Chronological Age (months)}*100.
Note that this analysis was both hypothesized to be of importance—and only possible—within the ASD sample as only 3 of our TD toddlers had not yet acquired first words.
Associations between eye- and mouth-looking in the ASD-Words and ASD-No Words subgroups were similar to that of the overall ASD and TD groups (ASD-Words r = − 0.80, p < .001; ASD-No Words r = − 0.82, p < .001, respectively).
Although preliminary analyses to formally test for this variation (one-way ANOVAs of eye- and mouth-looking by Mullen expressive item 11 score) found no significant effects (TD-eye: F(2,21) = 0.94, p = 0.406; TD-mouth: F(2,21) = 1.34, p = 0.284; ASD-eye: F(3,47) = 1.23, p = 0.310; ASD-mouth: F(3,47) = 0.72, p = 0.547) we retain this limitation as we might be underpowered to detect effects when splitting our samples into the 4 Mullen expressive language item 11 categories, particularly in the case of our 28 TD toddlers.
References
American Psychiatric Association [APA]. (2013). Diagnostic and statistical manual of mental disorders (5th ed.). American Psychiatric Association.
Bard, K., Myowa-Yamakoshi, M., Tomonaga, M., & Tanaka, M. (2005). Group differences in the mutual gaze of chimpanzees (Pan troglodytes). Developmental Psychology, 41(4), 616–624. https://doi.org/10.1037/0012-1649.41.4.616.
Bedford, R., Jones, E. J. H., Johnson, M. H., Pickles, A., Charman, T., & Gliga, T. (2016). Sex differences in the association between infant markers and later autistic traits. Molecular Autism. https://doi.org/10.1186/s13229-016-0081-0.
Bloom, L. (1991). Language development from two to three. Cambridge: Cambridge University Press.
Boraston, Z., & Blakemore, S.-J. (2007). The application of eye-tracking technology in the study of autism. The Journal of Physiology, 581(3), 893–898. https://doi.org/10.1113/jphysiol.2007.133587.
Brooks, R., & Meltzoff, A. N. (2005). The development of gaze following and its relation to language. Developmental Science, 8(6), 535–543. https://doi.org/10.1111/j.1467-7687.2005.00445.x.
Brooks, R., & Meltzoff, A. N. (2008). Infant gaze following and pointing predict accelerated vocabulary growth through two years of age: a longitudinal, growth curve modeling study. Journal of Child Language, 35, 207–220. https://doi.org/10.1017/S030500090700829X.
Bruner, J. (1981). The social context of language acquisition. Language & Communication, 1(2–3), 155–178. https://doi.org/10.1016/0271-5309(81)90010-0.
Bryant, G. A., & Barrett, H. C. (2007). Recognizing intentions in infant-directed speech. Psychological Science, 18(8), 746–751. https://doi.org/10.1111/j.1467-9280.2007.01970.x.
Campbell, D. J., Shic, F., Macari, S., & Chawarska, K. (2014). Gaze response to dyadic bids at 2 years related to outcomes at 3 years in autism spectrum disorders: A subtyping analysis. Journal of Autism and Developmental Disorders, 44(2), 431–442. https://doi.org/10.1007/s10803-013-1885-9.
Chawarska, K., Macari, S., Powell, K., DiNicola, L., & Shic, F. (2016). Enhanced social attention in female infant siblings at risk for autism. Journal of the American Academy of Child and Adolescent Psychiatry, 55(3), 188–195. https://doi.org/10.1016/j.jaac.2015.11.016.
Chawarska, K., Macari, S., & Shic, F. (2012). Context modulates attention to social scenes in toddlers with autism. Journal of Child Psychology and Psychiatry and Allied Disciplines, 53(8), 903–913. https://doi.org/10.1111/j.1469-7610.2012.02538.x.
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(3), 195–203. https://doi.org/10.1016/J.BIOPSYCH.2012.11.022.
Chawarska, K., & Shic, F. (2009). Looking but not seeing: atypical visual scanning and recognition of faces in 2 and 4-year-old children with autism spectrum disorder. Journal of Autism and Developmental Disorders, 39(12), 1663–1672. https://doi.org/10.1007/s10803-009-0803-7.
Chita-Tegmark, M. (2016). Social attention in ASD: A review and meta-analysis of eye-tracking studies. Research in Developmental Disabilities, 48, 79–93. https://doi.org/10.1016/J.RIDD.2015.10.011.
Clark, E. V. (2009). First Language acquisition (2nd ed.). Cambridge: Cambridge University Press.
Emery, N. J. (2000). The eyes have it: The neuroethology, function and evolution of social gaze. Neuroscience & Biobehavioral Reviews, 24(6), 581–604. https://doi.org/10.1016/S0149-7634(00)00025-7.
Falck-Ytter, T., Bölte, S., & Gredebäck, G. (2013). Eye tracking in early autism research. Journal of Neurodevelopmental Disorders, 5(1), 28. https://doi.org/10.1186/1866-1955-5-28.
Farroni, T., Csibra, G., Simion, F., & Johnson, M. H. (2002). Eye contact detection in humans from birth. Proceedings of the National Academy of Sciences of the United States of America, 99(14), 9602–9605. https://doi.org/10.1073/pnas.152159999.
Fernald, A., Perfors, A., & Marchman, V. A. (2006). Picking up speed in understanding: Speech processing efficiency and vocabulary growth across the 2nd year. Developmental Psychology, 42(1), 98–116. https://doi.org/10.1037/0012-1649.42.1.98.
Fox, J. (2016). Applied regression analysis and generalized linear models (3rd ed.). Thousand Oaks, CA: SAGE Publications Inc.
Geschwind, D. H., & State, M. W. (2015). Gene hunting in autism spectrum disorder: On the path to precision medicine. The Lancet Neurology, 14(11), 1109–1120. https://doi.org/10.1016/S1474-4422(15)00044-7.
Gliga, T., & Csibra, G. (2007). Seeing the face through the eyes: A developmental perspective on face expertise. Progress in Brain Research. https://doi.org/10.1016/S0079-6123(07)64018-7.
Goldstein, M. H., King, A. P., & West, M. J. (2003). Social interaction shapes babbling: Testing parallels between birdsong and speech. Proceedings of the National Academy of Sciences, 100(13), 8030–8035.
Guillon, Q., Hadjikhani, N., Baduel, S., & Rogé, B. (2014). Visual social attention in autism spectrum disorder: Insights from eye tracking studies. Neuroscience & Biobehavioral Reviews, 42, 279–297. https://doi.org/10.1016/J.NEUBIOREV.2014.03.013.
Hillairet de Boisferon, A., Tift, A. H., Minar, N. J., & Lewkowicz, D. J. (2018). The redeployment of attention to the mouth of a talking face during the second year of life. Journal of Experimental Child Psychology, 172, 189–200. https://doi.org/10.1016/J.JECP.2018.03.009.
Hosozawa, M., Tanaka, K., Shimizu, T., Nakano, T., & Kitazawa, S. (2012). How children with specific language impairment view social situations: An eye tracking study. Pediatrics, 129(6), e1453–e1460. https://doi.org/10.1542/peds.2011-2278.
Johnels, J. Å., Gillberg, C., Falck-Ytter, T., & Miniscalco, C. (2014). Face-viewing patterns in young children with autism spectrum disorders: Speaking up for the role of language comprehension. Journal of Speech, Language, and Hearing Research, 57(6), 2246–2252. https://doi.org/10.1044/2014_JSLHR-L-13-0268.
Jones, R. M., & Lord, C. (2013). Diagnosing autism in neurobiological research studies. Behavioural Brain Research, 251, 113–124. https://doi.org/10.1016/J.BBR.2012.10.037.
Jones, W., Carr, K., & Klin, A. (2008). Absence of preferential looking to the eyes of approaching adults predicts level of social disability in 2-year-old toddlers with autism spectrum disorder. Archives of General Psychiatry, 65(8), 946. https://doi.org/10.1001/archpsyc.65.8.946.
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(7480), 427–431. https://doi.org/10.1038/nature12715.
Kjelgaard, M. M., & Tager-Flusberg, H. (2001). An investigation of language impairment in autism: Implications for genetic subgroups. Language and Cognitive Processes, 16(2–3), 287–308. https://doi.org/10.1080/01690960042000058.
Kleinke, C. L. (1986). Gaze and eye contact: A research review. Psychological Bulletin, 100(1), 78–100. https://doi.org/10.1037/0033-2909.100.1.78.
Klin, A., & Jones, W. (2008). Altered face scanning and impaired recognition of biological motion in a 15-month-old infant with autism. Developmental Science, 11(1), 40–46. https://doi.org/10.1111/j.1467-7687.2007.00608.x.
Klin, A., & Jones, W. (2015). Measurement and mismeasurement of social development in infants later diagnosed with autism spectrum disorder. International Journal of Statistics in Medical Research, 4(2), 180–187. https://doi.org/10.6000/1929-6029.2015.04.02.3.
Klin, A., Jones, W., Schultz, R., & Volkmar, F. (2003). The enactive mind, or from actions to cognition: Lessons from autism. Philosophical Transactions of the Royal Society B, 358, 345–360. https://doi.org/10.1098/rstb.2002.1202.
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. https://doi.org/10.1001/archpsyc.59.9.809.
Klin, A., Lin, D. J., Gorrindo, P., Ramsay, G., & Jones, W. (2009). Two-year-olds with autism orient to non-social contingencies rather than biological motion. Nature, 459(7244), 257–261. https://doi.org/10.1038/nature07868.
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. https://doi.org/10.1016/J.NEUBIOREV.2014.10.006.
Kuhl, P. K. (2004). Early language acquisition: Cracking the speech code. Nature Reviews Neuroscience, 5(11), 831–843. https://doi.org/10.1038/nrn1533.
Lewkowicz, D. J., & Hansen-Tift, A. M. (2012). Infants deploy selective attention to the mouth of a talking face when learning speech. Proceedings of the National Academy of Sciences of the United States of America, 109(5), 1431–1436. https://doi.org/10.1073/pnas.1114783109.
Lord, C. (2012). Autism diagnostic observation schedule (2nd ed.). Los Angeles, CA: Western Psychological Services.
Mody, M., & Belliveau, J. W. (2012). Speech and language impairments in autism: Insights from behavior and neuroimaging. American Chinese Journal of Medicine and Science, 5(3), 157. https://doi.org/10.7156/v5i3p157.
Morales, M., Mundy, P., Delgado, C. E. F., Yale, M., Messinger, D., Neal, R., et al. (2000). Responding to joint attention across the 6- through 24-month age period and early language acquisition. Journal of Applied Developmental Psychology, 21(3), 283–298. https://doi.org/10.1016/S0193-3973(99)00040-4.
Mullen, E. (1995). Mullen scales of early learning (AGS ed.). Circle Pines, MN: AGS.
Nakano, T., Tanaka, K., Endo, Y., Yamane, Y., Yamamoto, T., Nakano, Y., … Kitazawa, S. (2010). Atypical gaze patterns in children and adults with autism spectrum disorders dissociated from developmental changes in gaze behaviour. Proceedings of the Royal Society B: Biological Sciences, 277(1696), 2935. https://doi.org/10.1098/RSPB.2010.0587
Rice, K., Moriuchi, J. M., Jones, W., & Klin, A. (2012). Parsing heterogeneity in autism spectrum disorders: Visual scanning of dynamic social scenes in school-aged children. Journal of the American Academy of Child and Adolescent Psychiatry, 51(3), 238–248. https://doi.org/10.1016/j.jaac.2011.12.017.
Senju, A., & Johnson, M. H. (2009). The eye contact effect: mechanisms and development. Trends in Cognitive Sciences, 13(3), 127–134. https://doi.org/10.1016/J.TICS.2008.11.009.
Shic, F., Bradshaw, J., Klin, A., Scassellati, B., & Chawarska, K. (2011). Limited activity monitoring in toddlers with autism spectrum disorder. Brain Research, 1380, 246–254. https://doi.org/10.1016/J.BRAINRES.2010.11.074.
StataCorp., (2017). Stata statistical software: Release 15. College Station, TX: StataCorp LLC.
Tager-Flusberg, H., Paul, R., & Lord, C. (2005). Language and communication in autism. Handbook of Autism and Pervasive Developmental Disorders, 1, 335–364.
Teinonen, T., Aslin, R. N., Alku, P., & Csibra, G. (2008). Visual speech contributes to phonetic learning in 6-month-old infants. Cognition, 108(3), 850–855. https://doi.org/10.1016/J.COGNITION.2008.05.009.
Tenenbaum, E. J., Amso, D., Abar, B., & Sheinkopf, S. J. (2014). Attention and word learning in autistic, language delayed and typically developing children. Frontiers in Psychology, 5, 490. https://doi.org/10.3389/fpsyg.2014.00490.
Tenenbaum, E. J., Amso, D., Righi, G., & Sheinkopf, S. J. (2017). Attempting to “Increase Intake from the Input”: Attention and word learning in children with autism. Journal of Autism and Developmental Disorders, 47(6), 1791–1805. https://doi.org/10.1007/s10803-017-3098-0.
Tenenbaum, E. J., Sobel, D. M., Sheinkopf, S. J., Malle, B. F., & Morgan, J. L. (2015). Attention to the mouth and gaze following in infancy predict language development. Journal of Child Language, 42(6), 1173–1190. https://doi.org/10.1017/S0305000914000725.
Tomasello, M. (1988). The role of joint attentional processes in early language development. Language Sciences, 10(1), 69–88. https://doi.org/10.1016/0388-0001(88)90006-X.
Trevarthen, C. (1998). The concept and foundations of infant intersubjectivity. In S. Bråten (Ed.), Intersubjective communication and emotion in early ontogeny (pp. 15–46). Cambridge: Cambridge University Press.
Tsang, T., Atagi, N., & Johnson, S. P. (2018). Selective attention to the mouth is associated with expressive language skills in monolingual and bilingual infants. Journal of Experimental Child Psychology, 169, 93–109. https://doi.org/10.1016/J.JECP.2018.01.002.
Wallentin, M. (2008). Putative sex differences in verbal abilities and language cortex: A critical review. Brain and Language. https://doi.org/10.1016/j.bandl.2008.07.001.
Weikum, W. M., Vouloumanos, A., Navarra, J., Soto-Faraco, S., Sebastián-Gallés, N., & Werker, J. F. (2007). Visual language discrimination in infancy. Science, 316(5828), 1159. https://doi.org/10.1126/science.1137686.
Young, G. S., Merin, N., Rogers, S. J., & Ozonoff, S. (2009). Gaze Behavior and affect at 6-months: predicting clinical outcomes and language development in typically developing infants and infants at-risk for autism. Developmental Science, 12(5), 798–814. https://doi.org/10.1111/j.1467-7687.2009.00833.x.
Acknowledgments
This study was supported by grants from the National Institute of Child Health and Human Development (K99 HD097290, L.A.E.), National Institute of Mental Health (P50 MH081756 and P50 MH100029), Georgia Research Alliance, Marcus Foundation, J.B. Whitehead Foundation, and Simons Foundation (A.K., W.J.). We thank the families and children for their time and participation. We also thank Sarah Shultz and Jennifer Moriuchi for discussions of concepts and methods; David Lin, Kelley Knoch, Katelin Carr, Phil Gorrindo, Anna Krasno, Casey Zampella, Jessie Northrup, Jennings Xu, Katherine Rice, José Paredes and Peter Lewis for their help with data collection; and Kasia Chawarska, Rhea Paul, Suzanne Macari, Amy Carney, Tina Goldsmith, Amanda Steiner, Grace Gengoux, Diane Goudreau, Erin Loring, James McGrath, and Abha Gupta for their contributions to the clinical characterization of a portion of the samples
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Habayeb, S., Tsang, T., Saulnier, C. et al. Visual Traces of Language Acquisition in Toddlers with Autism Spectrum Disorder During the Second Year of Life. J Autism Dev Disord 51, 2519–2530 (2021). https://doi.org/10.1007/s10803-020-04730-x
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DOI: https://doi.org/10.1007/s10803-020-04730-x