Infant and Adult Brains Are Coupled to the Dynamics of Natural Communication

Infancy is the foundational period for learning from adults, and the dynamics of the social environment have long been considered central to children’s development. Here, we reveal a novel, naturalistic approach for studying live interactions between infants and adults. Using functional near-infrared spectroscopy (fNIRS), we simultaneously and continuously measured the brains of infants (N = 18; 9–15 months of age) and an adult while they communicated and played with each other. We found that time-locked neural coupling within dyads was significantly greater when dyad members interacted with each other than with control individuals. In addition, we characterized the dynamic relationship between neural activation and the moment-to-moment fluctuations of mutual gaze, joint attention to objects, infant emotion, and adult speech prosody. This investigation advances what is currently known about how the brains and behaviors of infants both shape and reflect those of adults during real-life communication.

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References:

Arichi, T., Fagiolo, G., Varela, M., Melendez-Calderon, A., Allievi, A., Merchant, N., . . . Edwards, A. D. (2012). Development of BOLD signal hemodynamic responses in the human brain. NeuroImage, 63, 663–673.
Google Scholar | Crossref | Medline | ISI

 

Boas, D. A., Elwell, C. E., Ferrari, M., Taga, G. (2014). Twenty years of functional near-infrared spectroscopy: Introduction for the special issue. NeuroImage, 85, 1–5.
Google Scholar | Crossref | Medline | ISI
Boersma, P., Weenink, D. (2009). Praat: Doing phonetics by computer (Version 6.0.41) [Computer software]. Retrieved from http://www.praat.org/
Google Scholar
Brand, R. J., Baldwin, D. A., Ashburn, L. A. (2002). Evidence for ‘motionese’: Modifications in mothers’ infant-directed action. Developmental Science, 5, 72–83.
Google Scholar | Crossref | ISI
Brazelton, T. B., Koslowski, B., Main, M. (1974). The origins of reciprocity: The early mother-infant interaction. In Lewis, M., Rosenblum, L. A. (Eds.), The effect of the infant on its caregiver (pp. 49–76). Oxford, England: Wiley-Interscience.
Google Scholar
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.
Google Scholar | Crossref | Medline | ISI
Byrge, L., Sporns, O., Smith, L. B. (2014). Developmental process emerges from extended brain-body-behavior networks. Trends in Cognitive Sciences, 18, 395–403.
Google Scholar | Crossref | Medline | ISI
Cohn, J. F., Tronick, E. Z. (1988). Mother-infant face-to-face interaction: Influence is bidirectional and unrelated to periodic cycles in either partner’s behavior. Developmental Psychology, 24, 386–392.
Google Scholar | Crossref | ISI
Cronbach, L. J. (1951). Coefficient alpha and the internal structure of tests. Psychometrika, 16, 297–334.
Google Scholar | Crossref
Dikker, S., Silbert, L. J., Hasson, U., Zevin, J. D. (2014). On the same wavelength: Predictable language enhances speaker-listener brain-to-brain synchrony in posterior superior temporal gyrus. The Journal of Neuroscience, 34, 6267–6272.
Google Scholar | Crossref | Medline
Elsabbagh, M., Volein, A., Csibra, G., Holmboe, K., Garwood, H., Tucker, L., . . . Johnson, M. H. (2009). Neural correlates of eye gaze processing in the infant broader autism phenotype. Biological Psychiatry, 65, 31–38.
Google Scholar | Crossref | Medline | ISI
Emberson, L. L., Boldin, A. M., Robertson, C. E., Cannon, G., Aslin, R. N. (2018). Expectation affects neural repetition suppression in infancy. Developmental Cognitive Neuroscience, 37, Article 100597. doi:10.1016/j.dcn.2018.11.001
Google Scholar | Crossref | Medline
Ferguson, B., Lew-Williams, C. (2016). Communicative signals support abstract rule learning by 7-month-old infants. Scientific Reports, 6, Article 25434. doi:10.1038/srep25434
Google Scholar | Crossref
Fernald, A., Kuhl, P. (1987). Acoustic determinants of infant preference for motherese speech. Infant Behavior and Development, 10, 279–293.
Google Scholar | Crossref | ISI
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, USA, 100, 8030–8035.
Google Scholar | Crossref | Medline | ISI
Hasson, U., Ghazanfar, A. A., Galantucci, B., Garrod, S., Keysers, C. (2012). Brain-to-brain coupling: A mechanism for creating and sharing a social world. Trends in Cognitive Sciences, 16, 114–121.
Google Scholar | Crossref | Medline | ISI
Hirsch, J., Zhang, X., Noah, J. A., Ono, Y. (2017). Frontal temporal and parietal systems synchronize within and across brains during live eye-to-eye contact. NeuroImage, 157, 314–330.
Google Scholar | Crossref | Medline
Honey, C. J., Thompson, C. R., Lerner, Y., Hasson, U. (2012). Not lost in translation: Neural responses shared across languages. The Journal of Neuroscience, 32, 15277–15283.
Google Scholar | Crossref | Medline
Janata, P., Birk, J. L., Van Horn, J. D., Leman, M., Tillmann, B., Bharucha, J. (2002). The cortical topography of tonal structures underlying Western music. Science, 298, 2167–2170.
Google Scholar | Crossref | Medline | ISI
Jiang, J., Dai, B., Peng, D., Zhu, C., Liu, L., Lu, C. (2012). Neural synchronization during face-to-face communication. The Journal of Neuroscience, 45, 16064–16069.
Google Scholar | Crossref
Leong, V., Byrne, E., Clackson, K., Georgieva, S., Lam, S., Wass, S. (2017). Speaker gaze increases information coupling between infant and adult brains. Proceedings of the National Academy of Sciences, USA, 114, 13290–13295.
Google Scholar | Crossref | Medline
Lerner, Y., Honey, C. J., Silbert, L. J., Hasson, U. (2011). Topographic mapping of a hierarchy of temporal receptive windows using a narrated story. The Journal of Neuroscience, 31, 2906–2915.
Google Scholar | Crossref | Medline | ISI
Liu, Y., Piazza, E. A., Simony, E., Shewokis, P. A., Onaral, B., Hasson, U., Ayaz, H. (2017). Measuring speaker–listener neural coupling with functional near infrared spectroscopy. Scientific Reports, 7, Article 43293. doi:10.1038/srep43293
Google Scholar | Crossref
Marsh, K. L., Richardson, M. J., Schmidt, R. C. (2009). Social connection through joint action and interpersonal coordination. Topics in Cognitive Science, 1, 320–339.
Google Scholar | Crossref | Medline | ISI
Piazza, E. A., Iordan, M. C., Lew-Williams, C. (2017). Mothers consistently alter their unique vocal fingerprints when communicating with infants. Current Biology, 27, 3162–3167.
Google Scholar | Crossref | Medline
Regev, M., Simony, E., Lee, K., Tan, K. M., Chen, J., Hasson, U. (2019). Propagation of information along the cortical hierarchy as a function of attention while reading and listening to stories. Cerebral Cortex, 29, 4017–4034. doi:10.1093/cercor/bhy282
Google Scholar | Crossref | Medline
Ryan, B. P. (2000). Speaking rate, conversational speech acts, interruption, and linguistic complexity of 20 pre-school stuttering and non-stuttering children and their mothers. Clinical Linguistics & Phonetics, 14, 25–51.
Google Scholar | Crossref | Medline | ISI
Sameroff, A. (2009). The transactional model. In Sameroff, A. (Ed.), The transactional model of development: How children and contexts shape each other (pp. 3–21). Washington, DC: American Psychological Association.
Google Scholar | Crossref
Scholkmann, F., Spichtig, S., Muehlemann, T., Wolf, M. (2010). How to detect and reduce movement artifacts in near-infrared imaging using moving standard deviation and spline interpolation. Physiological Measurement, 31, 649–662.
Google Scholar | Crossref | Medline | ISI
Simony, E., Honey, C. J., Chen, J., Lositsky, O., Yeshurun, Y., Wiesel, A., Hasson, U. (2016). Dynamic reconfiguration of the default mode network during narrative comprehension. Nature Communications, 7, Article 12141. doi:10.1038/ncomms12141
Google Scholar | Crossref | Medline
Smith, L. B., Jayaraman, S., Clerkin, E., Yu, C. (2018). The developing infant creates a curriculum for statistical learning. Trends in Cognitive Sciences, 22, 325–336.
Google Scholar | Crossref | Medline
Smith, N. A., Trainor, L. J. (2008). Infant-directed speech is modulated by infant feedback. Infancy, 4, 410–420.
Google Scholar | Crossref
Stephens, G. J., Silbert, L. J., Hasson, U. (2010). Speaker–listener neural coupling underlies successful communication. Proceedings of the National Academy of Sciences, USA, 107, 14425–14430.
Google Scholar | Crossref | Medline | ISI
Thelen, E., Smith, L. B. (1996). A dynamic systems approach to the development of cognition and action. Cambridge, MA: MIT Press.
Google Scholar
Tomasello, M. (1992). The social bases of language acquisition. Social Development, 1, 67–87.
Google Scholar | Crossref
Trainor, L. J., Desjardins, R. J. (2002). Pitch characteristics of infant-directed speech affect infants’ ability to discriminate vowels. Psychonomic Bulletin & Review, 9, 335–340.
Google Scholar | Crossref | Medline | ISI
Urakawa, S., Takamoto, K., Ishikawa, A., Ono, T., Nishijo, H. (2015). Selective medial prefrontal cortex responses during live mutual gaze interactions in human infants: An fNIRS study. Brain Topography, 28, 691–701.
Google Scholar | Crossref | Medline
Vouloumanos, A., Werker, J. F. (2004). Tuned to the signal: The privileged status of speech for young infants. Developmental Science, 7, 270–276.
Google Scholar | Crossref | Medline | ISI
Vygotsky, L. (1978). Interaction between learning and development. In Gauvain, M., Cole, M. (Eds.), Readings on the development of children (Vol. 23, pp. 34–41). New York, NY: Scientific American Books.
Google Scholar
Wass, S. V., Noreika, V., Georgieva, S., Clackson, K., Brightman, L., Nutbrown, R., . . . Leong, V. (2019). Parental neural responsivity to infants’ visual attention: How mature brains influence immature brains during social interaction. PLOS Biology, 16(12), Article e2006328. doi:10.1371/journal.pbio.2006328
Google Scholar | Crossref
Yu, C., Smith, L. B. (2013). Joint attention without gaze following: Human infants and their parents coordinate visual attention to objects through eye-hand coordination. PLOS ONE, 8(11), Article e79659. doi:10.1371/journal.pone.0079659
Google Scholar | Crossref

 

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