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Speaker gaze increases information coupling between infant and adult brains

  1. Sam Wassd
  1. aDepartment of Psychology, University of Cambridge, Cambridge CB2 3EB, United Kingdom;
  2. bDivision of Psychology, Nanyang Technological University, Singapore 637332, Republic of Singapore;
  3. cMRC Cognition & Brain Sciences Unit, University of Cambridge, Cambridge CB2 7EF, United Kingdom;
  4. dDivision of Psychology, University of East London, London E16 2RD, United Kingdom
  1. Edited by Uri Hasson, Princeton University, Princeton, NJ, and accepted by Editorial Board Member Marlene Behrmann November 2, 2017 (received for review February 15, 2017)

Significance

During communication, social ostensive signals (like gaze) are exchanged in a temporally contingent manner. Synchronized behavior creates social connectedness within human dyads, and even infants synchronize behaviorally with adults. However, the neural mechanisms that support infant–adult synchronization are unknown. Here, we provide evidence that infants up-regulate neural synchronization with adult partners when offered direct ostensive gaze, as compared with gaze aversion. Gaze therefore brings infant–adult neural activity into mutual alignment, creating a joint-networked state that may facilitate communicative success. Further, infants’ own communicative attempts were positively associated with adults’ neural synchronization to them, indicating mutual regulation of synchronization within infant–adult dyads. Thus, interpersonal neural synchronization may provide a mechanism by which infants construct their own earliest social networks.

Abstract

When infants and adults communicate, they exchange social signals of availability and communicative intention such as eye gaze. Previous research indicates that when communication is successful, close temporal dependencies arise between adult speakers’ and listeners’ neural activity. However, it is not known whether similar neural contingencies exist within adult–infant dyads. Here, we used dual-electroencephalography to assess whether direct gaze increases neural coupling between adults and infants during screen-based and live interactions. In experiment 1 (n = 17), infants viewed videos of an adult who was singing nursery rhymes with (i) direct gaze (looking forward), (ii) indirect gaze (head and eyes averted by 20°), or (iii) direct-oblique gaze (head averted but eyes orientated forward). In experiment 2 (n = 19), infants viewed the same adult in a live context, singing with direct or indirect gaze. Gaze-related changes in adult–infant neural network connectivity were measured using partial directed coherence. Across both experiments, the adult had a significant (Granger) causal influence on infants’ neural activity, which was stronger during direct and direct-oblique gaze relative to indirect gaze. During live interactions, infants also influenced the adult more during direct than indirect gaze. Further, infants vocalized more frequently during live direct gaze, and individual infants who vocalized longer also elicited stronger synchronization from the adult. These results demonstrate that direct gaze strengthens bidirectional adult–infant neural connectivity during communication. Thus, ostensive social signals could act to bring brains into mutual temporal alignment, creating a joint-networked state that is structured to facilitate information transfer during early communication and learning.

Footnotes

  • ?1To whom correspondence should be addressed. Email: vvec2{at}cam.ac.uk.
  • Author contributions: V.L. and S.W. designed research; V.L., E.B., K.C., and S.G. performed research; V.L., S.G., S.L., and S.W. analyzed data; and V.L. and S.W. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission. U.H. is a guest editor invited by the Editorial Board.

  • This article contains supporting information online at www.danielhellerman.com/lookup/suppl/doi:10.1073/pnas.1702493114/-/DCSupplemental.

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