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Speaker gaze increases information coupling between infant and adult brains

Victoria Leong, Elizabeth Byrne, Kaili Clackson, Stanimira Georgieva, Sarah Lam, Sam Wass
doi: https://doi.org/10.1101/108878
Victoria Leong
1Department of Psychology, University of Cambridge
2Nanyang Technological University, Singapore
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Elizabeth Byrne
3MRC Cognition & Brain Sciences Unit, Cambridge
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Kaili Clackson
1Department of Psychology, University of Cambridge
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Stanimira Georgieva
1Department of Psychology, University of Cambridge
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Sarah Lam
1Department of Psychology, University of Cambridge
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Sam Wass
4University of East London
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ABSTRACT

Successful communication with infants requires the temporally-contingent exchange of social signals of availability and communicative intention, such as gaze. Previous research indicates that temporal dependencies arise between adult speakers’ and listeners’ neural activity during successful communication. 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 (a) Direct gaze (looking forward); (b) Indirect gaze (head and eyes averted by 20°); or (c) 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 conversely also influenced the adult more during Direct than Indirect gaze. Furthermore, infants vocalised more frequently during live Direct gaze, and individual infants who vocalized longer also elicited stronger synchronisation from the adult. This is the first demonstration that direct gaze strengthens bi-directional 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 could facilitate information transfer during early communication and learning.

SIGNIFICANCE STATEMENT During communication, social ostensive signals (like gaze) are exchanged in a temporally-contingent manner. Synchronised behaviour creates social connectedness within human dyads, and even infants synchronise behaviourally with adults. However, the neural mechanisms that support infant-adult synchronisation are unknown. Here, we provide the first evidence that infants up-regulate neural synchronisation with adult partners when offered direct ostensive gaze, as compared to 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 synchronisation to them, indicating mutual regulation of synchronisation within infant-adult dyads. Thus, interpersonal neural synchronisation may provide a mechanism by which infants construct their own earliest social networks.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted September 16, 2017.
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Speaker gaze increases information coupling between infant and adult brains
Victoria Leong, Elizabeth Byrne, Kaili Clackson, Stanimira Georgieva, Sarah Lam, Sam Wass
bioRxiv 108878; doi: https://doi.org/10.1101/108878
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Speaker gaze increases information coupling between infant and adult brains
Victoria Leong, Elizabeth Byrne, Kaili Clackson, Stanimira Georgieva, Sarah Lam, Sam Wass
bioRxiv 108878; doi: https://doi.org/10.1101/108878

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