Gaze onsets during naturalistic infant-caregiver interaction associate with ‘sender’ but not ‘receiver’ neural responses, and do not lead to changes in inter-brain synchrony

Abstract

Temporal coordination during infant-caregiver social interaction is thought to be crucial for supporting early language acquisition and cognitive development. Despite a growing prevalence of theories suggesting that increased inter-brain synchrony associates with many key aspects of social interactions such as mutual gaze, little is known about how this arises during development. Here, we investigated the role of mutual gaze onsets as a potential driver of inter-brain synchrony. We extracted dual EEG activity around naturally occurring gaze onsets during infant-caregiver social interactions in N = 55 dyads (mean age 12 months). We differentiated between two types of gaze onset, depending on each partners’ role. ‘Sender’ gaze onsets were defined at a time when either the adult or the infant made a gaze shift towards their partner at a time when their partner was either already looking at them (mutual) or not looking at them (non-mutual). ‘Receiver’ gaze onsets were defined at a time when their partner made a gaze shift towards them at a time when either the adult or the infant was already looking at their partner (mutual) or not (non-mutual). Contrary to our hypothesis we found that, during a naturalistic interaction, both mutual and non-mutual gaze onsets were associated with changes in the sender, but not the receiver’s brain activity and were not associated with increases in inter-brain synchrony above baseline. Further, we found that mutual, compared to non-mutual gaze onsets were not associated with increased inter brain synchrony. Overall, our results suggest that the effects of mutual gaze are strongest at the intra-brain level, in the ‘sender’ but not the ‘receiver’ of the mutual gaze.

Annual Research Review: ‘There, the dance is – at the still point of the turning world’ – dynamic systems perspectives on coregulation and dysregulation during early development

“…But in fact, the picture emerging from the microdynamic analyses and dual‐brain studies suggests that attention coregulation is in fact quite similar to arousal coregulation. Children rarely use ostensive signalling during early interactions (Beebe et al., 2016; Phillips et al., 2021; Yu & Smith, 2013) and can be remarkably insensitive to caregivers' ostensive signalling (Marriott Haresign et al., 2023). But during face‐to‐face, tabletop interactions, both shared entrainment and interactive contingencies develop (Moreno‐Núñez, Rodríguez, & Del Olmo, 2017; Wass et al., 2022).…”

Why behaviour matters: Studying inter-brain coordination during child-caregiver interaction

“…They also move their torsos, heads, limbs and faces; and they vocalise. It is important to note that many of these problems are also observed in traditional screen paradigms, where, for example, eye movements occur systematically, time-locked to the appearance of new objects on-screen (e.g., Dimigen et al, 2009 , Dimigen et al, 2011 ; Yuval-Greenberg et al, 2008 ), and participants can become fidgety during repetitious screen paradigms ( Marriott Haresign et al, 2023 ). But our discussion here will concentrate on naturalistic paradigms.…”

“…It is well established that the spectral range of muscle activity (∼20–300 Hz) overlaps with high-frequency neural activity ( Criswell, 2010 ; see Muthukumaraswamy, 2013 for a review), and that even state-of-the-art cleaning techniques are unable to remove this artifact fully. Because of this, many developmental scientists typically concentrate on lower-frequency neural dynamics ( Marshall et al, 2011 , Leong et al, 2017 ; Xie et al, 2018 ; van der Velde et al, 2019 ; Jones et al, 2020 ) and apply low pass filters during artifact rejection (e.g., at ∼30 Hz in adults ( Niedermeyer and da Silva, 2005 ; Fries et al, 2008 ) and ∼20 Hz in infants ( Wass et al, 2018 ; Marriott Haresign et al, 2023 ). Several studies have, though, illustrated muscle-related artifact contamination at much lower frequencies ( Whitham et al, 2007 ).…”

“…The primary objective of most hyperscanning research is to investigate the dynamics between the brain activities of two interacting individuals during spontaneous, naturalistic interactions. These dynamics are often evaluated using various metrics for assessing inter-brain coordination, such as synchrony (commonly defined as 'when X is high, Y is high') and sequential entrainment (commonly defined as 'changes in X forward-predict changes in Y′) ( Ayrolles et al, 2021 ; Marriott Haresign et al, 2023 ). In this article, we compare two distinct approaches for studying inter-brain coordination: the 'non-event-locked approach' and the 'event-locked approach'.…”

“…This approach, common in intra-brain coordination literature, involves event-locking brain activity to specific behaviours produced by individuals or externally presented events, enabling detailed examination of temporal dynamics in the associations between neural activity across different brain regions ( Friston, 1994 , Friston et al, 2003 , Honey et al, 2009 , Horwitz, 2003 , Horwitz and Glabus, 2005 , Kahan and Foltynie, 2013 , Sporns, 2007 ). Statistical tests are employed to compare changes in interbrain coordination relative to chance, around specific behavioural events, in order to determine significant patterns of interbrain coordination and their temporal scales (e.g., Lindenberger et al, 2009 ; Gugnowska et al, 2022 ; Marriott Haresign et al, 2023 ). Statistical testing most often utilizes standardized, permutation-based clustering measures of EEG activity ( Maris and Oostenveld, 2007 ).…”