2018 Friday Session B 1200

Friday, November 2, 2018 | Session B, Conference Auditorium | 12pm

Infant and adult brains are coupled to the dynamics of social behaviors during naturalistic communication
E. Piazza, L. Hasenfratz, U. Hasson, C. Lew-Williams

Infancy is the foundational period of learning from adults, and the dynamics of the social environment have long been proposed as central to children’s early language acquisition (Vygotsky, 1978; Tomasello, 1992). Here, we present a novel, naturalistic approach to studying live interactions to uncover the interdependencies between infant and adult brains and behaviors (including verbal behavior) during real-time communication.

Previous work using fMRI in adults has shown that neural coupling (measured with inter-subject temporal correlation, or ISC) relates to the quality of communication between a speaker telling a story and a listener later hearing the story (Stephens, Silbert, & Hasson, 2010). Here, using dual-brain functional near-infrared spectroscopy (fNIRS), we simultaneously and continuously measured the brains of infants (9-15 months) and an adult while they communicated and played with each other in real time. Each adult-infant dyad participated in two five-minute conditions (order counterbalanced): “Together” (in which the adult experimenter played with, sang to, and read to the infant; see Figure 1A, top) and “Apart” (in which the infant and experimenter participated in similarly communicative tasks but with other individuals instead of each other).

We found that time-locked neural synchrony within dyads was significantly greater when they interacted with each other (“Together”) than with control individuals (“Apart”). Figure 1B (bottom) shows significantly coupled channels, determined by a bootstrapped permutation procedure based on phase-scrambled surrogate data (see Simony et al., 2016) and corrected for multiple comparisons using false-discovery rate (q < .05; Benjamini & Hochberg, 1995). Surprisingly, by computing ISC across varying time lags between the adult and infant signals, we also found that prefrontal activation in the infant brain preceded and drove similar activation in the adult brain (Figure 1C), which crucially advances our understanding of children’s influence over the accommodative behaviors of the caregivers around them. Furthermore, we found that both infant and adult brains continuously tracked the moment-to-moment fluctuations of mutual gaze, infant emotion (smiling), and adult speech prosody with high temporal precision (Figure 1D, top). The specific temporal pattern of tracking was unique to each dyadic interaction and could not be explained by large-scale fluctuations (e.g., task-related changes in arousal; Figure 1D, bottom).

Our results provide the first demonstration that the PFC of a caregiver and infant are not only continuously synchronized to each other during naturalistic communication, but are also dynamically tuned to cues that are critical for language processing—gaze, smiling, and speech prosody. This investigation represents a critical step toward understanding how children’s brains begin to extract the most important structure from adults’ input, and how adults, in turn, represent infants’ emotional feedback as they strive to engage them. Our approach marks a new way to understand how the brains and the social/verbal behaviors of infants both shape and reflect those of their caregivers during real-life communication.