Selective Medial Prefrontal Cortex Responses During Live Mutual Gaze Interactions in Human Infants: An fNIRS Study

Abstract

To investigate the role of the prefrontal cortex (PFC) in processing multimodal communicative ostensive signals in infants, we measured cerebral hemodynamic responses by using near-infrared spectroscopy (NIRS) during the social interactive play "peek-a-boo", in which both visual (direct gaze) and auditory (infant-directed speech) stimuli were presented. The infants (mean age, around 7 months) sat on their mother's lap, equipped with an NIRS head cap, and looked at a partner's face during "peek-a-boo". An eye-tracking system simultaneously monitored the infants' visual fixation patterns. The results indicate that, when the partner presented a direct gaze, rather than an averted gaze, toward an infant during social play, the infant fixated on the partner's eye region for a longer duration. Furthermore, hemodynamic activity increased more prominently dorsomedial prefrontal cortex (mPFC) in response to social play with a partner's direct gaze compared to an averted gaze. In contrast, hemodynamic activity increased in the right dorsolateral prefrontal cortex (R-lPFC) regardless of a partner's eye gaze direction. These results indicate that a partner's direct gaze shifts an infant's attention to the partner's eyes for interactive communication, and specifically activates the mPFC. The differences in hemodynamic responses between the mPFC and R-lPFC suggest functional differentiation within the PFC, and a specific role of the mPFC in the perception of face-to-face communication, especially in mutual gaze, which is essential for social interaction.

Infant and adult brains are coupled to the dynamics of natural communication

“…Our work furthers previous fNIRS research showing heightened mPFC activation in infants in response to direct gaze (Urakawa et al, 2015) and EEG research showing enhanced inter-subject coupling between infants and adults during direct (versus indirect) gaze (Leong et al, 2017). The present study extends these findings by measuring neural coupling during rich, everyday social communication, including interactive playing, singing, and book-reading.…”

The present and future use of functional near‐infrared spectroscopy (fNIRS) for cognitive neuroscience

“…133 Building on the participant-friendly nature of fNIRS, a large number of studies use this method to explore the development of cognition and social cognition in infants, children, and individuals with developmental disorders. Such work tracks the development of body perception, 134 response to direct gaze, 135,136 responses to speech 137 and many other tasks. Reviewing all these papers is beyond the scope of the present article (see Refs.…”

Cortical responses before 6 months of life associate with later autism

“…Through a series of fNIRS studies with infants aged 6 months and under (Grossmann et al ., , ; Lloyd‐Fox et al ., , , ; Correia et al ., ; Farroni et al ., ), researchers have demonstrated enhanced activation to dynamic visual social stimuli (such as facial eye and mouth movements and nursery rhyme hand actions) in prefrontal, inferior frontal and superior temporal regions of the social brain network. These findings are consistent with patterns of activation found in studies with similar aged infants viewing static social and non‐social stimuli (Otsuka et al ., ; Carlsson et al ., ; Nakato et al ., ) and older infants viewing dynamic social stimuli (Minagawa‐Kawai et al ., ; Ichikawa et al ., ; Urakawa et al ., ; Lloyd‐Fox et al ., ) and fMRI studies with adults (Allison et al ., ; Pelphrey et al ., ; Lotze et al ., ; Van Overwalle & Baetens, ). Further, auditory social responses localized over regions of the middle and superior temporal gyri and sulci (particularly anterior regions) – to vocalizations and auditory communicative cues – have also been demonstrated in fNIRS studies with young infants (Grossmann et al ., ; Minagawa‐Kawai et al ., ; Lloyd‐Fox et al ., , ,, ), replicating and extending fMRI research with adults (Belin et al ., ).…”