The neurodevelopmental precursors of altruistic behavior in infancy

Abstract

Altruistic behavior is considered a key feature of the human cooperative makeup, with deep ontogenetic roots. The tendency to engage in altruistic behavior varies between individuals and has been linked to differences in responding to fearful faces. The current study tests the hypothesis that this link exists from early in human ontogeny. Using eye tracking, we examined whether attentional responses to fear in others at 7 months of age predict altruistic behavior at 14 months of age. Our analysis revealed that altruistic behavior in toddlerhood was predicted by infants’ attention to fearful faces but not happy or angry faces. Specifically, infants who showed heightened initial attention to (i.e., prolonged first look) followed by greater disengagement (i.e., reduced attentional bias over 15 seconds) from fearful faces at 7 months displayed greater prosocial behavior at 14 months of age. Our data further show that infants’ attentional bias to fearful faces and their altruistic behavior was predicted by brain responses in the dorsolateral prefrontal cortex (dlPFC), measured through functional near-infrared spectroscopy (fNIRS). This suggests that, from early in ontogeny, variability in altruistic helping behavior is linked to our responsiveness to seeing others in distress and brain processes implicated in attentional control. These findings critically advance our understanding of the emergence of altruism in humans by identifying responsiveness to fear in others as an early precursor contributing to variability in prosocial behavior.

Neural responses to happy, fearful and angry faces of varying identities in 5- and 7-month-old infants

“…Activations were observed in areas broadly consistent with previous adult fMRI studies, including temporal areas (Haxby et al, 2001), IFG (Sabatinelli et al, 2011), TPJ, and medial prefrontal SFG (Etkin, Egner, & Kalisch, 2011). Specifically, we found broad bilateral temporal and frontal responses to happy faces, in line with previous infant studies in which facial identity remained unvarying within each block (Grossmann et al, 2018;Krol et al, 2019;Minagawa-Kawai et al, 2009). Exploratory analyses of the current data revealed greater frontal (dSFG) activation to happy versus fearful faces, robust to changes in facial identity; this finding did not survive correction for multiple comparisons.…”

“…Exploratory analyses of the current data revealed greater frontal (dSFG) activation to happy versus fearful faces, robust to changes in facial identity; this finding did not survive correction for multiple comparisons. At least one fMRI study in adults (Zhang et al, 2016) and another fNIRS study in infants (Grossmann et al, 2018) also do not report differential activations to different types of facial emotions over temporal cortices. Interestingly, and contrary to previous reports in behavioral and ERP paradigms Xie et al, 2018), no differences between 5-and 7-month-olds were found.…”

“…While not all brain regions implicated in emotional face processing in adults are accessible by fNIRS due to limited depth penetration, superficial temporal and frontal cortices can be accessed. Prior infant fNIRS work has shown differential brain responses to happy and angry faces in the temporal cortex from 6-7 months of age (Nakato, Otsuka, Kanazawa, Yamaguchi, & Kakigi, 2011) and differential responses to happy, angry, and/or fearful faces in the right inferior frontal cortex at 7-months of age when modelled in conjunction with certain individual epigenetic differences (Grossmann, Missana, & Krol, 2018;Krol, Puglia, Morris, Connelly, & Grossmann, 2019). fNIRS has also revealed that medial frontal regions are implicated in processing happy faces in infants from 9-13 months (Minagawa-Kawai et al, 2009) and linked individual differences in frontal responses to emotional faces with earlier epigenetic changes (Krol et al, 2019) and later behavior (Grossmann et al, 2018).…”

“…Prior infant fNIRS work has shown differential brain responses to happy and angry faces in the temporal cortex from 6-7 months of age (Nakato, Otsuka, Kanazawa, Yamaguchi, & Kakigi, 2011) and differential responses to happy, angry, and/or fearful faces in the right inferior frontal cortex at 7-months of age when modelled in conjunction with certain individual epigenetic differences (Grossmann, Missana, & Krol, 2018;Krol, Puglia, Morris, Connelly, & Grossmann, 2019). fNIRS has also revealed that medial frontal regions are implicated in processing happy faces in infants from 9-13 months (Minagawa-Kawai et al, 2009) and linked individual differences in frontal responses to emotional faces with earlier epigenetic changes (Krol et al, 2019) and later behavior (Grossmann et al, 2018). However, no studies to date have directly tested for differences in neural activity between 5 and 7 months, a critical time window during which differential responses to fearful faces are often first observed with ERP (Leppänen, Richmond, Vogel-Farley, Moulson, & Nelson, 2009;Xie, McCormick, Westerlund, Bowman, & Nelson, 2018).…”

Epigenetic modification of the oxytocin receptor gene isassociated with emotion processing in the infant brain

“…Identifying factors that contribute to variability in emotion processing in infancy is important to A C C E P T E D M A N U S C R I P T achieve a more mechanistic understanding of healthy and atypical socio-emotional development. In prior work, individual differences in emotion processing have been linked to overt social behaviors in neurotypical adults and infants [4,5], and have in more extreme forms been associated with a host of mental health disorders in adolescents and adults [6,7]. One factor that may contribute to variability in emotion processing is the endogenous oxytocin system.…”