Correction to: Epigenetic tuning of brain signal entropy in emergent human social behavior.

An amendment to this paper has been published and can be accessed via the original article.

Epigenetic tuning of brain signal entropy in emergent human social behavior.

BACKGROUND: How the brain develops accurate models of the external world and generates appropriate behavioral responses is a vital question of widespread multidisciplinary interest. It is increasingly understood that brain signal variability-posited to enhance perception, facilitate flexible cognitive representations, and improve behavioral outcomes-plays an important role in neural and cognitive development. The ability to perceive, interpret, and respond to complex and dynamic social information is particularly critical for the development of adaptive learning and behavior. Social perception relies on oxytocin-regulated neural networks that emerge early in development. METHODS: We tested the hypothesis that individual differences in the endogenous oxytocinergic system early in life may influence social behavioral outcomes by regulating variability in brain signaling during social perception. In study 1, 55 infants provided a saliva sample at 5 months of age for analysis of individual differences in the oxytocinergic system and underwent electroencephalography (EEG) while listening to human vocalizations at 8 months of age for the assessment of brain signal variability. Infant behavior was assessed via parental report. In study 2, 60 infants provided a saliva sample and underwent EEG while viewing faces and objects and listening to human speech and water sounds at 4 months of age. Infant behavior was assessed via parental report and eye tracking. RESULTS: We show in two independent infant samples that increased brain signal entropy during social perception is in part explained by an epigenetic modification to the oxytocin receptor gene (OXTR) and accounts for significant individual differences in social behavior in the first year of life. These results are measure-, context-, and modality-specific: entropy, not standard deviation, links OXTR methylation and infant behavior; entropy evoked during social perception specifically explains social behavior only; and only entropy evoked during social auditory perception predicts infant vocalization behavior. CONCLUSIONS: Demonstrating these associations in infancy is critical for elucidating the neurobiological mechanisms accounting for individual differences in cognition and behavior relevant to neurodevelopmental disorders. Our results suggest that an epigenetic modification to the oxytocin receptor gene and brain signal entropy are useful indicators of social development and may hold potential diagnostic, therapeutic, and prognostic value.

Helping, fast and slow: Exploring intuitive cooperation in early ontogeny.

Cooperative behavior is central to human societies. Human adults who reach their cooperative decisions more rapidly and independently of cognitive control display greater levels of prosocial behavior. This is taken to show that cooperation is guided by intuitive processes rather than by active control of selfish impulses. The current study investigated the emergence of intuitive cooperation in early human ontogeny. We measured helping behavior (latency and frequency) in a longitudinal sample of infants at ages 14 and 18 months. Between 14 and 18 months, the frequency of helping significantly increased and latency to help significantly decreased, suggesting advances in helping behavior during this period of development. Moreover, at 18 months and to some extent, even at 14 months, infants who helped more rapidly (as indexed by a shorter latency) acted more prosocially (as indexed by a greater frequency of helping) than infants who were slower to help. This link between latency and frequency of prosocial behavior was independent of infants' ability for inhibitory control and general sociability levels. Prosocial behavior thus begins to be governed by intuitive processes that operate independently of cognitive control early in human ontogeny. This informs our understanding of the nature and emergence of cooperative behavior by supporting accounts that assign a central role to intuition in the evolution of human cooperation.

The neurodevelopmental precursors of altruistic behavior in infancy.

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 correlates of infants' sensitivity to vocal expressions of peers.

Responding to others' emotional expressions is an essential and early developing social skill among humans. Much research has focused on how infants process facial expressions, while much less is known about infants' processing of vocal expressions. We examined 8-month-old infants' processing of other infants' vocalizations by measuring event-related brain potentials (ERPs) to positive (infant laughter), negative (infant cries), and neutral (adult hummed speech) vocalizations. Our ERP results revealed that hearing another infant cry elicited an enhanced negativity (N200) at temporal electrodes around 200ms, whereas listening to another infant laugh resulted in an enhanced positivity (P300) at central electrodes around 300ms. This indexes that infants' brains rapidly respond to a crying peer during early auditory processing stages, but also selectively respond to a laughing peer during later stages associated with familiarity detection processes. These findings provide evidence for infants' sensitivity to vocal expressions of peers and shed new light on the neural processes underpinning emotion processing in infants.

Putting the face in context: Body expressions impact facial emotion processing in human infants.

Body expressions exert strong contextual effects on facial emotion perception in adults. Specifically, conflicting body cues hamper the recognition of emotion from faces, as evident on both the behavioral and neural level. We examined the developmental origins of the neural processes involved in emotion perception across body and face in 8-month-old infants by measuring event-related brain potentials (ERPs). We primed infants with body postures (fearful, happy) that were followed by either congruent or incongruent facial expressions. Our results revealed that body expressions impact facial emotion processing and that incongruent body cues impair the neural discrimination of emotional facial expressions. Priming effects were associated with attentional and recognition memory processes, as reflected in a modulation of the Nc and Pc evoked at anterior electrodes. These findings demonstrate that 8-month-old infants possess neural mechanisms that allow for the integration of emotion across body and face, providing evidence for the early developmental emergence of context-sensitive facial emotion perception.

The association of temperament and maternal empathy with individual differences in infants' neural responses to emotional body expressions.

We examined the role of infant temperament and maternal dispositional empathy in the neural processing of happy and fearful emotional body expressions in 8-month-old infants by measuring event-related brain potentials. Our results revealed that infants' tendency to approach novel objects and people was positively correlated with the neural sensitivity (attention allocation) to fearful expressions, while infant fearfulness was negatively correlated to the neural sensitivity to fearful expressions. Maternal empathic concern was associated with infants' neural discrimination between happy and fearful expression, with infants of more empathetically concerned mothers showing greater neural sensitivity (attention allocation) to fearful compared to happy expressions. It is critical that our results also revealed that individual differences in the sensitivity to emotional information are explained by an interaction between infant temperament and maternal empathic concern. Specifically, maternal empathy appears to impact infants' neural responses to emotional body expressions, depending on infant fearfulness. These findings support the notion that the way in which infants respond to emotional signals in the environment is fundamentally linked to their temperament and maternal empathic traits. This adds an early developmental neuroscience dimension to existing accounts of social-emotional functioning, suggesting a complex and integrative picture of why and how infants' emotional sensitivity varies.

Tuning the developing brain to emotional body expressions.

Reading others' emotional body expressions is an essential social skill. Adults readily recognize emotions from body movements. However, it is unclear when in development infants become sensitive to bodily expressed emotions. We examined event-related brain potentials (ERPs) in 4- and 8-month-old infants in response to point-light displays (PLDs) of happy and fearful body expressions presented in two orientations (upright and inverted). The ERP results revealed that 8-month-olds but not 4-month-olds respond sensitively to the orientation and the emotion of the dynamic expressions. Specifically, 8-month-olds showed (i) an early (200-400 ms) orientation-sensitive positivity over frontal and central electrodes, and (ii) a late (700-1100 ms) emotion-sensitive positivity over temporal and parietal electrodes in the right hemisphere. These findings suggest that orientation-sensitive and emotion-sensitive brain processes, distinct in timing and topography, develop between 4 and 8 months of age.

Infants' emerging sensitivity to emotional body expressions: insights from asymmetrical frontal brain activity.

Sensitive responding to others' emotional body expressions is an essential social skill in humans. Using event-related brain potentials, it has recently been shown that the ability to discriminate between emotional body expressions develops between 4 and 8 months of age. However, it is not clear whether the perception of emotional body expressions in others evokes sensitive brain responses linked to motivational processes in infants. We therefore examined frontal EEG alpha asymmetry in response to dynamic happy and fearful body expressions presented to 4- and 8-month-old infants in 2 orientations (upright and inverted). Our results revealed that only 8-month-olds but not 4-month-olds showed significant differences in their frontal asymmetry responses between emotional expressions when presented in an upright orientation. Specifically, 8-month-old infants showed a greater lateralization to the left hemisphere in response to happy expression, indexing a greater tendency to approach, whereas they showed a greater lateralization to the right hemisphere in response to fearful expressions, indexing a greater tendency to withdraw. These findings provide further support for the notion that infants' perception of emotion undergoes a developmental tuning during this period in development. Critically, the results suggest that the infant brain becomes sensitive to the motivational significance conveyed by the emotional body expressions.

Discrimination of fearful and happy body postures in 8-month-old infants: an event-related potential study.

Responding to others' emotional body expressions is an essential social skill in humans. Adults readily detect emotions from body postures, but it is unclear whether infants are sensitive to emotional body postures. We examined 8-month-old infants' brain responses to emotional body postures by measuring event-related potentials (ERPs) to happy and fearful bodies. Our results revealed two emotion-sensitive ERP components: body postures evoked an early N290 at occipital electrodes and a later Nc at fronto-central electrodes that were enhanced in response to fearful (relative to happy) expressions. These findings demonstrate that: (a) 8-month-old infants discriminate between static emotional body postures; and (b) similar to infant emotional face perception, the sensitivity to emotional body postures is reflected in early perceptual (N290) and later attentional (Nc) neural processes. This provides evidence for an early developmental emergence of the neural processes involved in the discrimination of emotional body postures.

Developmental and individual differences in the neural processing of dynamic expressions of pain and anger.

We examined the processing of facial expressions of pain and anger in 8-month-old infants and adults by measuring event-related brain potentials (ERPs) and frontal EEG alpha asymmetry. The ERP results revealed that while adults showed a late positive potential (LPP) to emotional expressions that was enhanced to pain expressions, reflecting increased evaluation and emotional arousal to pain expressions, infants showed a negative component (Nc) to emotional expressions that was enhanced to angry expressions, reflecting increased allocation of attention to angry faces. Moreover, infants and adults showed opposite patterns in their frontal asymmetry responses to pain and anger, suggesting developmental differences in the motivational processes engendered by these facial expressions. These findings are discussed in the light of associated individual differences in infant temperament and adult dispositional empathy.

Duration of exclusive breastfeeding is associated with differences in infants' brain responses to emotional body expressions.

Much research has recognized the general importance of maternal behavior in the early development and programing of the mammalian offspring's brain. Exclusive breastfeeding (EBF) duration, the amount of time in which breastfed meals are the only source of sustenance, plays a prominent role in promoting healthy brain and cognitive development in human children. However, surprisingly little is known about the influence of breastfeeding on social and emotional development in infancy. In the current study, we examined whether and how the duration of EBF impacts the neural processing of emotional signals by measuring electro-cortical responses to body expressions in 8-month-old infants. Our analyses revealed that infants with high EBF experience show a significantly greater neural sensitivity to happy body expressions than those with low EBF experience. Moreover, regression analyses revealed that the neural bias toward happiness or fearfulness differs as a function of the duration of EBF. Specifically, longer breastfeeding duration is associated with a happy bias, whereas shorter breastfeeding duration is associated with a fear bias. These findings suggest that breastfeeding experience can shape the way in which infants respond to emotional signals.

Neural correlates of perceptual narrowing in cross-species face-voice matching.

Integrating the multisensory features of talking faces is critical to learning and extracting coherent meaning from social signals. While we know much about the development of these capacities at the behavioral level, we know very little about the underlying neural processes. One prominent behavioral milestone of these capacities is the perceptual narrowing of face-voice matching, whereby young infants match faces and voices across species, but older infants do not. In the present study, we provide neurophysiological evidence for developmental decline in cross-species face-voice matching. We measured event-related brain potentials (ERPs) while 4- and 8-month-old infants watched and listened to congruent and incongruent audio-visual presentations of monkey vocalizations and humans mimicking monkey vocalizations. The ERP results indicated that younger infants distinguished between the congruent and the incongruent faces and voices regardless of species, whereas in older infants, the sensitivity to multisensory congruency was limited to the human face and voice. Furthermore, with development, visual and frontal brain processes and their functional connectivity became more sensitive to the congruence of human faces and voices relative to monkey faces and voices. Our data show the neural correlates of perceptual narrowing in face-voice matching and support the notion that postnatal experience with species identity is associated with neural changes in multisensory processing (Lewkowicz & Ghazanfar, 2009).

Three-year-old children intervene in third-party moral transgressions.

We investigated children's moral behaviour in situations in which a third party was harmed (the test case for possession of agent-neutral moral norms). A 3-year-old and two puppets each created a picture or clay sculpture, after which one puppet left the room. In the Harm condition, the remaining (actor) puppet then destroyed the absent (recipient) puppet's picture or sculpture. In a Control condition, the actor acted similarly but in a way that did not harm the recipient. Children protested during the actor's actions, and, upon the recipient's return, tattled on the actor and behaved prosocially towards the recipient more in the Harm than in the Control condition. This is the first study to show that children as young as 3 years of age actively intervene in third-party moral transgressions.