Genetic variation in CD38 and breastfeeding experience interact to impact infants’ attention to social eye cues

Abstract

Attending to emotional information conveyed by the eyes is an important social skill in humans. The current study examined this skill in early development by measuring attention to eyes while viewing emotional faces in 7-mo-old infants. In particular, we investigated individual differences in infant attention to eyes in the context of genetic variation (CD38 rs3796863 polymorphism) and experiential variation (exclusive breastfeeding duration) related to the oxytocin system. Our results revealed that, whereas infants at this age show a robust fear bias (increased attention to fearful eyes), their attention to angry and happy eyes varies as a function of exclusive breastfeeding experience and genetic variation in CD38. Specifically, extended exclusive breastfeeding duration selectively enhanced looking preference to happy eyes and decreased looking to angry eyes. Importantly, however, this interaction was impacted by CD38 variation, such that only the looking preferences of infants homozygous for the C allele of rs3796863 were affected by breastfeeding experience. This genotype has been associated with reduced release of oxytocin and higher rates of autism. In contrast, infants with the CA/AA genotype showed similar looking preferences regardless of breastfeeding exposure. Thus, differences in the sensitivity to emotional eyes may be linked to an interaction between the endogenous (CD38) and exogenous (breastfeeding) availability of oxytocin. These findings underline the importance of maternal care and the oxytocin system in contributing to the early development of responding to social eye cues.CD38 | oxytocin | breastfeeding | emotion perception | infancy S ensitive responding to emotions in others is a vital social skill that helps us relate to others, predict their actions, and coordinate our own behavior during social interactions. Given its critical importance for effective social functioning, it is not surprising that the ability to detect and distinguish between emotional expressions emerges early in human development. Findings from behavioral and neuroscience studies indicate that infants' ability to discriminate between positive and negative emotional expressions emerges in the first year of life (see refs. 1 and 2 for reviews). For example, by around 7 mo of age, infants distinguish between fearful and happy facial expressions and show increased allocation of attention to fear (3). This enhanced attention to fear in others marks the emergence of a "fear bias" in infancy, which is thought to orient and alert the infant to potentially threatening situations (2, 4). Prior work with adults demonstrates that emotion perception and, in particular, fear detection (eyes wide open) rely heavily on information from the eye region and occur even in the absence of conscious perception (5-8).The importance of eye cues for emotion perception has recently been studied in infants. In an event-related brain potential (ERP) study, 7-mo-old infants were found to discriminate between fear and happiness on the basis of eye c...

Demography and rapid local adaptation shape Creole cattle genome diversity in the tropics

“…Another region in BTA06 showing selection signal with the XP‐EHH methodology in two clusters, Colombian group (region #5) and Texas Longhorn (region #41), has not been associated with any QTL in cattle so far and includes genes such as C1QTNF7 , related to Trypanosoma cruzi cardiomyopathy (Deng et al., ), FBXL5 , which controls iron metabolism processes key for the regulation of reactive oxygen species that augment with the exposure of animals to high environmental temperatures (Paital et al., ), BST1 that has immune functions facilitating pre‐B‐cell growth, and CD38 that has pleiotropic functions in T‐cell activation (Würsch et al., ), social behaviour through its effect on the release of oxytocin (Krol, Monakhov, Lai, Ebstein, & Grossmann, ) and cancer. BST1 and CD38 are also implicated in salivary and pancreatic secretion and nicotinate and nicotinamide metabolism pathways (Table ).…”

The neurobiology of mammalian parenting and the biosocial context of human caregiving

“…Similar in this context is the role of breastfeeding. Although much research emphasized the positive effects of breastfeeding on the formation of mother-infant synchrony, the infant's social gaze (Feldman and Eidelman, 2003;Krol et al, 2015) and the development of cognitive competencies up to adulthood (Johnson et al, 1996;Mortensen et al, 2002), while bonding in rodents critically depends on lactation, human mothers can bond to their infants in the absence of breastfeeding via multiple alternative pathways and other forms of caregiving.…”

Genetic Variation in the Maternal Oxytocin System Affects Cortisol Responsiveness to Breastfeeding in Infants and Mothers

“…Why infant CD38 genotype did not have an impact on infants' cortisol response remains unclear. However, it should be mentioned that in prior work with older infants (7 months of age), infant CD38 genotype has been shown to impact differences in infants' attention to emotional eyes as a function of duration of exclusive breastfeeding (Krol et al 2015a). This indicates that in a different context (emotion perception and exclusive breastfeeding duration) and at an older age (7 instead of 4-6 months of age) infant CD38 genotype has an effect on socio-emotional processes.…”

“…Hardy-Weinberg equilibrium was tested in mothers and infants separately; no deviations were detected (all p-values >0.05). The majority of studies relating the polymorphism rs3796863 (CD38) with aspects of social behavior and plasma oxytocin find differences between homozygous risk allele carriers (CC) and A carriers (CA/AA) (Algoe and Way 2014;Feldman et al 2013;Feldman et al 2012;Krol et al 2015a;Sauer et al 2013;Sauer et al 2012). In keeping with prior studies, we conducted our analyses by grouping genotypes in the same manner (CC versus CA/AA).…”

“…Furthermore, the C allele is more common in autism spectrum disorder (ASD) than controls and is considered a risk allele for atypical social development (Lerer et al 2010;Munesue et al 2010). Prior work has also shown that breastfeeding experience interacts with genetic variation at this locus to account for individual differences in infants' attention to emotional cues (Krol et al 2015a).…”