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.

Keywords: CD38; breastfeeding; emotion perception; infancy; oxytocin.

Fig. 1.

Presentation paradigm. Please note that the side in which the emotional face was presented was counterbalanced. Colored borders are shown to aid the reader in assessing the graphs below but were not presented to the infants. Stimulus duration is represented in seconds (s).

Fig. 2.

Regions of interest (ROIs). Dashed lines represent the ROIs analyzed for each emotion and actress.

Fig. 3.

Bar graph illustrating the interaction between EBF and emotion. Infants with a high EBF duration displayed significantly longer looking preferences to happy eyes than infants with low EBF. *P < 0.05; n = 98; data are presented in raw form and bars represent ±1 SEM.

Fig. S1.

Partial regression plot illustrating the prediction of EBF on infant looking preference to happy eyes minus angry eyes. Please note that the residuals from the regression are plotted on the x and y axes. Points above zero represent a bias toward happy stimuli whereas points below zero represent a bias toward anger. P = 0.006, n = 98.

Fig. S2.

Bar graphs illustrating the results of one-sample t tests in which we compared each looking preference score to chance (50%) when (A) split by EBF group and (B) split by EBF and genotype groups. ^†P < 0.05, ^††P < 0.01, and ^†††P < 0.001.

Fig. 4.

Infant looking preferences were modulated by an interaction between EBF and CD38 genotype. Bar graphs represent emotion and EBF interactions for (A) CC carriers and (B) CA/AA carriers separately. *P < 0.05, **P < 0.01; n = 98; data are presented in raw form and bars represent ±1 SEM.