Reciprocal face-to-face communication between rhesus macaque mothers and their newborn infants

Abstract

Human mothers interact emotionally with their newborns through exaggerated facial expressions, speech, mutual gaze, and body contact, a capacity that has long been considered uniquely human [1-4]. Current developmental psychological theories propose that this pattern of mother-infant exchange promotes the regulation of infant emotions [4-6] and serves as a precursor of more complex forms of social exchange including perspective taking and empathy. Here we report that in rhesus macaques, mother-infant pairs also communicate intersubjectively via complex forms of emotional exchanges including exaggerated lipsmacking, sustained mutual gaze, mouth-mouth contacts, and neonatal imitation. Infant macaques solicit their mother's affiliative responses and actively communicate to her. However, this form of communication disappears within the infant's first month of life. Our data challenge the view that the mother-infant communicative system functions in order to sustain proximity and that infants are simply passive recipients in such interaction. Thus, emotional communication between mother and infant is not uniquely human. Instead, we can trace back to macaques the evolutionary foundation of those behaviors that are crucial for the establishment of a functional capacity to socially exchange with others.

Figure 1

1a. Frequency (means +/− SEM) of mutual gaze between mothers and infants (blue) and between other females and infants (red) during the infants’ first two months of life. 1b. Frequency of lipsmacking (means +/− SEM) directed at infants by mothers (blue) and other females (red) during the infants’ first two months of life. White dots show the frequency (means +/− SEM) of infants’ physical separation from their mothers outside mother’s arm reach.

Figure 2

Captured and cropped still frames (see video 1 of supporting materials) illustrating maternal behaviors toward infants. A. Mother is pulling her infant’s head and stares at him. The infant is about 10 days of age. B. Mother is lipsmacking at infant’s orbital area. C. Mother is licking at the infant’s orbital area.

Figure 3

Captured and cropped still frames (see video 2 of supporting materials) illustrating a mother lipsmacking at her infant. Infant is 6 days old. Note that the mother’s head is bouncing up and down and that facial expressions are alternating between teeth-chatter and lipsmacking (bottom figure).

Figure 4

4a. Frequency (means +/− SEM) of infants’ lipsmacking in response to mother’s lipsmack (blue) and other females’ lipsmack (red) during the infants’ first two months of life. 4b. Frequency (means +/− SEM) of infants’ lipsmacking directed at the mother (blue) or other females (red) without prior lipsmacking by adult monkeys during the infants’ first two months of life.