Delayed Imitation of Lipsmacking Gestures by Infant Rhesus Macaques (Macaca mulatta)

Abstract

Human infants are capable of accurately matching facial gestures of an experimenter within a few hours after birth, a phenomenon called neonatal imitation. Recent studies have suggested that rather than being a simple reflexive-like behavior, infants exert active control over imitative responses and ‘provoke’ previously imitated gestures even after a delay of up to 24 h. Delayed imitation is regarded as the hallmark of a sophisticated capacity to control and flexibly engage in affective communication and has been described as an indicator of innate protoconversational readiness. However, we are not the only primates to exhibit neonatal imitation, and delayed imitation abilities may not be uniquely human. Here we report that 1-week-old infant rhesus macaques (Macaca mulatta) who show immediate imitation of a lipsmacking gesture also show delayed imitation of lipsmacking, facilitated by a tendency to refrain from lipsmacking toward a still face during baseline measurements. Individual differences in delayed imitation suggest that differentially matured cortical mechanisms may be involved, allowing some newborns macaques to actively participate in communicative exchanges from birth. Macaque infants are endowed with basic social competencies of intersubjective communication that indicate cognitive and emotional commonality between humans and macaques, which may have evolved to nurture an affective mother-infant relationship in primates.

Early Social Experience Affects Neural Activity to Affiliative Facial Gestures in Newborn Nonhuman Primates

“…This is consistent with previous reports that newborn macaque infants imitate LS gestures across the first week of life [10,11,34], and extends this finding, demonstrating that early experiences impact this skill [33]. We found no evidence, however, of TP imitation, nor did we find any increases in facial gesturing in the non-biological control condition.…”

“…The imitation paradigm has been described in detail in previous studies (e.g., [33,34]), and is outlined in the Supplementary Materials. Briefly, all infants received live presentation of stimuli for three conditions: a) Tongue Protrusion (TP) with maximal extension and retraction of the tongue; b) Lipsmack (LS) a rapid opening and closing of the lips; and a 15-cm diameter plastic Disk (DK) with a red and black cross painted on it that was rotated 180°.…”

The mirror neuron system as revealed through neonatal imitation: presence from birth, predictive power and evidence of plasticity

“…happiness, sadness, surprise [38]) prior to having opportunities to form strong associative links between action observation and imitative responses. Similarly, macaque infants reared in a nursery from birth imitate before they have experienced any contingent facial interactions with carers [18,53,108], and they additionally show specific electroencephalogram changes (i.e. mu suppression), evidence of a functioning MNS, on the day of birth [17,109].…”

“…Indeed, many researchers argue that it is important to examine whether neonatal imitation is predictive of later social and cognitive development [44,45,58,103,119,120] because it could be an early marker of later deficits in social skills [57]. Previous studies suggest that in both humans and macaque monkeys, only about 50% of neonates consistently engage in imitation of facial gestures [53,54,121]. Only one study examined neonatal imitation predictively in human infants: imitation at three ages-2 to 3 days, three weeks and three months of age-predicted visual attention at three months of age.…”

“…Infants in the standard rearing group did not see facial gestures and did not receive any handling beyond basic care and other (non-related) experimental procedures. On day 7 or 8, infants were tested for neonatal imitation with two gestures-LPS and TP-that were compared with a non-social control condition, a rotating disc with orthogonal stripes (for methodological details, see [53,54]). We found that only infants who were exposed to facial gestures showed increased LPS in the LPS condition (baseline: M ¼ 2.00, s.d.…”