Sensitive periods in human social development: New insights from research on oxytocin, synchrony, and high-risk parenting

Abstract

Sensitive periods (SP) in behavioral development appeared in the biological sciences during the first decade of the 20th century, and research in animal models beginning in the 1950s provide terminology and evidence for SP effects. This paper proposes a rigorous program for human SP research and argues that the complexity of the human brain and variability of the human ecology necessitate that SP effects must be studied in humans, employ longitudinal designs starting at birth, test mechanism-based hypotheses based on animal studies that manipulate early environments, and utilize high-risk conditions as “natural experiments.” In light of research on the molecular basis of critical periods and their sequential cascades, it is proposed that the oxytocin (OT) system, an ancient and integrative system that cross-talks with the stress, reward, immune, and brain stem mediated homeostatic systems and supports mammalian sociality, plays a unique role in experience-dependent plasticity that buttresses SP effects due to its (a) dendritic mode of release leading to autoregulated functioning primed by early experience, (b) pulsatile pattern of activity, and (c) special role in neural plasticity at the molecular and network assembly levels. Synchrony, the coordination of biology and behavior during social contact, is suggested as a mechanism by which SP exert their effect on OT functionality, the social brain, and adult sociality. Findings from four high-risk birth cohorts, each followed repeatedly from birth to 10 years, provide unique “natural experiments” for human SP research based on specific programs in animal models. These include prematurity (maternal proximity), multiple birth (peer rearing), postpartum depression (low licking and grooming), and chronic unpredictable trauma (maternal rotation, variable foraging demands). In each cohort, hypotheses are based on the missing environmental component during SP, and findings on social synchrony, OT functionality, stress response, emotion regulation, and mental health accord with the multilevel and dynamic principles of developmental psychopathology. The results on the potential for reparation versus chronicity following early deprivation highlight a flexible conceptualization of resilience based on human SP research. Consideration of SP effects at the molecular, endocrine, brain, and behavioral levels and in relation to the neural plasticity and multifinality of human social functions may assist in fine-tuning early detection and the construction of targeted individualized interventions.