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

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. In the punctual center of all circles white Stands truly. The circles nearest to it share Its color, but less as they recede, impinged By difference and then by definition As a tone defines itself and separates And the circles quicken and crystal colors come And flare and bloom with his vast accumulation Stands and regards and repeats the primitive lines. From the Packet of Anacharsis, Wallace Stevens As the biological sciences became the central lens through which humans comprehended their world, assuming the position previously occupied by philosophy, Western thought shifted from understanding the universe in terms of hierarchical order or incremental progress, for which a “chain” or “line” may be the best underlying metaphor (see Lovejoy, 1936), to viewing the universe in terms of systems, for which the circle is the most fitting symbol. Reflected in Stevens’s poem (quoted in Bloom, 1980) is the notion that systems, or circles, have several important features: their center contains their most important qualities in a concentrated form; as rings grow farther away from the center, their “color” or qualities become integrated with foreign elements, mainly those outside the system; repetitions of “programs” encoded within the core reverberate throughout the circle rings; and all components of the system (all dots on the circle) are interrelated and constrained by the same external limits. Systems develop and reorganize, and colors become more pronounced and system specific from the initial “white. ” However, unlike the line, circles are not infinite but self-contained, grow from the core outward, follow a finite set of rules, and execute a predetermined series of programs, which, given adequate tools, can be observed already in their most embryonic form. Systems, therefore, contain sensitive periods (SP) by definition. Embedded in modern science is the assumption that getting to the root of systems and unraveling the laws of their SP can bring us closer to understanding the universe. Of all living systems, humans are by far the most complex, their development most extended, and the experience-dependent pathways to human cognitive functions involve the greatest plasticity. Research on SP in humans must therefore Address correspondence and reprint requests to: Ruth Feldman, Department of Psychology and the Gonda Brain Sciences Center, Bar-Ilan University, Ramat-Gan, Israel 52900; E-mail: Feldman@mail.biu. ac.il. Development and Psychopathology 27 (2015), 369–395 # Cambridge University Press 2015 doi:10.1017/S0954579415000048