Cited by 286Neuroendocrine regulation and behaviorChild and Animal Learning DevelopmentNeurogenesis and neuroplasticity mechanisms

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

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Feldman, Ruth·2015·Development and Psychopathology

DOI 10.1017/s0954579415000048

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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.

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Altered Basal Cortisol Levels at 3, 6, 8 and 18 Months in Infants Born at Extremely Low Gestational Age
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The development of regulatory functions from birth to 5 years: insights from premature infants
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Maternal depression and anxiety, social synchrony, and infant regulation of negative and positive emotions.
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Developmental changes in pain expression in premature, full-term, two- and four-month-old infants
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Impact of Maternal Depression Across the First 6 Years of Life on the Child’s Mental Health, Social Engagement, and Empathy: The Moderating Role of Oxytocin
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Prenatal stress generates deficits in rat social behavior: Reversal by oxytocin
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Early Social Relationships: A Psychobiologist's View
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Early social relationships: a psychobiologist’s view
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The cross-generation transmission of oxytocin in humans
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Neuropeptides and their receptors: a psychosomatic network
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Parenting stress, infant emotion regulation, maternal sensitivity, and the cognitive development of triplets: A model for parent and child influences in a unique ecology
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Annual research review: Epigenetic mechanisms and environmental shaping of the brain during sensitive periods of development
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Testing a family intervention hypothesis: The contribution of mother-infant skin-to-skin contact (kangaroo care) to family interaction, proximity, and touch.
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The Effects of Varying Environmental Demands on Maternal and Infant Behavior
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Oxytocin administration to parent enhances infant physiological and behavioral readiness for social engagement
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Oxytocin stimulates adult neurogenesis even under conditions of stress and elevated glucocorticoids
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Marital behavior, oxytocin, vasopressin, and wound healing
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Synchrony and specificity in the maternal and the paternal brain: relations to oxytocin and vasopressin
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Genetic variants in AVPR1A linked to autism predict amygdala activation and personality traits in healthy humans
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Identifying the What, Why, and How of an Observed Action: An fMRI Study of Mentalizing and Mechanizing during Action Observation
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Posttraumatic Stress Disorder in Infants and Young Children Exposed to War-Related Trauma
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Oxytocin induces morphological plasticity in the adult hypothalamo-neurohypophysial system
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Direct and indirect effects of breast milk on the neurobehavioral and cognitive development of premature infants
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“…comparable between groups prior to KC, maternal contact accelerated maturation of the autonomic nervous system, and infants who received contact had higher RSA, indicating a more mature system that enables a better foundation for the development of regulatory capacities (Feldman & Eidelman, 2003b).”
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Deconstructing sociality, social evolution and relevant nonapeptide functions
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Oxytocin mediates early experience-dependent cross-modal plasticity in the sensory cortices
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The Effects of Varying Environmental Demands on Maternal and Infant Behavior
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Mother-infant synchrony and the development of moral orientation in childhood and adolescence: Direct and indirect mechanisms of developmental continuity.
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The relational basis of adolescent adjustment: trajectories of mother–child interactive behaviors from infancy to adolescence shape adolescents' adaptation
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Biological and environmental initial conditions shape the trajectories of cognitive and social‐emotional development across the first years of life
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Parent-specific reciprocity from infancy to adolescence shapes children's social competence and dialogical skills
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Developmental Perspectives on Oxytocin and Vasopressin
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Oxytocin alleviates the neuroendocrine and cytokine response to bacterial endotoxin in healthy men
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Oxytocin Facilitation of Maternal Behavior in Sheepa
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Wired for behaviors: from development to function of innate limbic system circuitry
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Parent-infant synchrony and the social emotional development of triplets
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The main olfactory system and social learning in mammals
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Hormonal Changes in Mammalian Fathers
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Parent–child and triadic antecedents of children’s social competence: Cultural specificity, shared process.
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Neural plasticity in fathers of human infants
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Social Recovery by Isolation-Reared Monkeys
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Oxytocin administration, salivary testosterone, and father–infant social behavior
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Oxytocin, cortisol, and triadic family interactions
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Fatherhood affects dendritic spines and vasopressin V1a receptors in the primate prefrontal cortex
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A Theory of the Transition to Critical Period Plasticity: Inhibition Selectively Suppresses Spontaneous Activity
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Oxytocin mediates acquisition of maternally associated odor preferences in preweanling rat pups.
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Stress reactivity in war-exposed young children with and without posttraumatic stress disorder: Relations to maternal stress hormones, parenting, and child emotionality and regulation
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Sleep-Wake Transitions in Premature Neonates Predict Early Development
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Does a Triplet Birth Pose a Special Risk for Infant Development? Assessing Cognitive Development in Relation to Intrauterine Growth and Mother-Infant Interaction Across the First 2 Years
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The Neurobiology of Human Attachments
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The adaptive human parental brain: implications for children's social development
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See all 286

Authors: Feldman, R.
Affiliations: Bar-Ilan University (IL)
Corresponding author: Feldman, Ruth
ORCID: Feldman, Ruth
Venue: Development and Psychopathology
Publisher: Cambridge University Press (CUP)
Published: 2015-05
Volume: 27
Issue: 2
Pages: 369-395
ISSN: 0954-5794 (ISSN-L)
1469-2198
DOI: 10.1017/s0954579415000048
OpenAlex: W1924288196
Cited by: 271
References: 216
Citations by year: 2026: 16 · 2025: 30 · 2024: 20 · 2023: 23 · 2022: 20 · 2021: 29 · 2020: 30 · 2019: 26 · 2018: 26 · 2017: 19 · 2016: 19 · 2015: 11
FWCI: 3.90
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.cambridge.org/core/terms (unspecified, 5 d)
Locations: Development and Psychopathology (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroendocrine regulation and behavior
Social Sciences › Psychology › Developmental and Educational Psychology › Child and Animal Learning Development
Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Keywords: sensitive period, critical period, oxytocin, social synchrony, preterm birth, multiple births, postpartum depression, chronic unpredictable mild stress, social brain, neuroplasticity, developmental psychopathology, resilience, early deprivation, social development (developmental psychology), natural experiment
MeSH terms: Adult, Animals, Brain, Critical Period, Psychological, Female, Humans, Neuronal Plasticity, Oxytocin, Play and Playthings, Social Behavior, Parenting

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

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