Maternal buffering of human amygdala-prefrontal circuitry during childhood but not during adolescence
Open accessAbstract
Mature amygdala-prefrontal circuitry regulates affect in adulthood but shows protracted development. In altricial and semialtricial species, caregivers provide potent affect regulation when mature neurocircuitry is absent. The present investigation examined a potential mechanism through which caregivers provide regulatory influences in childhood. Children, but not adolescents, showed evidence of maternal buffering, such that maternal stimuli suppressed amygdala reactivity. In the absence of maternal stimuli, children exhibited immature amygdala-prefrontal connectivity. However, in the presence of maternal stimuli, children’s connectivity was more mature, resembling adolescents’ connectivity. Children showed improved affect-related regulation in the presence of their mothers. Individual differences emerged, with greater maternal influence on amygdala-prefrontal circuitry associated with stronger mother-child relationships and maternal modulation of behavioral regulation. These findings suggest a neural mechanism through which caregivers modulate children’s regulatory behavior by inducing more mature connectivity and buffering against heightened reactivity. Maternal buffering in childhood, but not adolescence, suggests that childhood may be a sensitive period for amygdala-prefrontal development.
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Early environmental factors, such as early caregiving or the lack thereof, modulate the timing and course of emotional development.
“A comprehensive set of literature reviews (9, 32, 78, 83–86) details the hypothesis that early environmental factors, e.g., early caregiving or the lack thereof, modulate the timing and course of emotional development.”
From The Stress Acceleration Hypothesis of Nightmares (2017) · cites this paper as [84]
The Discussion (page unavailable) says prolonged maternal separation may accelerate amygdala–prefrontal development, while maternal presence can support regulation during a possible sensitive period in childhood. This supports the proposed role of early caregiving and its absence in emotional development. However, the cited paper is an original investigation, not one of the literature reviews described in the citing sentence. (LLM, conf=0.84)
Experimental — accuracy not yet measuredThe maternal stimulus phasically induced an adult-like pattern of frontoamygdala negative connectivity in children, such that children resembled adolescents when viewing their mother's face.
“Moreover, the maternal stimulus phasically induced an adult-like pattern of frontoamygdala negative connectivity in children, such that children resembled adolescents when viewing their mother's face (Fig. 5b).”
From The impact of developmental timing for stress and recovery (2015) · cites this paper as Gee et al., 2014
The maternal stimulus buffered against heightened amygdala reactivity in childhood, but stopped being effective in adolescence.
“Findings revealed that the maternal stimulus buffered against heightened amygdala reactivity in childhood, but stopped being effective in adolescence (Fig. 5a).”
From The impact of developmental timing for stress and recovery (2015) · cites this paper as Gee et al., 2014
Children with greater neural modulation by the mother had lower separation anxiety and more secure attachment, as well as better emotion regulation in their mother's presence.
“Individual difference analyses suggested that children with greater neural modulation by the mother had lower separation anxiety and more secure attachment, as well as better emotion regulation in their mother's presence.”
From The impact of developmental timing for stress and recovery (2015) · cites this paper as Gee et al., 2014
Children displayed evidence of maternal buffering of behavior, such that they performed with enhanced affect-related regulatory behavior in the presence of their mother compared with a stranger.
“Children also displayed evidence of maternal buffering of behavior, such that they performed with enhanced affect-related regulatory behavior in the presence of their mother compared with a stranger.”
From The impact of developmental timing for stress and recovery (2015) · cites this paper as Gee et al., 2014
Social buffering of the infant is a dynamic process that wanes as individuals across species mature and become independent.
“Social buffering of the infant is a dynamic process that wanes as individuals across species mature and become independent (Gee et al., 2014, Levine, 2001, McCormack et al., 2009, Sanchez, 2006, Stanton and Levine, 1990, Suchecki et al., 1995, van Oers et al., 1998) (Fig. 1).”
From Early life adversity during the infant sensitive period for attachment: Programming of behavioral neurobiology of threat processing and social behavior (2017) · cites this paper as Gee et al., 2014
Grouping children (ages 4-10) and adolescents (ages 11-17) in terms of positive versus negative amygdala-mPFC connectivity in response to maternal vs. stranger stimuli predicted their levels of separation anxiety with a large effect size, η2 = .21.
“For example, Gee et al. (2014) found that grouping children (ages 4–10) and adolescents (ages 11–17) simply in terms of positive versus negative amygdala-mPFC connectivity in response to maternal vs. stranger stimuli predicted their levels of separation anxiety with a large effect size, η2 = .21.”
From Adolescent neurobiological susceptibility to social context (2016) · cites this paper as Gee et al., 2014
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- Authors
- Gee, D. G., Gabard-Durnam, L., Telzer, E. H., Humphreys, K. L., Goff, B., Shapiro, M., Flannery, J., Lumian, D. S., Fareri, D. S., Caldera, C., & Tottenham, N.
- Affiliations
- University of California, Los Angeles (US)
- Corresponding author
- Tottenham, Nim
- ORCID
- Venue
- Psychological Science
- Publisher
- SAGE Publications
- Published
- 2014-10-03
- Volume
- 25
- Issue
- 11
- Pages
- 2067-2078
- ISSN
- 0956-7976 (ISSN-L)
- 1467-9280
- PMC
- PMC4377225
- OpenAlex
- W2109186297
- Cited by
- 363
- References
- 50
- Citations by year
- 2026: 12 · 2025: 18 · 2024: 20 · 2023: 31 · 2022: 28 · 2021: 27 · 2020: 88 · 2019: 63 · 2018: 19 · 2017: 22 · 2016: 24 · 2015: 11
- FWCI
- 22.31
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Psychological Science (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Mental Health (P50MH078105, R01MH091864)
- Topics
- Social Sciences › Psychology › Clinical Psychology › Child and Adolescent Psychosocial and Emotional Development
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Keywords
- amygdala, prefrontal cortex, amygdala-prefrontal connectivity, emotion regulation, child development, adolescence, mother-child relationship, behavioral regulation, sensitive period, neural development
- MeSH terms
- Adolescent, Affect, Age Factors, Amygdala, Brain Mapping, Child, Child, Preschool, Female, Humans, Magnetic Resonance Imaging, Male, Mothers, Prefrontal Cortex
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