The development of human amygdala functional connectivity at rest from 4 to 23years: A cross-sectional study
Open accessAbstract
Functional connections (FC) between the amygdala and cortical and subcortical regions underlie a range of affective and cognitive processes. Despite the central role amygdala networks have in these functions, the normative developmental emergence of FC between the amygdala and the rest of the brain is still largely undefined. This study employed amygdala subregion maps and resting-state functional magnetic resonance imaging to characterize the typical development of human amygdala FC from age 4 to 23years old (n=58). Amygdala FC with subcortical and limbic regions was largely stable across this developmental period. However, three cortical regions exhibited age-dependent changes in FC: amygdala FC with the medial prefrontal cortex (mPFC) increased with age, amygdala FC with a region including the insula and superior temporal sulcus decreased with age, and amygdala FC with a region encompassing the parahippocampal gyrus and posterior cingulate also decreased with age. The transition from childhood to adolescence (around age 10years) marked an important change-point in the nature of amygdala-cortical FC. We distinguished unique developmental patterns of coupling for three amygdala subregions and found particularly robust convergence of FC for all subregions with the mPFC. These findings suggest that there are extensive changes in amygdala-cortical functional connectivity that emerge between childhood and adolescence.
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The mPFC and amygdala have extensive bidirectional connections and often function together.
“Although mPFC and amygdala have extensive bidirectional connections and often function in tandem (110, 116, 117), these mPFC findings on greater left responding under conditions of deprived care are suggestive but have yet to be extended to amygdala structure or function.”
From Disorganized attachment in infancy predicts greater amygdala volume in adulthood (2016) · cites this paper as [116]
Functional connections between amygdala and mPFC do not emerge until age 10 years, and continue to mature through at least 23 years of age.
“Functional connections between amygdala and mPFC do not emerge until age 10 years, and continue to mature through at least through 23 years of age (Gabard-Durnam et al., 2014).”
From Sensitive periods of substance abuse: Early risk for the transition to dependence (2017) · cites this paper as Gabard-Durnam et al., 2014
Positive functional connectivity between the amygdala and other subcortical regions, including the NAc and dorsal STR, is observed in childhood and remains largely stable through adulthood.
“In contrast to the development of cortical/subcortical connectivity, positive functional connectivity between the amygdala and other subcortical regions, including the NAc and dorsal STR (caudate/putamen), is observed in childhood and remains largely stable through adulthood (Gabard-Durnam et al., 2014).”
From Sensitive periods of substance abuse: Early risk for the transition to dependence (2017) · cites this paper as Gabard-Durnam et al., 2014
The structural and functional connectivity between the amygdala and cortical areas undergoes substantial maturation during adolescence.
“Structural and functional connectivity between the amygdala and cortical brain regions undergoes dramatic maturation across adolescence (Qin et al., 2012, Gabard-Durnam et al., 2014).”
From Developmental sex differences in resting state functional connectivity of amygdala sub-regions (2015) · cites this paper as Gabard-Durnam et al., 2014
The observed pattern of decreased parieto-occipital connectivity and increased medial prefrontal connectivity matches adult resting-state functional connectivity patterns of amygdala sub-regions.
“which corresponds with adult RSFC patterns of amygdala sub-regions (Roy et al., 2009, Qin et al., 2012, Gabard-Durnam et al., 2014), albeit with varying effects by sex.”
From Developmental sex differences in resting state functional connectivity of amygdala sub-regions (2015) · cites this paper as Gabard-Durnam et al., 2014
Earlier studies have reported that connectivity between the medial prefrontal cortex and all amygdala sub-regions increases with age.
“Previous research has shown coupling of mPFC and all amygdala sub-regions with increasing age (Roy et al., 2009, Qin et al., 2012, Gabard-Durnam et al., 2014),”
From Developmental sex differences in resting state functional connectivity of amygdala sub-regions (2015) · cites this paper as Gabard-Durnam et al., 2014
Negative functional connectivity, reflecting network segregation and specialization, has been found between amygdala sub-regions and more dorsal and posterior brain regions in adults and in a cross-sectional sample from childhood to early adulthood.
“Negative functional connectivity, or segregation and specialization of networks (Rubinov and Sporns, 2010), has been observed between amygdalar sub-regions and more dorsal and posterior brain regions in both adults (Roy et al., 2009) and in a cross-sectional sample spanning childhood and early adulthood (Gabard-Durnam et al., 2014).”
From Developmental sex differences in resting state functional connectivity of amygdala sub-regions (2015) · cites this paper as Gabard-Durnam et al., 2014
Only one previous study conducted a secondary analysis of sex differences in adolescents, and it did not find a significant effect of sex.
“However, only one study performed a secondary analysis to examine sex differences in adolescents, which did not yield a significant effect of sex (Gabard-Durnam et al., 2014).”
From Developmental sex differences in resting state functional connectivity of amygdala sub-regions (2015) · cites this paper as Gabard-Durnam et al., 2014
Previous research on resting-state functional connectivity of amygdala sub-regions found that positive connectivity between all sub-regions and the medial prefrontal cortex increases with age from 10 to 25 years.
“Previous research examining RSFC of amygdala sub-regions found increased positive connectivity with age (10 – 25 years) between all sub-regions and the mPFC (Gabard-Durnam et al., 2014),”
From Developmental sex differences in resting state functional connectivity of amygdala sub-regions (2015) · cites this paper as Gabard-Durnam et al., 2014
The comparable functional coupling patterns in both sexes are in accordance with a healthy developmental trajectory.
“which is in accordance with a healthy developmental trajectory (Roy et al., 2009, Qin et al., 2012, Gabard-Durnam et al., 2014).”
From Developmental sex differences in resting state functional connectivity of amygdala sub-regions (2015) · cites this paper as Gabard-Durnam et al., 2014
The amygdala has positive connectivity with subcortical and limbic regions, and connectivity between these regions stabilizes early in childhood.
“These and other studies suggest that the amygdala is positively connected with subcortical and limbic regions, and that functional connectivity between these brain regions is stabilized early in childhood development (Gabard-Durnam et al., 2014);”
From Developmental sex differences in resting state functional connectivity of amygdala sub-regions (2015) · cites this paper as Gabard-Durnam et al., 2014
If decoupling between the superficial amygdala and parieto-occipital cortices is the adult norm, then the sex-specific trajectories of amygdala sub-region connectivity seen in this adolescent sample may shift toward mature adult patterns.
“If decoupling of SFA and parieto-occipital cortices is indeed the norm in adulthood as some studies suggest (Roy et al., 2009, Gabard-Durnam et al., 2014), then the sexually dimorphic trajectories of amygdala sub-regional connectivity observed in the current sample may give way to mature patterns observed in adults;”
From Developmental sex differences in resting state functional connectivity of amygdala sub-regions (2015) · cites this paper as Gabard-Durnam et al., 2014
Weaker or less organized functional and structural connectivity between these brain regions in childhood may contribute to increased difficulty with emotion regulation.
“Weaker or less organized functional and structural connectivity between these brain regions in childhood may also be contributing toward increased difficulty with emotion regulation [55–57].”
From The neuroscience of emotion regulation development: Implications for education (2016) · cites this paper as [57]
Amygdala-prefrontal connectivity changes with age at rest.
“Research has demonstrated amygdala-prefrontal connectivity to change with age at rest17 and during the processing of affective information18.”
From Multimodal evidence for delayed threat extinction learning in adolescence and young adulthood (2019) · cites this paper as [17]
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- Authors
- Gabard-Durnam, L. J., Flannery, J., Goff, B., Gee, D. G., Humphreys, K. L., Telzer, E., Hare, T., & Tottenham, N.
- Affiliations
- University of California, Los Angeles (US)
- University of Illinois Urbana-Champaign (US)
- University of Zurich (CH)
- Corresponding author
- Gabard-Durnam, Laurel J.
- ORCID
- Venue
- NeuroImage
- Publisher
- Elsevier BV
- Published
- 2014-07
- Volume
- 95
- Pages
- 193-207
- ISSN
- 1053-8119 (ISSN-L)
- PMC
- PMC4305511
- OpenAlex
- W2015455914
- Cited by
- 372
- References
- 93
- Citations by year
- 2026: 14 · 2025: 11 · 2024: 21 · 2023: 25 · 2022: 18 · 2021: 28 · 2020: 72 · 2019: 49 · 2018: 35 · 2017: 29 · 2016: 40 · 2015: 22 · 2014: 7 · 2013: 1
- FWCI
- 18.23
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- NeuroImage (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Zurich Open Repository and Archive (University of Zurich) (acceptedVersion)
- Zurich Open Repository and Archive (University of Zurich) (submittedVersion)
- Funders
- National Institute of Mental Health (R01MH091864)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- amygdala, functional connectivity, resting-state functional connectivity, brain development, childhood to adolescence, amygdala subregions, medial prefrontal cortex, insula, superior temporal sulcus, parahippocampal gyrus, posterior cingulate cortex, normative development
- MeSH terms
- Adolescent, Amygdala, Brain Mapping, Child, Child, Preschool, Cross-Sectional Studies, Female, Humans, Image Processing, Computer-Assisted, Magnetic Resonance Imaging, Male, Neural Pathways, Rest, Young Adult
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