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Immature integration and segregation of emotion-related brain circuitry in young children.

ABSTRACT: The human brain undergoes protracted development, with dramatic changes in expression and regulation of emotion from childhood to adulthood. The amygdala is a brain structure that plays a pivotal role in emotion-related functions. Investigating developmental characteristics of the amygdala and associated functional circuits in children is important for understanding how emotion processing matures in the developing brain. The basolateral amygdala (BLA) and centromedial amygdala (CMA) are two major amygdalar nuclei that contribute to distinct functions via their unique pattern of interactions with cortical and subcortical regions. Almost nothing is currently known about the maturation of functional circuits associated with these amygdala nuclei in the developing brain. Using intrinsic connectivity analysis of functional magnetic resonance imaging data, we investigated developmental changes in functional connectivity of the BLA and CMA in twenty-four 7- to 9-y-old typically developing children compared with twenty-four 19- to 22-y-old healthy adults. Children showed significantly weaker intrinsic functional connectivity of the amygdala with subcortical, paralimbic, and limbic structures, polymodal association, and ventromedial prefrontal cortex. Importantly, target networks associated with the BLA and CMA exhibited greater overlap and weaker dissociation in children. In line with this finding, children showed greater intraamygdala connectivity between the BLA and CMA. Critically, these developmental differences were reproducibly identified in a second independent cohort of adults and children. Taken together, our findings point toward weak integration and segregation of amygdala circuits in young children. These immature patterns of amygdala connectivity have important implications for understanding typical and atypical development of emotion-related brain circuitry.

SUBMITTER: Qin S

PROVIDER: S-EPMC3356602 | biostudies-literature | 2012 May

REPOSITORIES: biostudies-literature

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Immature integration and segregation of emotion-related brain circuitry in young children.

Qin Shaozheng S Young Christina B CB Supekar Kaustubh K Uddin Lucina Q LQ Menon Vinod V

Proceedings of the National Academy of Sciences of the United States of America 20120430 20

The human brain undergoes protracted development, with dramatic changes in expression and regulation of emotion from childhood to adulthood. The amygdala is a brain structure that plays a pivotal role in emotion-related functions. Investigating developmental characteristics of the amygdala and associated functional circuits in children is important for understanding how emotion processing matures in the developing brain. The basolateral amygdala (BLA) and centromedial amygdala (CMA) are two majo ...[more]

PMID: 22547826

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Project description:A critical feature of the human brain that gives rise to complex cognition is its ability to reconfigure its network structure dynamically and adaptively in response to the environment. Existing research probing task-related reconfiguration of brain network structure has concluded that, although there are many similarities in network structure during an intrinsic, resting state and during the performance of a variety of cognitive tasks, there are meaningful differences as well. In this study, we related intrinsic, resting state network organization to reconfigured network organization during the performance of two tasks: a sequence tapping task, which is thought to probe motor execution and likely engages a single brain network, and an n-back task, which is thought to probe working memory and likely requires coordination across multiple networks. We implemented graph theoretical analyses using functional connectivity data from fMRI scans to calculate whole-brain measures of network organization in healthy young adults. We focused on quantifying measures of network segregation (modularity, system segregation, local efficiency, number of provincial hub nodes) and measures of network integration (global efficiency, number of connector hub nodes). Using these measures, we found converging evidence that local, within-network communication is critical for motor execution, whereas integrative, between-network communication is critical for working memory. These results confirm that the human brain has the remarkable ability to reconfigure its large-scale organization dynamically in response to current cognitive demands and that interpreting reconfiguration in terms of network segregation and integration may shed light on the optimal network structures underlying successful cognition. SIGNIFICANCE STATEMENT:The dynamic nature of the human brain gives rise to the wide range of behaviors and cognition of which humans are capable. We collected fMRI data from healthy young adults and measured large-scale functional connectivity patterns between regions distributed across the entire brain. We implemented graph theoretical analyses to quantify network organization during two tasks hypothesized to require different combinations of brain networks. During motor execution, segregation of distinct networks increased. Conversely, during working memory, integration across networks increased. These changes in network organization were related to better behavioral performance. These results underscore the human brain's ability to reconfigure network organization selectively and adaptively when confronted with changing cognitive demands to achieve an optimal balance between segregation and integration.

Dataset Information

Immature integration and segregation of emotion-related brain circuitry in young children.

Publications

Immature integration and segregation of emotion-related brain circuitry in young children.

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