A Developmental Shift from Positive to Negative Connectivity in Human Amygdala-Prefrontal Circuitry

By Dylan G. Gee, Kathryn L. Humphreys, Jessica E. Flannery, Bonnie Goff, Eva H. Telzer, Mor Shapiro, Todd A. Hare, Susan Y. Bookheimer, Nim Tottenham. Journal of Neuroscience, 2013

673 citations recorded by the source corpus.

Recent human imaging and animal studies highlight the importance of frontoamygdala circuitry in the regulation of emotional behavior and its disruption in anxiety-related disorders. Although tracing studies have suggested changes in amygdala–cortical connectivity through the adolescent period in rodents, less is known about the reciprocal connections within this circuitry across human development, when these circuits are being fine-tuned and substantial changes in emotional control are observed. The present study examined developmental changes in amygdala–prefrontal circuitry across the ages of 4–22 years using task-based functional magnetic resonance imaging. Results suggest positive amygdala–prefrontal connectivity in early childhood that switches to negative functional connectivity during the transition to adolescence. Amygdala–medial prefrontal cortex functional connectivity was significantly positive (greater than zero) among participants younger than 10 years, whereas functional connectivity was significantly negative (less than zero) among participants 10 years and older, over and above the effect of amygdala reactivity. The developmental switch in functional connectivity was paralleled by a steady decline in amygdala reactivity. Moreover, the valence switch might explain age-related improvement in task performance and a developmentally normative decline in anxiety. Initial positive connectivity followed by a valence shift to negative connectivity provides a neurobiological basis for regulatory development and may present novel insight into a more general process of developing regulatory connections.

Subfields: Behavioral Neuroscience, Cognitive Neuroscience

View Paper: https://www.semanticscholar.org/paper/75552b3e546e6142a040e84fe191b70302bfdb18

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Citations in the corpus

The Adolescent Brain Cognitive Development (ABCD) study: Imaging acquisition across 21 sites (2018, neutral): “Cognitive processing of these stimuli taps fronto-amygdala circuitry and functions involved in emotion reactivity and regulation (Hare et al., 2008; Gee et al., 2013), and taps ventral fronto-striatal circuitry implicated in reward (Somerville et al.”
The Adolescent Brain and the Emergence and Peak of Psychopathology (2015, background): “As such, children raised in these environments are subjected to higher levels of stress and less child-parent interaction than their non-orphaned peers and are prone to higher rates of emotion dysregulation and psychopathology (Tottenham et al., 2010, 2011; Gee et al., 2013).”
Early-Life Adversity and Physical and Emotional Health across the Lifespan: A Neuro-Immune Network Hypothesis (2015, background): “Furthermore, prefrontal regulation of the amygdala typically emerges in adolescence (37,38).”
Early developmental emergence of human amygdala–prefrontal connectivity after maternal deprivation (2013, methodology): “Speci ﬁ cally, adolescents and adults exhibit inverse (negative) correlations between amygdala and mPFC in response to emotional stimuli, a pattern of connectivity that has been characterized as indexing top-down inhibitory connections (24, 27, 28).”
The Development of Human Amygdala Functional Connectivity at Rest from 4 to 23 Years: a cross-sectional study (2014, positive): “Dramatic changes occur across childhood and adolescence in emotional behaviors that have been associated with amygdala-mediated cortical functional connections (e.g., emotion processing tasks: Gee et al., 2013; Hare et al., 2008; Perlman and Pelphrey, 2011; emotion reappraisal: McRae et al., 2012).”
Childhood Adversity and Neural Development: A Systematic Review (2019, background): “…and neutral faces (Maheu et al. 2010), but two contrasted fearful faces to implicit baseline instead of a neutral or scrambled face or other perceptual control (Gee et al. 2013a, Tottenham et al. 2011), making it difficult to conclude that differences are specific to threat-related processing.”
Early-Life Adversity Accelerates Child and Adolescent Development (2019, background): “In other words, and consistent with more proximate perspectives on the effects of adversity on human development, including behavioral, psychological, and neuroscientific ones (Callaghan & Tottenham, 2016; Ellis & Del Giudice, 2019; Gee et al., 2013), accelerated development was conceptualized as a ”
Brain On Stress: Vulnerability and Plasticity of the Prefrontal Cortex Over the Life Course (2013, background): “It is also noteworthy that the PFC to amygdala connectivity changes from positive to negative between early childhood and adolescence and young adulthood (Gee et al., 2013).”