Stimulus-Elicited Connectivity Influences Resting-State Connectivity Years Later in Human Development: A Prospective Study.
Although the functional architecture of the brain is indexed by resting-state connectivity networks, little is currently known about the mechanisms through which these networks assemble into stable mature patterns. The current study posits and tests the long-term phasic molding hypothesis that resting-state networks are gradually shaped by recurring stimulus-elicited connectivity across development by examining how both stimulus-elicited and resting-state functional connections of the human brain emerge over development at the systems level. Using a sequential design following 4- to 18-year-olds over a 2 year period, we examined the predictive associations between stimulus-elicited and resting-state connectivity in amygdala-cortical circuitry as an exemplar case (given this network's protracted development across these ages). Age-related changes in amygdala functional connectivity converged on the same regions of medial prefrontal cortex (mPFC) and inferior frontal gyrus when elicited by emotional stimuli and when measured at rest. Consistent with the long-term phasic molding hypothesis, prospective analyses for both connections showed that the magnitude of an individual's stimulus-elicited connectivity unidirectionally predicted resting-state functional connectivity 2 years later. For the amygdala-mPFC connection, only stimulus-elicited connectivity during childhood and the transition to adolescence shaped future resting-state connectivity, consistent with a sensitive period ending with adolescence for the amygdala-mPFC circuit. Together, these findings suggest that resting-state functional architecture may arise from phasic patterns of functional connectivity elicited by environmental stimuli over the course of development on the order of years.



A fundamental issue in understanding the ontogeny of brain function is how resting-state (intrinsic) functional networks emerge and relate to stimulus-elicited functional connectivity. Here, we posit and test the long-term phasic molding hypothesis that resting-state network development is influenced by recurring stimulus-elicited connectivity through prospective examination of the developing human amygdala-cortical functional connections. Our results provide critical insight into how early environmental events sculpt functional network architecture across development and highlight childhood as a potential developmental period of heightened malleability for the amygdala-medial prefrontal cortex circuit. These findings have implications for how both positive and adverse experiences influence the developing brain and motivate future investigations of whether this molding mechanism reflects a general phenomenon of brain development.
Department of Psychology, Columbia University, New York, New York 10025, laurel.gabarddurnam@gmail.com.
Laurel Joy
LJ
Gabard-Durnam
Department of Psychiatry, Weill Cornell Medical College, New York, New York 10065.
Dylan Grace
DG
Gee
Department of Psychology, University of California-Los Angeles, Los Angeles, California 90024.
Bonnie
B
Goff
Department of Psychology, University of Oregon, Eugene, Oregon 97403.
Jessica
J
Flannery
Department of Psychology, University of Illinois at Urbana-Champaign, Champaign, Illinois 61801, and.
Eva
E
Telzer
Department of Psychology, University of California-Los Angeles, Los Angeles, California 90024.
Kathryn Leigh
KL
Humphreys
Department of Psychology, University of Denver, Denver, Colorado 80208.
Daniel Stephen
DS
Lumian
Department of Psychology, Columbia University, New York, New York 10025.
Dominic Stephen
DS
Fareri
Department of Psychology, University of California-Los Angeles, Los Angeles, California 90024.
Christina
C
Caldera
Department of Psychology, Columbia University, New York, New York 10025.
Nim
N
Tottenham
D000293:Adolescent; D041923:Adolescent Development / Q000502:physiology*; D000679:Amygdala / Q000254:growth & development / Q000502:physiology; D001931:Brain Mapping; D002648:Child; D002657:Child Development / Q000502:physiology*; D002675:Child, Preschool; D003430:Cross-Sectional Studies; D004644:Emotions / Q000502:physiology*; D005260:Female; D006801:Humans; D007091:Image Processing, Computer-Assisted; D008137:Longitudinal Studies; D008279:Magnetic Resonance Imaging; D008297:Male; D009434:Neural Pathways / Q000254:growth & development; D017397:Prefrontal Cortex / Q000254:growth & development / Q000502:physiology; D012146:Rest / Q000502:physiology*
amygdala; development; prefrontal cortex; prospective; resting-state connectivity; stimulus-elicited connectivity