Elsevier

NeuroImage

Volume 124, Part A, 1 January 2016, Pages 409-420
NeuroImage

Testing a dual-systems model of adolescent brain development using resting-state connectivity analyses

https://doi.org/10.1016/j.neuroimage.2015.04.069Get rights and content

Highlights

  • We tested age-related changes in intrinsic functional connectivity across adolescence.

  • Strengthening of subcortical and prefrontal-cortical connections was observed over age.

  • Increasing independence of prefrontal and motor connections was observed over age.

  • These changes in functional connectivity strength related to changes in behavior.

  • These findings highlight neural circuit changes across adolescence.

Abstract

The current study aimed to test a dual-systems model of adolescent brain development by studying changes in intrinsic functional connectivity within and across networks typically associated with cognitive-control and affective-motivational processes. To this end, resting-state and task-related fMRI data were collected of 269 participants (ages 8–25). Resting-state analyses focused on seeds derived from task-related neural activation in the same participants: the dorsal lateral prefrontal cortex (dlPFC) from a cognitive rule-learning paradigm and the nucleus accumbens (NAcc) from a reward-paradigm. Whole-brain seed-based resting-state analyses showed an age-related increase in dlPFC connectivity with the caudate and thalamus, and an age-related decrease in connectivity with the (pre)motor cortex. nAcc connectivity showed a strengthening of connectivity with the dorsal anterior cingulate cortex (ACC) and subcortical structures such as the hippocampus, and a specific age-related decrease in connectivity with the ventral medial PFC (vmPFC). Behavioral measures from both functional paradigms correlated with resting-state connectivity strength with their respective seed. That is, age-related change in learning performance was mediated by connectivity between the dlPFC and thalamus, and age-related change in winning pleasure was mediated by connectivity between the nAcc and vmPFC. These patterns indicate (i) strengthening of connectivity between regions that support control and learning, (ii) more independent functioning of regions that support motor and control networks, and (iii) more independent functioning of regions that support motivation and valuation networks with age. These results are interpreted vis-à-vis a dual-systems model of adolescent brain development.

Section snippets

Participants

Participants were recruited through local schools and advertisements (N = 299; ages 8–25). All participants provided written informed consent for the study (parental consent and participant assent for children and adolescents). Participants were screened for MRI contra indications and had no history of neurological or psychiatric disorders. All anatomical MRI scans were reviewed and cleared by a radiologist from the radiology department of the Leiden University Medical Center. No anomalous

Age related changes in functional connectivity with dlPFC

The first question we addressed was whether connectivity with the dlPFC changed across age. The bilateral dlPFC seed revealed a linear age-related increase in functional connectivity with subcortical regions such as the bilateral caudate, putamen, and thalamus, and with cortical regions such as the bilateral insula and inferior frontal gryus (see Fig. 1, Fig. 3, and Table 2). A linear age-related decrease in functional connectivity was observed with the pre-SMA, motor cortex, and precuneus (see

Discussion

Adolescent brain development has been described by a dual-systems model, suggesting an imbalance between an early maturing, limbic, affective-motivational system, together with a relatively late developing cortical-control system (Somerville et al., 2010, Casey et al., 2008, Casey, 2015). The current study aimed to test this model by studying changes in intrinsic functional connectivity within and across networks typically associated with cognitive-control and affective-motivational processes.

Acknowledgment

This work was supported by a grant from the European Research Counsel (ERC Innovative Ideas) awarded to E.A.C (ERC-2010-StG-263234).

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