Strengthening of Top-Down Frontal Cognitive Control Networks Underlying the Development of Inhibitory Control: A Functional Magnetic Resonance Imaging Effective Connectivity Study
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The ability to voluntarily inhibit responses to task-irrelevant stimuli, which is a fundamental component of cognitive control, has a protracted development through adolescence. Previous human developmental imaging studies have found immaturities in localized brain activity in children and adolescents. However, little is known about how these regions integrate with age to form the distributed networks known to support cognitive control. In the present study, we used Granger causality analysis to characterize developmental changes in effective connectivity underlying inhibitory control (antisaccade task) compared with reflexive responses (prosaccade task) in human participants. By childhood, few top-down connectivities were evident with increased parietal interconnectivity. By adolescence, connections from prefrontal cortex increased and parietal interconnectivity decreased. From adolescence to adulthood, there was evidence of increased number and strength of frontal connections to cortical regions as well as subcortical regions. Together, results suggest that developmental improvements in inhibitory control may be supported by age-related enhancements in top-down effective connectivity between frontal, oculomotor, and subcortical regions.
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Effective integration of cognitive control processes relies not only on functional recruitment of implicated brain regions but also on the strength of connectivity among them.
“The effective integration of these processes relies not only on the functional recruitment of implicated brain regions, but also on the strength of connectivity among them (Hwang et al., 2010, van Belle et al., 2014).”
From The dual systems model: Review, reappraisal, and reaffirmation (2016) · cites this paper as Hwang et al., 2010
Connectivity between the prefrontal cortex and other cortical areas increases from childhood into adolescence, with some connections continuing to strengthen from adolescence to adulthood.
“connectivity between the prefrontal cortex and other cortical areas increased from childhood into adolescence, with some connections continuing to strengthen from adolescence to adulthood.”
From The dual systems model: Review, reappraisal, and reaffirmation (2016) · cites this paper as Hwang et al., 2010
Slightly posterior and ventral portions of the insula showed curvilinear thinning, similar to pruning patterns in reward-related regions such as the striatum.
“Meanwhile, slightly posterior and ventral portions of the insula evinced a curvilinear pattern of thinning, similar to pruning patterns found in reward-related regions (the striatum) [63].”
From The role of the anterior insula in adolescent decision making (2014) · cites this paper as [63]
PPC in childhood may support attentional modulation.
“PPC in childhood may support attentional modulation (Asplund et al., 2010) as has been found to be predominant at this age during AS performance (Hwang et al., 2010).”
From Effects of incentives, age, and behavior on brain activation during inhibitory control: a longitudinal fMRI study (2015) · cites this paper as Hwang et al., 2010
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Self-citationLongitudinal Growth Curves of Brain Function Underlying Inhibitory Control through Adolescence
Ordaz, S. J., Foran, W., Velanova, K., & Luna, B. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.1741-13.2013 · Cited by 302 · see citing works
Self-citationThe development of hub architecture in the human functional brain network
Hwang, K., Hallquist, M. N., & Luna, B. (2013) · Cerebral Cortex · doi:10.1093/cercor/bhs227 · Cited by 226 · see citing works
Self-citationDevelopmental changes in brain network hub connectivity in late adolescence
Baker, S. T. E., Lubman, D. I., Yucel, M., Allen, N. B., Whittle, S., Fulcher, B. D., Zalesky, A., & Fornito, A. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.5043-14.2015 · Cited by 168 · see citing works
Top-down regulation of default mode activity in spatial visual attention
Wen, X., Liu, Y., Yao, L., & Ding, M. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.4939-12.2013 · Cited by 150 · see citing works
Effects of alcohol use initiation on brain structure in typically developing adolescents
Luciana, M., Collins, P. F., Muetzel, R. L., & Lim, K. O. (2013) · The American Journal of Drug and Alcohol Abuse · doi:10.3109/00952990.2013.837057 · Cited by 145 · see citing works
Incentive Motivation, Cognitive Control, and the Adolescent Brain: Is It Time for a Paradigm Shift?
Luciana, M., & Collins, P. F. (2012) · Child Development Perspectives · doi:10.1111/j.1750-8606.2012.00252.x · Cited by 123 · see citing works
Vink, M., Zandbelt, B. B., Gladwin, T., Hillegers, M., Hoogendam, J. M., van den Wildenberg, W. P. M., Du Plessis, S., & Kahn, R. S. (2014) · Human Brain Mapping · doi:10.1002/hbm.22483 · Cited by 116 · see citing works
The role of the anterior insula in adolescent decision making
Smith, A. R., Steinberg, L., & Chein, J. (2014) · Developmental Neuroscience · doi:10.1159/000358918 · Cited by 110 · see citing works
The Teenage Brain: Cognitive Control and Motivation
Luna, B., Paulsen, D. J., Padmanabhan, A., & Geier, C. (2013) · Current Directions in Psychological Science · doi:10.1177/0963721413478416 · Cited by 92 · see citing works
Self-citationDevelopmental imaging genetics: Linking dopamine function to adolescent behavior
Padmanabhan, A., & Luna, B. (2014) · Brain and Cognition · doi:10.1016/j.bandc.2013.09.011 · Cited by 87 · see citing works
Self-citationPaulsen, D. J., Hallquist, M. N., Geier, C. F., & Luna, B. (2015) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2014.09.003 · Cited by 86 · see citing works
Self-citationAlahyane, N., Brien, D. C., Coe, B. C., Stroman, P. W., & Munoz, D. P. (2014) · NeuroImage · doi:10.1016/j.neuroimage.2014.03.008 · Cited by 68 · see citing works
Adolescent cognitive control, theta oscillations, and social observation
Buzzell, G. A., Barker, T. V., Troller-Renfree, S. V., Bernat, E. M., Bowers, M. E., Morales, S., Bowman, L. C., Henderson, H. A., Pine, D. S., & Fox, N. A. (2019) · NeuroImage · doi:10.1016/j.neuroimage.2019.04.077 · Cited by 65 · see citing works
Adolescent development of cortical oscillations: Power, phase, and support of cognitive maturation
Marek, S., Tervo-Clemmens, B., Klein, N., Foran, W., Ghuman, A. S., & Luna, B. (2018) · PLOS Biology · doi:10.1371/journal.pbio.2004188 · Cited by 48 · see citing works
Self-citationLydon‐Staley, D. M., & Geier, C. F. (2018) · Journal of Research on Adolescence · doi:10.1111/jora.12335 · Cited by 41 · see citing works
Feng, D., Yuan, K., Li, Y., Cai, C., Yin, J., Bi, Y., Cheng, J., Guan, Y., Shi, S., Yu, D., et al. (2016) · Brain Imaging and Behavior · doi:10.1007/s11682-015-9427-z · Cited by 34 · see citing works
- Authors
- Hwang, K., Velanova, K., & Luna, B.
- Affiliations
- University of Pittsburgh (US)
- ORCID
- Hwang, Kai
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2010-11-17
- Volume
- 30
- Issue
- 46
- Pages
- 15535-15545
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC2995693
- OpenAlex
- W2025651860
- Cited by
- 314
- References
- 89
- Citations by year
- 2026: 7 · 2025: 17 · 2024: 11 · 2023: 9 · 2022: 15 · 2021: 10 · 2020: 48 · 2019: 20 · 2018: 34 · 2017: 17 · 2016: 17 · 2015: 22 · 2014: 23 · 2013: 31 · 2012: 19
- FWCI
- 12.38
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Mental Health (MH-067924, K01MH082123, R01MH067924)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- inhibitory control, cognitive control, top-down connectivity, effective connectivity, developmental changes, adolescence, prefrontal cortex, parietal cortex, oculomotor control, antisaccade task, prosaccade task, subcortical structures, Granger causality
- MeSH terms
- Adolescent, Adult, Age Factors, Child, Female, Humans, Magnetic Resonance Imaging, Male, Nerve Net, Neural Inhibition, Neural Pathways, Psychomotor Performance, Prefrontal Cortex, Young Adult
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