Functional brain imaging across development.

paper Cited Public

Authors: Rubia, Katya
Year: 2013
Journal: European child & adolescent psychiatry
PMID: 22729957
DOI: 10.1007/s00787-012-0291-8
PMCID: PMC3853580

The developmental cognitive neuroscience literature has grown exponentially over the last decade. This paper reviews the functional magnetic resonance imaging (fMRI) literature on brain function development of typically late developing functions of cognitive and motivation control, timing and attention as well as of resting state neural networks. Evidence shows that between childhood and adulthood, concomitant with cognitive maturation, there is progressively increased functional activation in task-relevant lateral and medial frontal, striatal and parieto-temporal brain regions that mediate these higher level control functions. This is accompanied by progressively stronger functional inter-regional connectivity within task-relevant fronto-striatal and fronto-parieto-temporal networks. Negative age associations are observed in earlier developing posterior and limbic regions, suggesting a shift with age from the recruitment of "bottom-up" processing regions towards "top-down" fronto-cortical and fronto-subcortical connections, leading to a more mature, supervised cognition. The resting state fMRI literature further complements this evidence by showing progressively stronger deactivation with age in anti-correlated task-negative resting state networks, which is associated with better task performance. Furthermore, connectivity analyses during the resting state show that with development increasingly stronger long-range connections are being formed, for example, between fronto-parietal and fronto-cerebellar connections, in both task-positive networks and in task-negative default mode networks, together with progressively lesser short-range connections, suggesting progressive functional integration and segregation with age. Overall, evidence suggests that throughout development between childhood and adulthood, there is progressive refinement and integration of both task-positive fronto-cortical and fronto-subcortical activation and task-negative deactivation, leading to a more mature and controlled cognition.

Fig. 1

The figure shows areas that progressively increase in activation with age (orange) and areas that progressively decrease (blue) in activation with age between late childhood and adulthood (10–43 years) in a range of cognitive control tasks. Task-relevant frontal and/or fronto-striatal regions increase progressively with age in their activation while posterior and limbic areas showing negative age correlations. a Stop motor response inhibition task: left dorsal and inferior lateral as well as medial prefrontal areas, striato-thalamic and parietal activation increases linearly with age [27]. b Go/No-Go motor response inhibition task: medial and lateral frontal activation increases linearly with age [42]. c Simon (interference inhibition) task: predominantly left dorsolateral and inferior prefrontal as well as medial prefrontal activation together with striato-thalamic and temporo-parietal activation increases progressively with age [28]. d Switch task (cognitive flexibility): Bilateral dorsolateral and inferior prefrontal, medial frontal and striato-thalamic activation increases progressively with age [28]. e Performance monitoring (Stop failures): anterior cingulate and medial frontal together with superior temporal activation increases linearly with age [27] (color figure online)

Fig. 2

The figure illustrates areas that progressively increase in activation with age (orange) and areas that progressively decrease (blue) in activation with age between late childhood and adulthood (10–43 years) during tasks of attention and timing. A shift from medial to lateral frontal activation is observed during the two attention and time estimation tasks. a Time discrimination: progressively increased recruitment with age of left lateral prefrontal activation with diminishing recruitment of medial frontal activation [31]. b Attention allocation in an Oddball task: progressively more right and left lateral frontal and striatal areas are recruited with increasing age, with diminishing recruitment of medial frontal activation [35]. c Rewarded sustained attention task in a continuous performance task: progressively more right dorsal and inferior lateral prefrontal regions are recruited with increasing age with diminishing recruitment with age in medial frontal activation [32]. The reduction in medial frontal regions may also reflect enhanced deactivation of the default mode network (color figure online)

#	Section	Preview
20	Functional maturation of timing functions	In conclusion, it appears that during tasks of temporal processes, including motor timing, time…
21	Functional maturation of attention functions	Relatively few fMRI studies have investigated attention control functions, despite the fact that…
22	Functional maturation of attention functions	sacrificing speed, suggesting a less impulsive performance style in adults. Performance in this…
23	Functional maturation of attention functions	task performance [32]. Furthermore, linear age-associated activation decreases were observed in…
24	Functional maturation of motivation control	“Hot” executive functions, such as reward-related decision-making tasks, measure the impact of…
25	Functional maturation of motivation control	enhanced ventral striatal activation in adolescents relative to adults and children during reward…
26	Functional maturation of motivation control	While developmental activation changes in OFC and ACC have been inconsistent during reward-related…
27	Functional maturation of motivation control	commission errors and showed heightened activation in ventral striatum that was not observed during…
28	Sex by age interactions	Very few developmental imaging studies had the power to test for age by sex interactions. Two fMRI…
29	Sex by age interactions	range of 13–38 years during interference inhibition and switching [28]. Similarly, the…
30	Sex by age interactions	In summary, it seems that sex differences in the form or enhanced recruitment of fronto-striatal…
31	Sex by age interactions	Given that across all subjects, inferior frontal and striatal regions were positively…
32	Sex by age interactions	The finding of more mature frontal activation in females is in line with structural evidence of…
33	Sex by age interactions	These developmental age by sex interaction findings thus demonstrate that sex differences in…
34	Developmental functional connectivity studies	As mentioned, during cognitive tasks there is consistent evidence for enhanced inter-regional…
35	Developmental functional connectivity studies	Recent interest has been on the resting state or default mode network (DMN). The DMN consists of…
36	Developmental functional connectivity studies	Developmental neuroimaging studies of the DMN show that children as young as 1–2 year old show a…
37	Developmental functional connectivity studies	and 57 years [30]. The progressive age-associated deactivation of medial frontal DMN regions could…
38	Developmental functional connectivity studies	cognitive maturation [84]. An impactful recent study using multivariate pattern recognition analysis…
39	Conclusions and future directions	In conclusion, there is substantial evidence in the developmental cognitive neuroscience literature…

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Individual differences in amygdala volumes predict changes in functional connectivity between subcortical and cognitive control networks throughout adolescence.	Taylor BK et al.	—	2022	→
Neurofeedback for the Education of Children with ADHD and Specific Learning Disorders: A Review.	Patil AU et al.	—	2022	→
Neuroprotection in late life attention-deficit/hyperactivity disorder: A review of pharmacotherapy and phenotype across the lifespan.	Dutta CN et al.	—	2022	→
Neurotherapeutics for ADHD: Do they work?	Rubia K	—	2022	→
Relationships Between Regional Cerebral Blood Flow and Neurocognitive Outcomes in Children and Adolescents With Congenital Heart Disease.	Schmithorst VJ et al.	—	2022	→
Resting state networks mediate the association between both cardiovascular fitness and gross motor skills with neurocognitive functioning.	Meijer A et al.	—	2022	→
Structural and Functional Neural Correlates of Treatment Response for Interpersonal Psychotherapy for Depressed Adolescents.	Klimes-Dougan B et al.	—	2022	→
Systematic review of structural and functional neuroimaging studies of cannabis use in adolescence and emerging adulthood: evidence from 90 studies and 9441 participants.	Lichenstein SD et al.	—	2022	→
The impact of pubertal DHEA on the development of visuospatial oscillatory dynamics.	Fung MH et al.	—	2022	→
Training for Awareness, Resilience and Action (TARA) for medical students: a single-arm mixed methods feasibility study to evaluate TARA as an indicated intervention to prevent mental disorders and stress-related symptoms.	Ekbäck E et al.	—	2022	→
Biological Bases of Empathy and Social Cognition in Patients with Attention-Deficit/Hyperactivity Disorder: A Focus on Treatment with Psychostimulants.	Fantozzi P et al.	—	2021	→
Children with autism spectrum disorder show altered functional connectivity and abnormal maturation trajectories in response to inverted faces.	Mamashli F et al.	—	2021	→
Neurotherapeutics for Attention Deficit/Hyperactivity Disorder (ADHD): A Review.	Rubia K et al.	—	2021	→
Oxytocin, PTSD, and sexual abuse are associated with attention network intrinsic functional connectivity.	Crum KI et al.	—	2021	→
Selective Inhibitory Control in Middle Childhood.	Rincón-Pérez I et al.	—	2021	→
Sexually dimorphic development in the cortical oscillatory dynamics serving early visual processing.	Fung MH et al.	—	2021	→
The interplay of resting and inhibitory control-related theta-band activity depends on age.	Pscherer C et al.	—	2021	→
The Prisoner's Dilemma paradigm provides a neurobiological framework for the social decision cascade.	Thompson K et al.	—	2021	→
A Review of Default Mode Network Connectivity and Its Association With Social Cognition in Adolescents With Autism Spectrum Disorder and Early-Onset Psychosis.	Nair A et al.	—	2020	→
Early- Versus Adult-Onset Schizophrenia as a Predictor of Response to Neuroscience-Informed Cognitive Training.	Puig O et al.	—	2020	→
Functional MRI in Children: Current Clinical Applications.	Guerin JB et al.	—	2020	→
Heavy drinking in adolescents is associated with change in brainstem microstructure and reward sensitivity.	Galinowski A et al.	—	2020	→
Lateral Prefrontal Theta Oscillations Reflect Proactive Cognitive Control Impairment in Males With Attention Deficit Hyperactivity Disorder.	Zamorano F et al.	—	2020	→
Meta-analysis of the neural correlates of vigilant attention in children and adolescents.	Morandini HAE et al.	—	2020	→
Neural and behavioral correlates associated with adolescent marijuana use.	Subramaniam P et al.	—	2020	→
Neurofunctional and behavioural measures associated with fMRI-neurofeedback learning in adolescents with Attention-Deficit/Hyperactivity Disorder.	Lam SL et al.	—	2020	→
Neuropsychological Trajectories Associated with Adolescent Alcohol and Cannabis Use: A Prospective 14-Year Study.	Infante MA et al.	—	2020	→
Resting-state network dysconnectivity in ADHD: A system-neuroscience-based meta-analysis.	Sutcubasi B et al.	—	2020	→
Stimulus probability affects the visual N700 component of the event-related potential.	Althen H et al.	—	2020	→
Striatal bases of temporal discounting in early adolescents.	Hamilton KR et al.	—	2020	→
Adaptive control and the avoidance of cognitive control demands across development.	Niebaum JC et al.	—	2019	→
Conflict control of emotional and non-emotional conflicts in preadolescent children.	Liu T et al.	—	2019	→
Critical thinking and regional gray matter volume interact to predict representation connection in scientific problem solving.	Tong D et al.	—	2019	→
Developmental changes in resting-state functional networks among individuals with and without internalizing psychopathologies.	Burkhouse KL et al.	—	2019	→
Development of spatial suppression surrounding the focus of visual attention.	Wong-Kee-You AMB et al.	—	2019	→
Girls' attentive traits associate with cerebellar to dorsal attention and default mode network connectivity.	Rohr CS et al.	—	2019	→
Maturation changes the excitability and effective connectivity of the frontal lobe: A developmental TMS-EEG study.	Määttä S et al.	—	2019	→
Migraine in the Young Brain: Adolescents vs. Young Adults.	Colon E et al.	—	2019	→
Modulation of Resting Connectivity Between the Mesial Frontal Cortex and Basal Ganglia.	Popa T et al.	—	2019	→
Multiple causal pathways in attention-deficit/hyperactivity disorder - Do emerging executive and motivational deviations precede symptom development?	Pauli-Pott U et al.	—	2019	→
Serotonin Transporter Binding Potentials in Brain of Juvenile Monkeys 1 Year After Discontinuation of a 2-Year Treatment With Fluoxetine.	Golub MS et al.	—	2019	→
Social distance modulates the process of uncertain decision-making: evidence from event-related potentials.	Guo H et al.	—	2019	→
Adolescent alcohol exposure decreases frontostriatal resting-state functional connectivity in adulthood.	Broadwater MA et al.	—	2018	→
Altered Functional Connectivity of Fronto-Cingulo-Striatal Circuits during Error Monitoring in Adolescents with a History of Childhood Abuse.	Hart H et al.	—	2018	→
Altered neural processing of reward and punishment in adolescents with Major Depressive Disorder.	Landes I et al.	—	2018	→
A Neuroscience-Oriented Research Approach to Borderline Personality Disorder.	Stanley B et al.	—	2018	→
An fMRI study of coherent visual motion processing in children and adults.	Taylor CM et al.	—	2018	→
A systematic review of neuropsychological studies involving young binge drinkers.	Carbia C et al.	—	2018	→
Cognitive ability is associated with changes in the functional organization of the cognitive control brain network.	A Breukelaar I et al.	—	2018	→
Cognitive Neuroscience of Attention Deficit Hyperactivity Disorder (ADHD) and Its Clinical Translation.	Rubia K	—	2018	→
Differential patterns of age-related cortical and subcortical functional connectivity in 6-to-10 year old children: A connectome-wide association study.	Langen CD et al.	—	2018	→
Distinct Neurobehavioral Mechanisms for Expectancy Violation and Value Updating.	Das M et al.	—	2018	→
Effects of behavioral activation on default mode network connectivity in subthreshold depression: A preliminary resting-state fMRI study.	Yokoyama S et al.	—	2018	→
Feedback-related neurophysiology in children and their parents: Developmental differences, familial transmission, and relationship to error-monitoring.	Moser JS et al.	—	2018	→
[Formula: see text]A longitudinal analysis of the attention networks in 6- to 11-year-old children.	Lewis FC et al.	—	2018	→
From swing to cane: Sex differences of EEG resting-state temporal patterns during maturation and aging.	Tomescu MI et al.	—	2018	→
Identification of alterations associated with age in the clustering structure of functional brain networks.	Guzman GEC et al.	—	2018	→
Leveraging translational neuroscience to inform early intervention and addiction prevention for children exposed to early life stress.	Roos LE et al.	—	2018	→
Maternal Responsiveness as a Predictor of Self-Regulation Development and Attention-Deficit/Hyperactivity Symptoms Across Preschool Ages.	Pauli-Pott U et al.	—	2018	→
Mind wandering perspective on attention-deficit/hyperactivity disorder.	Bozhilova NS et al.	—	2018	→
Neural activity patterns between different executive tasks are more similar in adulthood than in adolescence.	Moisala M et al.	—	2018	→
Neural Mechanisms of Early-Life Social Stress as a Developmental Risk Factor for Severe Psychiatric Disorders.	Reinwald JR et al.	—	2018	→
Novel in silico multivariate mapping of intrinsic and anticorrelated connectivity to neurocognitive functional maps supports the maturational hypothesis of ADHD.	de Lacy N et al.	—	2018	→
On the relation between theory of mind and executive functioning: A developmental cognitive neuroscience perspective.	Wade M et al.	—	2018	→
Quality of maternal behaviour during infancy predicts functional connectivity between default mode network and salience network 9 years later.	Dégeilh F et al.	—	2018	→
The Lifespan Human Connectome Project in Development: A large-scale study of brain connectivity development in 5-21 year olds.	Somerville LH et al.	—	2018	→
A KCNJ6 gene polymorphism modulates theta oscillations during reward processing.	Kamarajan C et al.	—	2017	→
Alcohol Binge Drinking and Executive Functioning during Adolescent Brain Development.	Gil-Hernandez S et al.	—	2017	→
A one-week 5-choice serial reaction time task to measure impulsivity and attention in adult and adolescent mice.	Remmelink E et al.	—	2017	→
Beyond stereotypes of adolescent risk taking: Placing the adolescent brain in developmental context.	Romer D et al.	—	2017	→
Brain functional connectivity patterns in children and adolescents with gender dysphoria: Sex-atypical or not?	Nota NM et al.	—	2017	→
Docosahexaenoic acid biostatus is associated with event-related functional connectivity in cortical attention networks of typically developing children.	Almeida DM et al.	—	2017	→
Evidence of substantial development of inhibitory control and sustained attention between 6 and 8years of age on an unpredictable Go/No-Go task.	Lewis FC et al.	—	2017	→
Functional Connectivity of the Dorsal Attention Network Predicts Selective Attention in 4-7 year-old Girls.	Rohr CS et al.	—	2017	→
Genetic correlates of the development of theta event related oscillations in adolescents and young adults.	Chorlian DB et al.	—	2017	→
Heritability of brain activity related to response inhibition: A longitudinal genetic study in adolescent twins.	Anokhin AP et al.	—	2017	→
Increased default-mode variability is related to reduced task-performance and is evident in adults with ADHD.	Mowinckel AM et al.	—	2017	→
Intrinsic functional connectivity of fronto-temporal networks in adolescents with early psychosis.	Solé-Padullés C et al.	—	2017	→
Lateral prefrontal activity as a compensatory strategy for deficits of cortical processing in Attention Deficit Hyperactivity Disorder.	Zamorano F et al.	—	2017	→
Motor Learning Induces Plasticity in the Resting Brain-Drumming Up a Connection.	Amad A et al.	—	2017	→
Preparatory Engagement of Cognitive Control Networks Increases Late in Childhood.	Church JA et al.	—	2017	→
Recent theoretical, neural, and clinical advances in sustained attention research.	Fortenbaugh FC et al.	—	2017	→
Reduced functional connectivity of fronto-parietal sustained attention networks in severe childhood abuse.	Hart H et al.	—	2017	→
Shared and disorder-specific task-positive and default mode network dysfunctions during sustained attention in paediatric Attention-Deficit/Hyperactivity Disorder and obsessive/compulsive disorder.	Norman LJ et al.	—	2017	→
Sustained attention to a predictable, unengaging Go/No-Go task shows ongoing development between 6 and 11 years.	Lewis FC et al.	—	2017	→
The Nature of the Relationship between Anxiety and the Error-Related Negativity across Development.	Moser JS	—	2017	→
Time dilation in children and adults: The idea of a slower internal clock in young children tested with different click frequencies.	Droit-Volet S	—	2017	→
Working memory over a six-year period in young binge drinkers.	Carbia C et al.	—	2017	→
Adolescent Emotional Maturation through Divergent Models of Brain Organization.	Oron Semper JV et al.	—	2016	→
Assessing Executive Functions in Preschoolers Using Shape School Task.	Nieto M et al.	—	2016	→
Development of brain networks and relevance of environmental and genetic factors: A systematic review.	Richmond S et al.	—	2016	→
Factor structure of the Behavior Rating Inventory of Executive Functions (BRIEF-P) at age three years.	Skogan AH et al.	—	2016	→
Intrinsic connectivity networks from childhood to late adolescence: Effects of age and sex.	Solé-Padullés C et al.	—	2016	→
Language at rest: A longitudinal study of intrinsic functional connectivity in preterm children.	Rowlands MA et al.	—	2016	→
Maturation of interhemispheric signal propagation in autism spectrum disorder and typically developing controls: a TMS-EEG study.	Jarczok TA et al.	—	2016	→
Neural Correlates of Response Inhibition in Adolescents Prospectively Predict Regular Tobacco Smoking.	Anokhin AP et al.	—	2016	→
Neural Correlates of Reward Processing in Typical and Atypical Development.	Duerden EG et al.	—	2016	→
Neurofunctional Abnormalities during Sustained Attention in Severe Childhood Abuse.	Lim L et al.	—	2016	→
Neuropsychological profile in new-onset benign epilepsy with centrotemporal spikes (BECTS): Focusing on executive functions.	Filippini M et al.	—	2016	→
The contributions of resting state and task-based functional connectivity studies to our understanding of adolescent brain network maturation.	Stevens MC	—	2016	→
The Health Consequences of Obesity in Young Adulthood.	Cheng HL et al.	—	2016	→
Advances in pediatric neuroimaging.	Krishnan P et al.	—	2015	→
Asymmetric development of dorsal and ventral attention networks in the human brain.	Farrant K et al.	—	2015	→
Cognitive abilities required in time judgment depending on the temporal tasks used: A comparison of children and adults.	Droit-Volet S et al.	—	2015	→
Cognitive emotion regulation in children: Reappraisal of emotional faces modulates neural source activity in a frontoparietal network.	Wessing I et al.	—	2015	→
Developmental Trajectories for Visuo-Spatial Attention are Altered by Prenatal Alcohol Exposure: A Longitudinal FMRI Study.	Gautam P et al.	—	2015	→
fMRI functional connectivity applied to adolescent neurodevelopment.	Ernst M et al.	—	2015	→
Functional brain connectome and sensorimotor networks in rolandic epilepsy.	Xiao F et al.	—	2015	→
Gender modulates the development of theta event related oscillations in adolescents and young adults.	Chorlian DB et al.	—	2015	→
Intergenerational transmission of self-regulation: A multidisciplinary review and integrative conceptual framework.	Bridgett DJ et al.	—	2015	→
Neural Correlates of Error Processing in Young People With a History of Severe Childhood Abuse: An fMRI Study.	Lim L et al.	—	2015	→
Predictability and context determine differences in conflict monitoring between adolescence and adulthood.	Chmielewski WX et al.	—	2015	→
Regional homogeneity of resting-state brain abnormalities in violent juvenile offenders: a biomarker of brain immaturity?	Chen C et al.	—	2015	→
Sensation-to-cognition cortical streams in attention-deficit/hyperactivity disorder.	Carmona S et al.	—	2015	→
Specific functional connectivity alterations of the dorsal striatum in young people with depression.	Kerestes R et al.	—	2015	→
Time windows matter in ADHD-related developing neuropsychological basic deficits: A comprehensive review and meta-regression analysis.	Pauli-Pott U et al.	—	2015	→
Variation in functional connectivity along anterior-to-posterior intraparietal sulcus, and relationship with age across late childhood and adolescence.	Vinette SA et al.	—	2015	→
An eight month randomized controlled exercise intervention alters resting state synchrony in overweight children.	Krafft CE et al.	—	2014	→
Developmental changes in effective connectivity associated with relational reasoning.	Bazargani N et al.	—	2014	→
Developmental changes in the reward positivity: an electrophysiological trajectory of reward processing.	Lukie CN et al.	—	2014	→
Development of impulse control circuitry in children of alcoholics.	Hardee JE et al.	—	2014	→
Effects of prenatal alcohol exposure on the development of white matter volume and change in executive function.	Gautam P et al.	—	2014	→
Functional brain imaging studies of youth depression: a systematic review.	Kerestes R et al.	—	2014	→
Imaging the ADHD brain: disorder-specificity, medication effects and clinical translation.	Rubia K et al.	—	2014	→
Neurodevelopmental changes in the responsiveness of systems involved in top down attention and emotional responding.	Hwang S et al.	—	2014	→
Optimized simultaneous ASL and BOLD functional imaging of the whole brain.	Schmithorst VJ et al.	—	2014	→
Pattern classification of response inhibition in ADHD: toward the development of neurobiological markers for ADHD.	Hart H et al.	—	2014	→
Research updates in neuroimaging studies of children who stutter.	Chang SE	—	2014	→
The development of an RDoC-based treatment program for adolescent depression: "Training for Awareness, Resilience, and Action" (TARA).	Henje Blom E et al.	—	2014	→
The development of the neural substrates of cognitive control in adolescents with autism spectrum disorders.	Solomon M et al.	—	2014	→
The small-world organization of large-scale brain systems and relationships with subcortical structures.	Koziol LF et al.	—	2014	→
Young children's difficulties in switching from rhythm production to temporal interval production (>1 s).	Bobin-Bègue A et al.	—	2014	→
Brain imaging: closing the gap between basic research and clinical application is urgently needed.	Buitelaar JK et al.	—	2013	→
Conditioned pain modulation in children and adolescents: effects of sex and age.	Tsao JC et al.	—	2013	→
Effects of age and gender on neural networks of motor response inhibition: from adolescence to mid-adulthood.	Rubia K et al.	—	2013	→
Performance monitoring in children and adolescents: a review of developmental changes in the error-related negativity and brain maturation.	Tamnes CK et al.	—	2013	→
Reduced functional integration of the sensorimotor and language network in rolandic epilepsy.	Besseling RM et al.	—	2013	→
Traumatic brain injury, neuroimaging, and neurodegeneration.	Bigler ED	—	2013	→