What has fMRI told us about the Development of Cognitive Control through Adolescence?

doi:10.1016/j.bandc.2009.08.005

Brain and Cognition

Volume 72, Issue 1, February 2010, Pages 101-113

https://doi.org/10.1016/j.bandc.2009.08.005 Get rights and content

Abstract

Cognitive control, the ability to voluntarily guide our behavior, continues to improve throughout adolescence. Below we review the literature on age-related changes in brain function related to response inhibition and working memory, which support cognitive control. Findings from studies using functional magnetic resonance imaging (fMRI) indicate that processing errors, sustaining a cognitive control state, and reaching adult levels of precision, persist through adolescence. Developmental changes in patterns of brain function suggest that core regions of the circuitry underlying cognitive control are on-line early in development. However, age-related changes in localized processes across the brain, and in establishing long range connections that support top-down modulation of behavior, more effective neural processing for optimal mature executive function. While great progress has been made in understanding the age-related changes in brain processes underlying cognitive development, there are still important challenges in developmental neuroimaging methods and the interpretation of data that need to be addressed.

Introduction

Adolescence is a period when many aspects of decision-making appear adult-like, yet adolescents’ decisions are inconsistent, and this often leads to suboptimal or even dangerous behavior. The ability to voluntarily guide behavior in a goal-directed fashion is essential to mature decision making. Cognitive control and executive function are terms used to describe the processes that allow us to voluntarily guide our behavior. While adolescents can exhibit sophisticated voluntary behavior, the ability to do so consistently continues to improve during adolescence, making cognitive control a particularly useful model for investigating the vulnerabilities of this period. Characterizing the brain circuitry underlying immaturities in cognitive control can elucidate the important aspects of the neural basis of decision making in adolescence. This paper reviews how typical adolescents differ from adults on two fundamental aspects of cognitive control – response inhibition and working memory (Fuster, 1997b). Response inhibition refers to the ability to voluntarily select a task-appropriate, goal-directed response while suppressing a more compelling but task-inappropriate response. Working memory refers to the mental ‘sketch pad’ that allows us to retain relevant information on-line in order to make a planned, goal-directed response. While these processes work together to support goal driven behavior (Miller & Cohen, 2001), they can be considered independently to characterize specific profiles of cognitive development (Demetriou et al., 2002, Luna et al., 2004).

Major psychopathology can often emerge or intensify during adolescence, indicating that there are vulnerabilities inherent to this developmental transition that may contribute to mental disorders. Additionally, cognitive control is usually compromised in major psychopathology (Luna and Sweeney, 2004a, Sweeney et al., 2004). This suggests that investigating neurocognitive development can serve as a way to probe the integrity of complex brain circuitries associated with psychopathology. For example, if the maturation of long-range connectivity in the brain proves to be important for the late developmental improvements in cognitive control, these processes may be compromised in psychopathology. Additionally, normative adolescence is also characterized by a peak in sensation-seeking that can lead to risk-taking behavior that undermines survival (Chambers et al., 2003, Spear, 2000). Delineating the normative processes that underlie the improvement in cognitive control from adolescence to adulthood provides a template for understanding the neurobehavioral basis of both psychopathology and risk-taking behavior.

Given that behavior is the result of both environmental and biological influences, the ability to assess their association is optimal for characterizing developmental change. Neuroimaging methods provide one approach to investigate concurrent changes in brain and behavior. Functional Magnetic Resonance Imaging (fMRI) is particularly appropriate for developmental studies because it is non-invasive and allows the assessment of brain function relevant for a specific behavior. However, the interpretation of developmental neuroimaging results differs from that of adult neuroimaging studies, because results from younger individuals must be considered in the context of brain function in adulthood. That is, we identify immaturities in brain function in young individuals by comparing them to results in mature adult populations. In this paper, we review the literature characterizing age-related changes in brain function underlying cognitive control of behavior through adolescence. We consider studies that have focused on voluntary response inhibition and those that measure changes in response to working memory demands. We end by discussing methodological issues that are specific to interpreting developmental fMRI results.

Section snippets

The development of cognitive control

Voluntary planned behavior requires the ability to retain online the goal of the response (working memory), to plan and prepare the response, and the ability to suppress task irrelevant responses in order to make a task-appropriate response (response inhibition). In this section, we review how basic components of cognitive control (response inhibition and working memory) change during childhood and adolescence, focusing on neuroimaging studies examining changes in brain function.

Response inhibition

Response inhibition is central to the voluntary control of behavior, providing the flexibility needed for behavior to be guided by a task goal (Davidson et al., 2006, Fuster, 1997b, Miller and Cohen, 2001). As in real life, what is being inhibited varies across experimental tasks – it may be extremely prepotent, such as reflexive responses to external stimuli (e.g., antisaccade task), or a learned automatic response (e.g., go-no-go task). The most frequently used tasks include the go-no-go,

Working memory

Voluntary responses require the ability to maintain a representation of the rules that will guide behavior in working memory (Baddeley, 1986). Much like response inhibition, working memory is a central component of executive function (Fuster, 1997b, Miller and Cohen, 2001) and has a protracted developmental trajectory through adolescence (Demetriou et al., 2002, Luna et al., 2004). Studies have shown that at both the behavioral and neural levels, fundamental working memory skills and their

Development of integrated systems level circuitry

Studies delineating age-related changes in both response inhibition and working memory find that there are enhancements in the recruitment of widespread regions outside of PFC, including parietal, temporal, subcortical and cerebellar regions, with age (Bunge et al., 2002, Crone et al., 2006, Luna et al., 2001, O’Hare et al., 2008, Rubia et al., 2006). Indeed, PFC may be engaged only when other circuitries cannot support processing (Hazy, Frank, & O’Reilly, 2007). PFC allows the active

Considerations in interpreting developmental neuroimaging results

While great strides have been made in understanding age-related changes in brain processes underlying cognitive development, there are still important challenges that we need to address regarding methods and the interpretation of data. A crucial feature of developmental neuroimaging studies is that adults are considered the model system. Therefore, any deviation from adult brain activity is interpreted as an immaturity. This particular aspect of interpreting developmental results can be viewed

Direction of developmental differences

When age groups differ in activation, qualitatively different processes may be involved, each with distinct interpretations. One common result is that the younger group demonstrates an increased magnitude of activity compared to adults in an equivalent region. When the same circuitry as adults is being accessed by younger subjects, but the younger subjects show higher activity, this is often interpreted as indicating that greater effort is required for younger subjects to do the task (Luna et

Conclusions

The developmental fMRI literature characterizing age-related differences in cognitive control includes a range of methodological approaches. This work has generated diverse findings that still share some important consistencies. As has been proposed in the literature, prefrontal systems play a primary role in executive processes and have a protracted development (much like other association areas) into adolescence. Studies therefore have used PFC as an a priori region of interest and have shown

References (99)

N.E. Adleman et al.
A developmental fMRI study of the Stroop color-word task
NeuroImage
(2002)
D. Amso et al.
Selection and inhibition in infancy: Evidence from the spatial negative priming paradigm
Cognition
(2005)
D.F. Bjorklund et al.
The resources construct in cognitive development: Diverse sources of evidence and a theory of inefficient inhibition
Developmental Review
(1990)
S.A. Bunge et al.
Immature frontal lobe contributions to cognitive control in children: Evidence from fMRI
Neuron
(2002)
B.J. Casey et al.
Activation of prefrontal cortex in children during a nonspatial working memory task with functional MRI
NeuroImage
(1995)
B.J. Casey et al.
Imaging the developing brain: What have we learned about cognitive development?
Trends in Cognitive Sciences
(2005)
K.T. Ciesielski et al.
Developmental neural networks in children performing a Categorical N-Back Task
NeuroImage
(2006)
N. Cowan et al.
Development of working memory for verbal–spatial associations
Journal of Memory and Language
(2006)
M. D’Esposito et al.
Maintenance versus manipulation of information held in working memory: An event-related fMRI study
Brain and Cognition
(1999)
M.C. Davidson et al.
Development of cognitive control and executive functions from 4 to 13 years: Evidence from manipulations of memory, inhibition, and task switching
Neuropsychologia
(2006)

N.U. Dosenbach et al.

A core system for the implementation of task sets

Neuron

(2006)

S. Everling et al.

The antisaccade: A review of basic research and clinical studies

Neuropsychologia

(1998)

B. Fischer et al.

On the development of voluntary and reflexive components in human saccade generation

Brain Research

(1997)

J. Fukushima et al.

Development of voluntary control of saccadic eye movements. I. Age-related changes in normal children

Brain & Development

(2000)

S. Funahashi et al.

Delay-period activity in the primate prefrontal cortex encoding multiple spatial positions and their order of presentation

Behavioural Brain Research

(1997)

J.M. Fuster

Network memory

Trends in Neurosciences

(1997)

C.F. Geier et al.

Circuitry underlying temporally extended spatial working memory

Neuoimage

(2007)

C. Geier et al.

The maturation of incentive processing and cognitive control

Pharmacology, Biochemistry and Behavior

(2009)

P.R. Huttenlocher

Morphometric study of human cerebral cortex development

Neuropsychologia

(1990)

H.C. Kang et al.

Comparison of functional activation foci in children and adults using a common stereotactic space

NeuroImage

(2003)

A. Kok

Varieties of inhibition: Manifestations in cognition, event-related potentials and aging

Acta Psychologica

(1999)

B. Luna et al.

Maturation of widely distributed brain function subserves cognitive development

NeuroImage

(2001)

E.D. O’Hare et al.

Neurodevelopmental changes in verbal working memory load-dependency: An fMRI investigation

NeuroImage

(2008)

P.J. Olesen et al.

Combined analysis of DTI and fMRI data reveals a joint maturation of white and grey matter in a fronto-parietal network

Cognitive Brain Research

(2003)

D. Passingham et al.

The prefrontal cortex and working memory: Physiology and brain imaging

Current Opinion in Neurobiology

(2004)

K.R. Ridderinkhof et al.

Sources of interference from irrelevant information: A developmental study

Journal of Experimental Child Psychology

(1997)

K. Rubia et al.

Functional frontalisation with age: Mapping neurodevelopmental trajectories with fMRI

Neuroscience and Biobehavioral Reviews

(2000)

M. Sakagami et al.

Functional role of the ventrolateral prefrontal cortex in decision making

Current Opinion in Neurobiology

(2007)

L.P. Spear

The adolescent brain and age-related behavioral manifestations

Neuroscience and Biobehavioral Reviews

(2000)

M.C. Stevens et al.

Functional neural networks underlying response inhibition in adolescents and adults

Behavioural Brain Research

(2007)

L. Tamm et al.

Maturation of brain function associated with response inhibition

Journal of the American Academy of Child and Adolescent Psychiatry

(2002)

K.M. Thomas et al.

A developmental functional MRI study of spatial working memory

NeuroImage

(1999)

S.P. Tipper et al.

Mechanisms of attention: A developmental study

Journal of Experimental Child Psychology

(1989)

L.G. Ungerleider et al.

Imaging brain plasticity during motor skill learning

Neurobiology of Learning and Memory

(2002)

W.P.M. Van den Wildenberg et al.

Developmental trends in simple and selective inhibition of compatible and incompatible responses

Journal of Experimental Child Psychology

(2004)

A. Baddeley

Working memory

(1986)

A.C. Bedard et al.

The development of selective inhibitory control across the life span

Developmental Neuropsychology

(2002)

M.A. Bell et al.

The relations between frontal brain electrical activity and cognitive development during infancy

Child Development

(1992)

T.S. Braver et al.

Anterior cingulate cortex and response conflict: Effects of frequency, inhibition and errors

Cerebral Cortex

(2001)

S.A. Bunge et al.

Neural circuitry underlying rule use in humans and nonhuman primates

The Journal of Neuroscience

(2005)

C.S. Carter et al.

Anterior cingulate cortex, error detection, and the online monitoring of performance

Science

(1998)

B.J. Casey et al.

A developmental functional MRI study of prefrontal activation during performance of a go-no-go task

Journal of Cognitive Neuroscience

(1997)

V.S. Caviness et al.

The human brain age 7–11 years: A volumetric analysis based on magnetic resonance images

Cerebral Cortex

(1996)

R.A. Chambers et al.

Developmental neurocircuitry of motivation in adolescence: A critical period of addiction vulnerability

American Journal of Psychiatry

(2003)

S.M. Courtney et al.

An area specialized for spatial working memory in human frontal cortex

Science

(1998)

E.A. Crone et al.

Neurocognitive development of the ability to manipulate information in working memory

Proceedings of the National Academy of Sciences of the United States of America

(2006)

C.E. Curtis et al.

Maintenance of spatial and motor codes during oculomotor delayed response tasks

Journal of Neuroscience

(2004)

C.R. DeLuca et al.

Normative data from the Cantab: I. Development of executive function over the lifespan

Journal of Clinical & Experimental Neuropsychology

(2003)

A. Demetriou et al.

The development of mental processing: Efficiency, working memory, and thinking

Monographs of the Society for Research in Child Development

(2002)

Cited by (603)

Behavioral and neural responses to social rejection: Individual differences in developmental trajectories across childhood and adolescence
2024, Developmental Cognitive Neuroscience
Dealing with social rejection is challenging, especially during childhood when behavioral and neural responses to social rejection are still developing. In the current longitudinal study, we used a Bayesian multilevel growth curve model to describe individual differences in the development of behavioral and neural responses to social rejection in a large sample (n > 500). We found a peak in aggression following negative feedback (compared to neutral feedback) during late childhood, as well as individual differences during this developmental phase, possibly suggesting a sensitive window for dealing with social rejection across late childhood. Moreover, we found evidence for individual differences in the linear development of neural responses to social rejection in our three brain regions of interest: The anterior insula, the medial prefrontal cortex, and the dorsolateral prefrontal cortex. In addition to providing insights in the individual trajectories of dealing with social rejection during childhood, this study also makes a meaningful methodological contribution: Our statistical analysis strategy (and can be found in this study’s online supplementary materials at https://jeroendmulder.github.io/social-emotion-regulation/) can be used as an example on how to take into account the many complexities of developmental neuroimaging datasets, while still enabling researchers to answer interesting questions about individual-level relationships.
Enhancing cognitive control with transcranial magnetic stimulation in subject-specific frontoparietal networks
2024, Cortex
Cognitive control processes, including those involving frontoparietal networks, are highly variable between individuals, posing challenges to basic and clinical sciences. While distinct frontoparietal networks have been associated with specific cognitive control functions such as switching, inhibition, and working memory updating functions, there have been few basic tests of the role of these networks at the individual level.
To examine the role of cognitive control at the individual level, we conducted a within-subject excitatory transcranial magnetic stimulation (TMS) study in 19 healthy individuals that targeted intrinsic (“resting”) frontoparietal networks. Person-specific intrinsic networks were identified with resting state functional magnetic resonance imaging scans to determine TMS targets. The participants performed three cognitive control tasks: an adapted Navon figure-ground task (requiring set switching), n-back (working memory), and Stroop color-word (inhibition).
Hypothesis: We predicted that stimulating a network associated with externally oriented control [the “FPCN-B” (fronto-parietal control network)] would improve performance on the set switching and working memory task relative to a network associated with attention (the Dorsal Attention Network, DAN) and cranial vertex in a full within-subjects crossover design.
We found that set switching performance was enhanced by FPCN-B stimulation along with some evidence of enhancement in the higher-demand n-back conditions.
Higher task demands or proactive control might be a distinguishing role of the FPCN-B, and personalized intrinsic network targeting is feasible in TMS designs.
Early life interpersonal stress and depression: Social reward processing as a potential mediator
2024, Progress in Neuro-Psychopharmacology and Biological Psychiatry
Experiencing stressful events early in life is lamentably very common and widespread across the globe. Despite the strong link between experiencing such stress and developing depression, the mechanisms underlying this association remain unclear. This review addresses this critical question by drawing focus to “early life interpersonal stress” (ELIS), or stressful experiences that occur within the context of a relationship where there is close, direct interaction. Recent evidence suggests that ELIS uniquely relates to depression. A growing body of work demonstrates that ELIS impacts how youth respond to social reward (e.g., positive social stimuli/ feedback). Similar social reward-related impairments are noted in youth with depression. The current review synthesizes these two disparate, yet related, bodies of literature examining the relations between a) ELIS and neurobehavioral alterations in social reward processing; and b) behavioral and neural processing of social reward in depression. A preliminary model presents neurobehavioral disruptions in social reward processing as one mediating factor underlying the connection between ELIS and depression. Key limitations and future directions are discussed.
Changes in Brain Network Connections After Exposure and Response Prevention Therapy for Obsessive-Compulsive Disorder in Adolescents and Adults
2024, Biological Psychiatry: Cognitive Neuroscience and Neuroimaging
Functional alterations of tripartite neural networks during cognitive control (i.e., frontoparietal network [FPN], cingulo-opercular network, and default mode network) occur in patients with obsessive-compulsive disorder (OCD) and may contribute to illness expression. However, the degree to which changes in these networks are elicited by gold standard treatment (e.g., exposure and response prevention [EX/RP]) remains unknown. Understanding how EX/RP modulates network connectivity in adolescent versus adult patients with OCD may aid the identification of developmentally sensitive treatment targets that enhance cognitive control.
Data from a total of 169 adolescents (13–17 years) and adults (25–40 years; 57% female) were analyzed, including healthy control participants (n = 58) and patients with OCD (n = 111) who were randomized to either EX/RP or an active control therapy (stress management training). Participants performed a flanker task during functional magnetic resonance imaging pre- and posttreatment. To retain sensitivity to individual differences in connectivity, group iterative multiple model estimation was used to assess functional connectivity (i.e., density) within and between brain networks.
Significant increases in FPN density and decreases in FPN–default mode network density were observed from pre- to posttreatment in patients who received EX/RP. The opposite patterns of change occurred in patients who received stress management training. These treatment-related changes in network density did not differ across age group.
Results suggest EX/RP-specific changes in task-based connectivity in patients with OCD. Given baseline differences between healthy control participants and patients by age group, these treatment-related changes may indicate restoration of healthy FPN and default mode network development across patients, providing targets for improving response to EX/RP.
Neural Correlates of the p Factor in Adolescence: Cognitive Control With and Without Enhanced Positive Affective Demands
2024, Biological Psychiatry: Cognitive Neuroscience and Neuroimaging
Recent research has aimed to characterize processes underlying general liability toward psychopathology, termed the p factor. Given previous research linking the p factor with difficulties in both executive functioning and affective regulation, the present study investigated nonaffective and positive affective inhibition in the context of a sustained attention/inhibition paradigm in adolescents exhibiting mild to severe psychopathology.
Functional magnetic resonance imaging data were collected during an integrated reward conditioning and go/no-go task in 138 adolescents assigned female at birth. We modeled the p factor using hierarchical confirmatory factor analysis. Positive affective inhibition was measured by examining responses to no-go stimuli with a history of reward conditioning. We examined associations between p factor scores and neural function and behavioral performance.
Consistent with nonaffective executive function as a primary risk factor, p factor scores were associated with worse behavioral performance and hypoactivation in the left superior frontal gyrus and middle frontal gyrus during response initiation (go trials). The p factor scores were additionally associated with increased error-related signaling in the temporal cortex during incorrect no-go trials.
During adolescence, a period characterized by heightened risk for emergent psychopathology, we observed unique associations between p factor scores and neural and behavioral indices of response initiation, which relies primarily on sustained attention. These findings suggest that shared variation in mental disorder categories is characterized in part by sustained attention deficits. While we did not find evidence that the p factor was associated with inhibition in this study, this observation is consistent with our hypothesis that the p factor would be related to nonaffective control processes.
The influence of ultra-processed food consumption on reward processing and energy intake: Background, design, and methods of a controlled feeding trial in adolescents and young adults
2023, Contemporary Clinical Trials
The greatest age-related weight gain occurs in the early/mid-20s. Overall dietary quality among adolescents and emerging adults (age 18–25) is poor, with ultra-processed foods (UPF) representing more than two-thirds of adolescents' total energy intake (i.e., 68%). UPF consumption may impact cognitive and neurobiological factors that influence dietary decision-making and energy intake (EI). To date, no research has addressed this in this population.
Participants aged 18–25 will undergo two 14-day controlled feeding periods (81% UPF, 0% UPF) using a randomly assigned crossover design, with a 4-week washout between conditions. Brain response to a UPF-rich milkshake, as well as behavioral measures of executive function, will be evaluated before and after each diet. Following each diet, measurements include ad libitum buffet meal EI, food selection, eating rate, and eating in the absence of hunger (EAH). Prior to initiating recruitment, controlled diet menus, buffet, and EAH snacks were developed and evaluated for palatability. Sensory and texture attributes of buffet and EAH snack foods were also evaluated.
Overall diet palatability was rated “like very much” (8)/”like moderately”(7) (UPF: 7.6 ± 1.0; Non-UPF: 6.8 ± 1.5). Subjective hardness rating (range = 1–9 [1 = soft, 9 = hard] was similar between UPF and Non-UPF buffet and snack items (UPF:4.22 ± 2.19, Non-UPF: 4.70 ± 2.03), as was the objective measure of hardness (UPF: 2874.33 ± 2497.06 g, Non-UPF: 2243.32 ± 1700.51 g).
Findings could contribute to an emerging neurobiological understanding of the effects of UPF consumption including energy overconsumption and weight gain among individuals at a critical developmental stage.

View all citing articles on Scopus

View full text

Review ArticleWhat has fMRI told us about the Development of Cognitive Control through Adolescence?

Abstract

Introduction

Section snippets

The development of cognitive control

Response inhibition

Working memory

Development of integrated systems level circuitry

Considerations in interpreting developmental neuroimaging results

Direction of developmental differences

Conclusions

NeuroImage

Cognition

Developmental Review

Neuron

NeuroImage

Trends in Cognitive Sciences

NeuroImage

Journal of Memory and Language

Brain and Cognition

Neuropsychologia

Neuron

Neuropsychologia

Brain Research

Brain & Development

Behavioural Brain Research

Trends in Neurosciences

Neuoimage

Pharmacology, Biochemistry and Behavior

Neuropsychologia

NeuroImage

Acta Psychologica

NeuroImage

NeuroImage

Cognitive Brain Research

Current Opinion in Neurobiology

Journal of Experimental Child Psychology

Neuroscience and Biobehavioral Reviews

Current Opinion in Neurobiology

Neuroscience and Biobehavioral Reviews

Behavioural Brain Research

Journal of the American Academy of Child and Adolescent Psychiatry

NeuroImage

Journal of Experimental Child Psychology

Neurobiology of Learning and Memory

Journal of Experimental Child Psychology

Working memory

The development of selective inhibitory control across the life span

Developmental Neuropsychology

The relations between frontal brain electrical activity and cognitive development during infancy

Child Development

Anterior cingulate cortex and response conflict: Effects of frequency, inhibition and errors

Cerebral Cortex

Neural circuitry underlying rule use in humans and nonhuman primates

The Journal of Neuroscience

Anterior cingulate cortex, error detection, and the online monitoring of performance

Science

A developmental functional MRI study of prefrontal activation during performance of a go-no-go task

Journal of Cognitive Neuroscience

The human brain age 7–11 years: A volumetric analysis based on magnetic resonance images

Cerebral Cortex

Developmental neurocircuitry of motivation in adolescence: A critical period of addiction vulnerability

American Journal of Psychiatry

An area specialized for spatial working memory in human frontal cortex

Science

Neurocognitive development of the ability to manipulate information in working memory

Proceedings of the National Academy of Sciences of the United States of America

Maintenance of spatial and motor codes during oculomotor delayed response tasks

Journal of Neuroscience

Normative data from the Cantab: I. Development of executive function over the lifespan

Journal of Clinical & Experimental Neuropsychology

The development of mental processing: Efficiency, working memory, and thinking

Monographs of the Society for Research in Child Development

Review Article
What has fMRI told us about the Development of Cognitive Control through Adolescence?