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Cited by 299Neural and Behavioral Psychology StudiesFunctional Brain Connectivity StudiesChild and Adolescent Psychosocial and Emotional Development

Arrested development? Reconsidering dual-systems models of brain function in adolescence and disorders

Open access
Pfeifer, Jennifer H., Allen, Nicholas B.·2012·Trends in Cognitive Sciences
DOI 10.1016/j.tics.2012.04.011PMC PMC3711850
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Abstract

The dual-systems model of a ventral affective system, whose reactivity confers risks and liabilities, and a prefrontal control system, whose regulatory capacities buffer against these vulnerabilities, is an intuitive account that pervades many fields in the cognitive neurosciences – especially in the study of populations that differ from neurotypical adults, such as adolescents or individuals with affective or impulse regulation disorders. However, recent evidence that is inconsistent with dual-systems models illustrates the complexity of developmental and clinical variations in brain function. Building new models to account for this complexity is critical to progress in these fields, and will be facilitated by research that emphasizes network-based approaches and maps relationships between structure and function, as well as brain and behavior, over time.

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Crossref · 10.1016/j.tics.2012.04.011

Cites

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Claims the paper makes

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  • Premisecitation

    Some resting-state connectivity findings of age-related growth in long-range connections were artifacts of greater motion in younger participants and disappeared with proper motion correction.

    “researchers recently discovered that some functional connectivity analyses interpreted as demonstrating developmental increases in long-range connections during rest (i.e., independent from any task) were spurious effects of greater motion in younger participants [62,63], which were eliminated with appropriate controls for motion-induced artifacts.”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [62] Power JD Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage 2012 59 2142 2154 22019881 PMC3254728 source

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    • cites [63] Van Dijk KRA The influence of head motion on intrinsic functional connectivity MRI. Neuroimage 2012 59 431 438 21810475 PMC3683830 source

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  • Interpretationreasoning

    Comparable motion artifacts might affect studies reporting age-related rises in task-dependent prefrontal-subcortical connectivity.

    “Similar effects could be at work in the empirical studies that show developmental increases in task-dependent functional connectivity between prefrontal and subcortical regions [2,31].”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [2] Hare TA Biological substrates of emotional reactivity and regulation in adolescence during an emotional go-nogo task. Biol Psychiatry 2008 63 927 934 18452757 PMC2664095 source

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    • cites [31] Pfeifer JH Entering adolescence: resistance to peer influence, risky behavior, and neural changes in emotion reactivity. Neuron 2011 69 1029 1036 21382560 PMC3840168 source

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  • Premisecitation

    Age group did not change how individual differences in these regional volumes related to reward sensitivity facets.

    “The effects of individual differences in volumes across these regions on facets of reward sensitivity did not vary by age group.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [59] Urošević S Longitudinal changes in behavioral approach system sensitivity and brain structures involved in reward processing during adolescence. Dev Psychol 2012 doi: 10.1037/a0027502 PMC3370133 22390662 source

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  • Premisecitation

    Activity patterns across prefrontal and subcortical regions are influenced by task performance, task design, and data analysis techniques.

    “other key factors besides development are known to influence patterns of activity across prefrontal and subcortical regions. These include (i) task performance [60], (ii) task design, including transient-event versus sustained-set paradigms [6] or different baseline and timing conditions [28,61], and (iii) various data analysis techniques.”
    Quote in the paperSubstantial claim0 of 4 sources checked
    • cites [60] Koolschijn PC A three-year longitudinal functional magnetic resonance imaging study of performance monitoring and test-retest reliability from childhood to early adulthood. J Neurosci 2011 31 4204 4212 21411661 PMC6623527 source

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    • cites [6] Velanova K The maturation of task set-related activation supports late developmental improvements in inhibitory control. J Neurosci 2009 29 12558 12567 19812330 PMC2788337 source

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    • cites [28] Galvan A Adolescent development of the reward system. Front Hum Neurosci 2010 4 6 20179786 PMC2826184

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    • cites [61] Geier C Luna B The maturation of incentive processing and cognitive control. Pharmacol. Biochem. Behav 2009 93 212 221 19593842 PMC2792989 source

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  • Premisecitation

    Other work has found no significant amygdala reactivity differences between depressed people and several comparison groups, including healthy controls.

    “many other studies have found no significant differences in amygdala reactivity between depressed individuals and various other subgroups, including healthy controls [68-70].”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites [68] Brotman MA Amygdala activation during emotion processing of neutral faces in children with severe mood dysregulation versus ADHD or bipolar disorder. Am J Psychiatry 2010 167 61 69 19917597 PMC3075433 source

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    • cites [69] Demenescu LR Neural correlates of perception of emotional facial expressions in out-patients with mild-to-moderate depression and anxiety. A multicenter fMRI study. Psychol Med 2011 41 2253 2264 21557888 source

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    • cites [70] Townsend JD fMRI activation in the amygdala and the orbitofrontal cortex in unmedicated subjects with major depressive disorder. Psychiatry Res 2010 183 209 217 20708906 PMC3382985 source

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  • May combine two claims. 16
  • Classified as probably not a substantial claim. 8

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    Premisecitation

    In some reward tasks, adolescent VS responses are either lower than adults' or not different from them.

    “many researchers observe either hypoactivity or no differences between adolescents and adults in VS responses to some reward conditions or paradigms [1,3,43].”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites [1] Geier CF Immaturities in reward processing and its influence on inhibitory control in adolescence. Cereb Cortex 2010 20 1613 1629 19875675 PMC2882823 source

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    • cites [3] Van Leijenhorst L What motivates the adolescent? Brain regions mediating reward sensitivity across adolescence. Cereb Cortex 2010 20 61 69 19406906 source

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    • cites [43] Bjork JM Adolescents, adults and rewards: comparing motivational neurocircuitry recruitment using fMRI. PLoS One 2010 5 e11440 (2010) 20625430 PMC2897849 source

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    Premisecitation

    Across three groups initially aged 9 to 23, nucleus accumbens volume grew over two years, and that growth correlated with rising behavioral approach system drive.

    “VS (specifically, nucleus accumbens) actually volumetrically increased over a two-year period across three age groups ranging in initial age from 9-23 years, and that this was correlated with increased drive in the behavioral approach system (BAS [58]).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [58] Gray JA Fear, panic, and anxiety: what's in a name? Psychol. Inquiry 1991 2 77 78 source

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    Premisecitation

    One recent study observed reward-related amygdala hyperactivity in depressed participants, which is hard to square with the view that such hyperactivity produces depressive negative affect.

    “recently recent study demonstrated amygdala hyperactivity in response to rewards amongst depressed samples, a finding that fits less well with the idea that amygdala hyperactivity is responsible for the negative affect associated with depression [67].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [67] Davey CG Increased Amygdala Response to Positive Social Feedback in Young People with Major Depressive Disorder. Biol. Psychiatry 2011 69 734 741 21257158 source

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    Premisecitation

    An antisaccade study found that short-lived PFC activity tied to stopping a saccade declines with age, while sustained task-set activity rises.

    “a recent study examining inhibitory control in an antisaccade task found that transient activations in PFC related to inhibitory control during a given saccade decrease with age, whereas sustained set-related activations in PFC increase [6].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [6] Velanova K The maturation of task set-related activation supports late developmental improvements in inhibitory control. J Neurosci 2009 29 12558 12567 19812330 PMC2788337 source

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    Collectively, these findings indicate that adolescent ventral affective reactivity is not uniformly elevated and can accompany positive adjustment.

    “Taken together, these studies suggest that occasionally the ventral affective system is not hyperreactive during adolescence and that heightened responses are sometimes associated with adaptive outcomes.”
    Quote in the paperSubstantial claim

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    Premisecitation

    A longitudinal study found that rising VS reactivity to emotional faces tracked with greater resistance to peer influence and less risky behavior.

    “a recent longitudinal study of the transition from childhood to adolescence found increases in VS response to emotional facial expressions were associated with increases in resistance to peer influence and decreases in risky behavior [31].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [31] Pfeifer JH Entering adolescence: resistance to peer influence, risky behavior, and neural changes in emotion reactivity. Neuron 2011 69 1029 1036 21382560 PMC3840168 source

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    Interpretationcitation

    Research on cognitive control development reports both increases and decreases in PFC activity, with patterns differing by subregion and task.

    “Overall, the literature on neurodevelopmental underpinnings of cognitive control shows bidirectional, complex patterns – both increases and decreases in PFC activations that vary across subregions and tasks – that should be interpreted with caution [8,54-56].”
    Quote in the paperSubstantial claim0 of 4 sources checked
    • cites [8] Luna B What has fMRI told us about the development of cognitive control through adolescence? Brain Cogn 2010 72 101 113 19765880 PMC2815087 source

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    • cites [54] Astle DE Scerif G Using developmental cognitive neuroscience to study behavioral and attentional control. Dev Psychobiol 2009 51 107 118 18973175 source

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    • cites [55] Crone EA Richard Ridderinkhof K The developing brain: from theory to neuroimaging and back. Dev. Cogn. Neurosci 2011 1 101 109 22436435 PMC6987573 source

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    • cites [56] Poldrack RA Mapping mental function to brain structure: how can cognitive neuroimaging succeed? Persp. Psychol. Sci 2010 5 753 761 PMC4112478 25076977 source

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    Premisecitation

    Functional networks correspond to structural connections seen with diffusion tensor imaging, and resting-state and structural connectivity estimates resemble each other in development and disorders, though they are not fully redundant.

    “These functional networks map on to the structural connections between regions illuminated by techniques such as diffusion tensor imaging [77] and there are similarities between resting-state and structural estimates of regional connectivity across development [78] and disorders [79], although the two methodologies are not completely redundant [80,81].”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [77] Greicius MD Resting-state functional connectivity reflects structural connectivity in the default mode network. Cereb Cortex 2009 19 72 78 18403396 PMC2605172 source

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    • cites [78] Fair DA The maturing architecture of the brain's default network. Proc Natl Acad Sci U S A 2008 105 4028 4032 18322013 PMC2268790 source

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    • cites [79] Uddin LQ Typical and atypical development of functional human brain networks: insights from resting-state FMRI. Front Syst Neurosci 2010 4 21 20577585 PMC2889680 source

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    Premisecitation

    The literature lacks selective mappings between brain structure and function and between brain and behavior.

    “the lack of selective structure-function mappings and brain-behavior mappings [18,56,75]”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites [18] Johnson SB Adolescent maturity and the brain: the promise and pitfalls of neuroscience research in adolescent health policy. J Adolesc Health 2009 45 216 221 19699416 PMC2892678 source

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    • cites [56] Poldrack RA Mapping mental function to brain structure: how can cognitive neuroimaging succeed? Persp. Psychol. Sci 2010 5 753 761 PMC4112478 25076977 source

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    • cites [75] Poldrack RA Inferring mental states from neuroimaging data: from reverse inference to large-scale decoding. Neuron 2011 72 692 697 22153367 PMC3240863 source

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  • Probably not a substantial claim: may not pass S4 (based).

    Premisenone given

    Legal, educational, and journalistic audiences for behavioral science have embraced dual-systems accounts of adolescent, clinical, and forensic behavior with enthusiasm.

    “the dual-systems interpretations of adolescent, clinical, and forensic behavior have been so enthusiastically adopted by the legal, educational, and journalistic consumers of behavioral science (Box 1)”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation

    Depression rates begin to rise in adolescence and remain elevated into adulthood, beyond the point when prefrontal regulation is thought to mature.

    “increased rates of depression start in adolescence, they persist though adulthood – well past the period when prefrontal regulatory mechanisms have presumably matured [74].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [74] Davey CG The emergence of depression in adolescence: development of the prefrontal cortex and the representation of reward. Neurosci Biobehav Rev 2008 32 1 19 17570526 source

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  • Probably not a substantial claim: may not pass S2 (checkable).

    Interpretationnone given

    The functions and response profiles within and between the regions discussed in dual-systems models are numerous and complex.

    “the functions and response profiles exhibited within and between regions addressed in these models are numerous and complex”
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  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Resting-state studies of slow BOLD fluctuations revealed several networks with coordinated activity even without a task.

    “studies of low-frequency oscillations in the BOLD signal during ‘rest’ helped to identify multiple networks whose response profiles were coordinated in absence of tasks [76].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [76] Dosenbach NU A dual-networks architecture of top-down control. Trends Cogn Sci 2008 12 99 105 18262825 PMC3632449 source

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  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    A review concluded that depression typically involves lower dorsolateral PFC activity, including dorsal ACC, and higher ventromedial PFC activity, including subgenual ACC.

    “One recent review of brain function in depression [71] concluded that depression is typified by hypoactivation in dorsolateral PFC (including dorsal ACC), as well as hyperactivation in ventromedial PFC (including subgenual ACC).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [71] Koenigs M Grafman J The functional neuroanatomy of depression: distinct roles for ventromedial and dorsolateral prefrontal cortex. Behav Brain Res 2009 201 239 243 (2009) 19428640 PMC2680780 source

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  • Classified as probably not a substantial claim. May combine two claims.

    Interpretationcitation

    An alternative account holds that depression is not a failure of prefrontal control; instead, developing prefrontal capacities, such as anticipating distant or abstract rewards, may raise vulnerability.

    “According to an alternative hypothesis [74], depression does not represent a failure of prefrontal regulation. Instead, vulnerability to depression may actually be increased by the development of prefrontally mediated capacities, such as the adolescent's enhanced ability to anticipate abstract and distal rewards (or punishments; Figure 1).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [74] Davey CG The emergence of depression in adolescence: development of the prefrontal cortex and the representation of reward. Neurosci Biobehav Rev 2008 32 1 19 17570526 source

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    Depending too heavily on dual-systems models to interpret functional or structural data after the fact is likely to make those models more concrete and to repeat the pattern of other influential ideas in neurodevelopment and disorders.

    “overreliance on these models for post hoc interpretations of patterns in functional or structural data will tend to reify them, repeating the history of other strong memes in neurodevelopment and disorders discussed in Box 2”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation

    In adolescents, more depressive symptoms and less daily positive affect have been linked to stronger PFC responses.

    “greater depressive symptoms and lower daily positive affect have been associated with heightened PFC responses in adolescence [50,51].”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [50] Forbes EE Altered striatal activation predicting real-world positive affect in adolescent major depressive disorder. Am J Psychiatry 2009 166 64 73 19047324 PMC2701209 source

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    • cites [51] Forbes EE Healthy adolescents’ neural response to reward: associations with puberty, positive affect, and depressive symptoms. J Am Acad Child Adolesc Psychiatry 2010 49 162 72 e1 5 20215938 PMC2837556

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  • May combine two claims.

    Premisecitation

    Mental processes rarely map one-to-one onto single brain regions; instead, distributed networks jointly support a function.

    “simple one-to-one mappings between mental processes and brain regions are rare – instead, entire networks of regions interactively support a given function [75].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [75] Poldrack RA Inferring mental states from neuroimaging data: from reverse inference to large-scale decoding. Neuron 2011 72 692 697 22153367 PMC3240863 source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S2 (checkable), S3 (load-bearing).

    Interpretationreasoning

    Recognition of these limitations in the field is increasing.

    “Acknowledgment of our limitations is gradually growing”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    MVPA is still rare in developmental and clinical populations.

    “although this methodology is still rare in developmental and clinical populations [82].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [82] Dosenbach NU Prediction of individual brain maturity using fMRI. Science 2010 329 1358 1361 20829489 PMC3135376 source

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  • Probably not a substantial claim: may not pass S1 (asserted), S3 (load-bearing).

    Premisecitation

    Some researchers propose that ventromedial PFC is centrally involved in dampening amygdala responses.

    “other researchers have suggested that ventromedial PFC plays a central role in the downregulation of amygdala responses [2,72].”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [2] Hare TA Biological substrates of emotional reactivity and regulation in adolescence during an emotional go-nogo task. Biol Psychiatry 2008 63 927 934 18452757 PMC2664095 source

      Not checked in the free run.

    • cites [72] Lieberman MD Putting feelings into words: affect labeling disrupts amygdala activity in response to affective stimuli. Psychol Sci 2007 18 421 428 17576282 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Risk taking and substance use rise in adolescence and fall in early adulthood, by which time regulatory brain systems are usually mature.

    “although risk taking and substance use become more common during adolescence, they decline during early adulthood, when regulatory brain systems have usually reached adult levels of maturity [11,27].”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [11] Steinberg L A behavioral scientist looks at the science of adolescent brain development. Brain Cogn 2010 72 160 164 19963311 PMC2904973 source

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    • cites [27] Steinberg L A social neuroscience perspective on adolescent risk-taking. Dev Rev 2008 28 78 106 18509515 PMC2396566 source

      Not checked in the free run.

22 of 22

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Most theoretical work concentrates on two general brain systems: a ventral affective system (including subcortical regions such as amygdala and ventral striatum) and the prefrontal cortex (PFC), which modulates the reactions of the ventral affective system.

    “Most of the theoretical work in this area concentrates on two general brain systems that work in concerta ventral affective system, including subcortical regions such as the amygdala and ventral striatum; and the prefrontal cortex (PFC), which modulates the reactions of the ventral affective system [1].”

    From The depressed brain: an evolutionary systems theory (2017) · cites this paper as [1]

  • The medial prefrontal cortex is strongly implicated in social cognition and shows functional segregation along a dorsal-ventral axis.

    “The mPFC has been strongly implicated in social cognition and also displays functional segregation along the dorsal-ventral axis (Amodio and Frith, 2006, Pfeifer and Allen, 2012, Bzdok et al., 2013b);”

    From Developmental sex differences in resting state functional connectivity of amygdala sub-regions (2015) · cites this paper as Pfeifer and Allen, 2012

  • Dual systems models emphasize asynchronous development of the neural systems underlying sensation seeking and self-regulation.

    “Dual systems models highlight the asynchronous development of the neural systems that underlie sensation seeking – the tendency to seek varied, novel, complex and intense sensations and experiences [20] – and self-regulation – the deliberate modulation of one’s thoughts, feelings or actions in the pursuit of planned goals [21, 22].”

    From The role of the anterior insula in adolescent decision making (2014) · cites this paper as [17]

  • Dual-process models have become prominent in research on adolescent cognitive development because they accommodate interacting cognitive and affective inputs.

    “the ability of dual-process models to accommodate the interacting influences of cognitive and affective inputs to decision making has elevated this class of models to the forefront of research on adolescent cognitive development”

    From Impact of socio-emotional context, brain development, and pubertal maturation on adolescent risk-taking (2013) · cites this paper as Pfeifer & Allen, 2012

  • Neural systems models have been criticized as too simplistic and unable to account for findings contrary to their predictions.

    “Of note, neural systems models have been challenged recently as being too simplistic and not able to account for findings running against predictions based on these models (Pfeifer and Allen, 2012).”

    From A systematic review of fMRI reward paradigms used in studies of adolescents vs. adults: The impact of task design and implications for understanding neurodevelopment (2013) · cites this paper as Pfeifer and Allen, 2012

Cites

Flagged first, then by citations

1 of the 105 references couldn’t be matched to a known paper.

Research works printed but not linked: 3

  1. Geier, 2009, The maturation of incentive processing and cognitive control, Pharmacol. Biochem. Behav., 93, 212, 10.1016/j.pbb.2009.01.021 · DOI · Paper page
  2. Wallis, 2004, What makes teens tick, Time Magazine, 163, 56
  3. Dobbs, 2011, Beautiful brains, Natl. Geographic, 220

Cited by

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Related

Authors
Pfeifer, J. H., & Allen, N. B.
Affiliations
  • University of Oregon (US)
  • The University of Melbourne (AU)
ORCID
Venue
Trends in Cognitive Sciences
Publisher
Elsevier BV
Published
2012-06
Volume
16
Issue
6
Pages
322-329
ISSN
1364-6613 (ISSN-L)
DOI
10.1016/j.tics.2012.04.011
PMC
PMC3711850
OpenAlex
W2165975182
Semantic Scholar
ca9f8fadbd14253e02b07ae48fc7a5bac44f6a94
Cited by
299
References
105
Citations by year
2026: 3 · 2025: 17 · 2024: 12 · 2023: 4 · 2022: 19 · 2021: 19 · 2020: 17 · 2019: 22 · 2018: 36 · 2017: 32 · 2016: 30 · 2015: 31 · 2014: 23 · 2013: 25 · 2012: 7
FWCI
2.11
Type
journal article
Language
en
Open access
Licence
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations
  • Trends in Cognitive Sciences (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • University of Oregon
  • National Institute of Mental Health (L40MH087356)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
  • Social Sciences › Psychology › Clinical Psychology › Child and Adolescent Psychosocial and Emotional Development
Keywords
dual systems model, adolescence, mood disorders, brain development, network models, structure-function relationship, developmental variation, clinical heterogeneity
MeSH terms
Adolescent, Adolescent Behavior, Adult, Amygdala, Basal Ganglia, Major Depressive Disorder, Humans, Models, Neurological, Prefrontal Cortex, Adolescent Development, Functional Neuroimaging

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