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Cited by 485Neural and Behavioral Psychology StudiesChild and Adolescent Psychosocial and Emotional DevelopmentFunctional Brain Connectivity Studies

Development of the emotional brain

Open access
Casey, B.J., Heller, Aaron S., Gee, Dylan G., Cohen, Alexandra O.·2019·Neuroscience Letters
DOI 10.1016/j.neulet.2017.11.055PMC PMC5984129
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Abstract

In this article, we highlight the importance of dynamic reorganization of neural circuitry during adolescence, as it relates to the development of emotion reactivity and regulation. We offer a neurobiological account of hierarchical, circuit-based changes that coincide with emotional development during this time. Recent imaging studies suggest that the development of the emotional brain involves a cascade of changes in limbic and cognitive control circuitry. These changes are particularly pronounced during adolescence, when the demand for self regulation across a variety of emotional and social situations may be greatest. We propose that hierarchical changes in circuitry, from subcortico-subcortical to subcortico-cortical to cortico-subcortical and finally to cortico-cortical, may underlie the gradual changes in emotion reactivity and regulation throughout adolescence into young adulthood, with changes at each level being necessary for the instantiation of changes at the next level.

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Crossref · 10.1016/j.neulet.2017.11.055

Cites

51 of 51 references verified0 citation errors · 0 not checkable

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Claims the paper makes

0 of 30 cited sources checked · 0 supported · 0 flagged

  • Interpretationreasoning

    A hierarchical sequence of circuit changes-first within subcortical circuits, then from subcortical to cortical, then from cortical to subcortical, and finally between cortical regions-may explain the gradual development of emotion reactivity and regulation from adolescence to young adulthood.

    “We propose that hierarchical changes in circuitry, from subcortico-subcortical to subcortico-cortical to cortico-subcortical and finally to cortico-cortical, may underlie the gradual changes in emotion reactivity and regulation throughout adolescence into young adulthood”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: Adolescence is a sensitive developmental period in which the capacity to regulate emotion is especially vulnerable to social and emotional environmental influences.
  • Interpretationnone given

    Each step in the proposed hierarchical circuit sequence is required for the next step to occur.

    “with changes at each level being necessary for the instantiation of changes at the next level.”
    Quote in the paperNot a substantial claim
  • Premisecitation

    Amygdala-ventral striatum functional connectivity is associated with more impulsive responses to emotional cues regardless of valence, after controlling for impulsivity to non-valenced cues.

    “Functional connectivity between the amygdala and ventral striatum was associated with greater impulsive actions towards emotional cues regardless of valence, controlling for impulsivity to nonvalenced cues.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [28] Heller AS Cohen AO Dreyfuss MFW Casey BJ Changes in cortico-subcortical and subcortico- subcortical connectivity impact cognitive control to emotional cues across development Soc Cogn Affect Neurosci 2016 1910 1918 10.1093/scan/nsw097 27445212 PMC5141951

      Not checked in the free run.

    • Rests on an assumption: Age differences observed in cross-sectional samples reflect developmental changes within individuals.
    • Rests on an assumption: Functional connectivity between brain regions indexes their effective communication or regulatory influence.
  • Premisecitation

    The link between subcortical connectivity and impulsive responses to emotional cues declines linearly with age.

    “The association between subcortical connectivity and impulsive responses to emotional cues decreased linearly with age.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [28] Heller AS Cohen AO Dreyfuss MFW Casey BJ Changes in cortico-subcortical and subcortico- subcortical connectivity impact cognitive control to emotional cues across development Soc Cogn Affect Neurosci 2016 1910 1918 10.1093/scan/nsw097 27445212 PMC5141951

      Not checked in the free run.

    • Rests on an assumption: Age differences observed in cross-sectional samples reflect developmental changes within individuals.
  • Interpretationcitation

    Subcortical-subcortical and cortical-subcortical connectivity have different effects on emotion reactivity and regulation to environmental cues across age.

    “These findings suggest a dissociation in how subcortical-subcortical and cortical-subcortical connectivity differentially impact emotion reactivity and regulation to cues in the environment with age.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: Functional connectivity between brain regions indexes their effective communication or regulatory influence.
  • May combine two claims. 14
  • The quote only partly states this claim. 1
  • Classified as probably not a substantial claim. 2

  • May combine two claims.

    Premisecitation

    Basolateral amygdala microcircuits separate reward and aversion, with valence coding that can bias motivated action toward appetitive cues through projections to the accumbens and toward aversive cues through projections to the central nucleus of the amygdala.

    “They [29,30] showed parsing of reward and aversion in basolateral amygdala microcircuits. Specifically, they provided evidence of valence coding in the basolateral amygdala, that could bias motivated action to appetitive cues via projections to the accumbens and to aversive cues via projections to the central nucleus of the amygdala.”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [29] Beyeler A Namburi P Glober GF Simonnet C Calhoon GG Conyers GF Luck R Wildes CP Tye KM Divergent Routing of Positive and Negative Information from the Amygdala during Memory Retrieval Neuron 90 2016 348 361 10.1016/j.neuron.2016.03.004 27041499 PMC4854303 source

      Not checked in the free run.

    • cites [30] Namburi P Beyeler A Yorozu S Calhoon GG Halbert SA Wichmann R Holden SS Mertens KL Anahtar M Felix-Ortiz AC Wickersham IR Gray JM Tye KM A circuit mechanism for differentiating positive and negative associations Nature 520 2015 675 678 10.1038/nature14366 25925480 PMC4418228 source

      Not checked in the free run.

    • Rests on an assumption: Findings from rodent models about amygdala–prefrontal circuitry and microcircuits can be generalized to human emotional development.

  • May combine two claims. The quote only partly states this claim.

    Interpretationcitation

    The emotional brain develops through a series of changes in limbic and cognitive control circuits, with these changes being especially evident in adolescence.

    “Recent imaging studies suggest that the development of the emotional brain involves a cascade of changes in limbic and cognitive control circuitry.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The demand for self-regulation across emotional and social situations is greatest during adolescence.

  • May combine two claims.

    Premisecitation

    Human developmental imaging studies have found impulsivity to emotional cues in early adolescence regardless of whether the cues are positive or negative or rewarding, along with activation of the amygdala and ventral striatum.

    “Consistent with this hypothesis is evidence from human developmental imaging studies showing impulsivity to emotional cues regardless of valence (positive or negative) or value (rewarding) in early adolescence [25,26] and activation of these two regions [25,27].”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites [25] Somerville LH Hare T Casey BJ Frontostriatal maturation predicts cognitive control failure to appetitive cues in adolescents J Cogn Neurosci 23 2011 2123 2134 10.1162/jocn.2010.21572 20809855 PMC3131482 source

      Not checked in the free run.

    • cites [26] Dreyfuss M Caudle K Drysdale AT Johnston NE Cohen AO Somerville LH Galván A Tottenham N Hare Ta Casey BJ Teens Impulsively React rather than Retreat from Threat Dev Neurosci 36 2014 220 7 10.1159/000357755 24821576 PMC4125471 source

      Not checked in the free run.

    • cites [27] Hare TA Tottenham N Galvan A Voss HU Glover GH Casey BJ Biological substrates of emotional reactivity and regulation in adolescence during an emotional go-nogo task Biol Psychiatry 63 2008 927 934 S0006-3223(08)00359-4 [pii] 10.1016/j.biopsych.2008.03.015 18452757 PMC2664095 source

      Not checked in the free run.

    • Rests on an assumption: Age differences observed in cross-sectional samples reflect developmental changes within individuals.

  • May combine two claims.

    Premisecitation

    Distinct populations of amygdala neurons respond preferentially to unexpected rewards, punishments, or both, which supports a role for the amygdala in emotional processes that are not specific to valence.

    “However, rodent work has shown that different populations of amygdala neurons respond preferentially to either or both unexpected rewards and punishments [23], reflecting the role of the amygdala in valence non-specific emotional processes and behaviors [24].”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [23] Paton JJ Belova MA Morrison SE Salzman CD The primate amygdala represents the positive and negative value of visual stimuli during learning Nature 439 2006 865 870 16482160 PMC2396495 source

      Not checked in the free run.

    • cites [24] Peck CJ Lau B Salzman CD The primate amygdala combines information about space and value Nat Neurosci 16 2013 340 348 10.1038/nn.3328 23377126 PMC3596258 source

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Premisecitation

    Adolescent changes in synaptic structure, dendritic branching, cortical firing, and neurochemical and receptor availability have been proposed to produce temporary imbalances in functional brain circuits that affect behavior.

    “The regional changes in synaptic morphology, dendritic arborization, cortical cell firing, and availability of neurochemicals and their receptors during adolescence have been posited to lead to transient imbalances in functional brain circuitry that impact behavior [1].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [1] Casey BJ Beyond Simple Models of Self-Control to Circuit-Based Accounts of Adolescent Behavior Annu Rev Psychol 66 2015 295 319 10.1146/annurev-psych-010814-015156 25089362 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Greater medial prefrontal-amygdala connectivity is associated with better cognitive control over emotional cues, and this cortical-subcortical connectivity mediates the relationship between amygdala-ventral striatum connectivity and emotional cognitive control.

    “They found that increased medial prefrontal-amygdala connectivity was associated with better cognitive control to emotional cues, and this cortical-subcortical connectivity mediated the association between amygdala-ventral striatum connectivity and emotional cognitive control (Figure 2).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [28] Heller AS Cohen AO Dreyfuss MFW Casey BJ Changes in cortico-subcortical and subcortico- subcortical connectivity impact cognitive control to emotional cues across development Soc Cogn Affect Neurosci 2016 1910 1918 10.1093/scan/nsw097 27445212 PMC5141951

      Not checked in the free run.

    • Rests on an assumption: Age differences observed in cross-sectional samples reflect developmental changes within individuals.
    • Rests on an assumption: Functional connectivity between brain regions indexes their effective communication or regulatory influence.

  • May combine two claims.

    Interpretationreasoning

    If subcortical circuits develop before cortico-subcortical circuits, this could produce an unchecked subcortical system and lead to impulsivity driven by emotional cues.

    “Thus, developmental changes in subcortical circuits before cortico-subcortical circuits could lead to an unchecked subcortical system resulting in emotional cue-driven impulsivity.”
    Quote in the paperSubstantial claim

  • Classified as probably not a substantial claim.

    Premisecitation

    The imbalance model holds that behavioral changes in adolescence accompany a sequence of developmental changes across systems: fine-tuning within subcortical limbic circuits, then between prefrontal and limbic circuits, and later between cortical circuits.

    “According to the imbalance model, changes in behavior during adolescence coincide with a series of developmental changes across multiple systems with the regional fine-tuning of connections within subcortical limbic circuits, then between cortical prefrontal and limbic circuits and subsequently between corticocortical circuits ([7], see Figure 1).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [7] Casey BJ Galván A Somerville LH Developmental Cognitive Neuroscience Beyond simple models of adolescence to an integrated circuit-based account: A commentary Dev Cogn Neurosci 17 2016 128 130 10.1016/j.dcn.2015.12.006 26739434 PMC6987976 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Human neuroimaging shows regional brain changes across development, and functional connectivity studies indicate that local subcortical circuits are refined before more distant cortical circuits.

    “Human neuroimaging studies have shown corresponding patterns of regional brain changes across development [12] with functional connectivity studies [13,14] suggesting refinement of local subcortical circuits precedes refinement of distal cortical ones.”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites [12] Mills KL Goddings AL Clasen LS Giedd JN Blakemore SJ The Developmental Mismatch in Structural Brain Maturation during Adolescence Dev Neurosci 36 2014 147 60 10.1159/000362328 24993606 source

      Not checked in the free run.

    • cites [13] Fair DA Cohen AL Power JD Dosenbach NU Church JA Miezin FM Schlaggar BL Petersen SE Functional brain networks develop from a “local to distributed” organization PLoS Comput Biol 5 2009 1 14 PMC2671306 19412534 source

      Not checked in the free run.

    • cites [14] Satterthwaite TD Wolf DH Ruparel K Erus G Elliott MA Eickhoff SB Gennatas ED Jackson C Prabhakaran K Smith A Hakonarson H Verma R Davatzikos C Gur RE Gur RC Heterogeneous impact of motion on fundamental patterns of developmental changes in functional connectivity during youth ☆ Neuroimage 83 2013 45 57 10.1016/j.neuroimage.2013.06.045 23792981 PMC3874413 source

      Not checked in the free run.

    • Rests on an assumption: Age differences observed in cross-sectional samples reflect developmental changes within individuals.

  • May combine two claims.

    Interpretationreasoning

    Greater function and connectivity in subcortical circuits may be required before top-down cortical control circuits can develop, and those cortical control circuits may in turn be required before cortico-cortical interactions supporting complex cognitive-affective processes can emerge.

    “Thus, heightened functionality and connectivity of subcortical circuits may be a necessary precursor for signaling top-down cortical control circuitry which is then a necessary precursor for cortico-cortical interactions for complex interactions among cognitive and affective processes.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationcitation

    Strong subcortical signaling may supply the functional input needed to strengthen descending cortical projections, and later top-down control of cortico-subcortical circuits may depend partly on the prior development of subcortical circuits within a dynamic cascade.

    “For example, robust subcortical signaling could provide the key functional inputs to provoke strengthening of descending cortical projections. Subsequently, the capacity for top-down control of cortico-subcortical circuits may be dependent in part on the functional development of subcortical circuits as part of a dynamic cascade [7].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [7] Casey BJ Galván A Somerville LH Developmental Cognitive Neuroscience Beyond simple models of adolescence to an integrated circuit-based account: A commentary Dev Cogn Neurosci 17 2016 128 130 10.1016/j.dcn.2015.12.006 26739434 PMC6987976 source

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    Cognitive control remains vulnerable to negative emotional influences into young adulthood while lateral and ventromedial prefrontal circuits continue to develop.

    “These results suggest that cognitive control remains susceptible to negative emotional influences into young adulthood as lateral and ventromedial prefrontal circuitries continue to develop.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: Age differences observed in cross-sectional samples reflect developmental changes within individuals.

  • May combine two claims.

    Premisecitation

    Adolescents show weaker cognitive control than adults under both negative and positive emotional states, while young adults show weaker performance than adults over 21 only under negatively valenced arousal.

    “Teens showed diminished cognitive control relative to adults under both negative and positive emotional states. Like teens, young adults showed diminished performance relative to adults over 21, but only in the context of negatively valenced arousal.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [18] Cohen AO Breiner K Steinberg L Bonnie RJ Scott ES Taylor-Thompson KA Rudolph MD Chein JM Richeson JA Heller AS Silverman MR Dellarco DV Fair DA Galván A Casey BJ When Is an Adolescent an Adult? Assessing Cognitive Control in Emotional and Nonemotional Contexts Psychol Sci 2016 0956797615627625 10.1177/0956797615627625 26911914 source

      Not checked in the free run.

    • Rests on an assumption: Age differences observed in cross-sectional samples reflect developmental changes within individuals.

  • May combine two claims.

    Premisecitation

    In adolescents and young adults, this behavioral pattern was accompanied by greater ventromedial prefrontal activity linked to emotion regulation and lower lateral prefrontal activity linked to cognitive control.

    “This behavioral pattern was paralleled by enhanced ventromedial prefrontal activity associated with emotional regulation and diminished lateral prefrontal activity implicated in cognitive control in the teens and young adults.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [18] Cohen AO Breiner K Steinberg L Bonnie RJ Scott ES Taylor-Thompson KA Rudolph MD Chein JM Richeson JA Heller AS Silverman MR Dellarco DV Fair DA Galván A Casey BJ When Is an Adolescent an Adult? Assessing Cognitive Control in Emotional and Nonemotional Contexts Psychol Sci 2016 0956797615627625 10.1177/0956797615627625 26911914 source

      Not checked in the free run.

    • Rests on an assumption: Age differences observed in cross-sectional samples reflect developmental changes within individuals.

  • May combine two claims.

    Premisereasoning

    Later decreases in subcortical connectivity are associated with reduced reactivity to emotional cues, and changes in medial prefrontal-amygdala functional connectivity mediate this relationship.

    “Subsequent decreases in this subcortical connectivity are associated with diminished reactivity to emotional cues, and changes in medial PFC-amygdala functional connectivity mediate this association.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: Age differences observed in cross-sectional samples reflect developmental changes within individuals.
    • Rests on an assumption: Functional connectivity between brain regions indexes their effective communication or regulatory influence.

  • May combine two claims.

    Premisecitation

    Lateral prefrontal cortex plays a significant role in developing cognitive reappraisal, mediating the link between increasing age and reduced amygdala responses to emotionally evocative stimuli; this link is stronger in individuals with greater inverse vmPFC-amygdala coupling.

    “Recent evidence suggests that the lateral PFC plays a significant role in the development of these abilities [46], mediating the association between increasing age and diminished amygdala responses to emotionally evocative stimuli. This association is stronger for individuals with greater inverse coupling between the vmPFC and amygdala.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [46] Silvers JA Insel C Powers A Franz P Helion C Martin RE Weber J Mischel W Casey BJ Ochsner KN vlPFC–vmPFC–Amygdala Interactions Underlie Age-Related Differences in Cognitive Regulation of Emotion Cereb Cortex 2016 bhw073 10.1093/cercor/bhw073 PMC6059245 27341851 source

      Not checked in the free run.

    • Rests on an assumption: Age differences observed in cross-sectional samples reflect developmental changes within individuals.
    • Rests on an assumption: Functional connectivity between brain regions indexes their effective communication or regulatory influence.
16 of 16

  • The paper relies on this without support.

    Adolescence is a sensitive developmental period in which the capacity to regulate emotion is especially vulnerable to social and emotional environmental influences.

    “Although individuals differ substantially in the capacity to regulate emotions, adolescence is thought to be a sensitive period of development when this ability may be especially vulnerable to influences of the social and emotional environment.”

  • The paper relies on this without support.

    Age differences observed in cross-sectional samples reflect developmental changes within individuals.

    “He utilized task-based fMRI from a cross-sectional sample of over 150 children, adolescents and adults, who performed a go/no-go task to emotional faces.”

  • The paper relies on this without support.

    Findings from rodent models about amygdala–prefrontal circuitry and microcircuits can be generalized to human emotional development.

    “A collection of recent optogenetic studies by Tye and colleagues provide novel insights from adult mice that may inform our developmental findings.”

  • The paper relies on this without support.

    Functional connectivity between brain regions indexes their effective communication or regulatory influence.

    “this cortical-subcortical connectivity mediated the association between amygdala-ventral striatum connectivity and emotional cognitive control”

  • The paper relies on this without support.

    The demand for self-regulation across emotional and social situations is greatest during adolescence.

    “when the demand for self regulation across a variety of emotional and social situations may be greatest”
5 of 5

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?

  • During adolescence, receptor systems and brain regions undergo critical developmental changes including a reduction in gray matter volume, an increase in white matter volume, changes in connections from subcortical to cortical circuits for emotional control, elimination of excess neural connections, refinement of the GABAergic system in the neocortex, increases in dopamine receptor expression, and

    “these receptor systems and brain regions undergo critical developmental changes during adolescence including a reduction in gray matter volume (GMV) [5] accompanied by an increase in white matter volume [6], changes in connections from subcortical to cortical circuits for emotional control [7], elimination of excess neural connections [8], refinement of the GABAergic system in the neocortex [9, 10”

    From Consequences of adolescent drug use (2023) · cites this paper as [7]

  • A core hypothesis underlying brain development is that ongoing changes in brain maturation lead to a period when limbic structures, such as the amygdala and striatum, predominate over prefrontal areas during youth.

    “A core hypothesis underlying brain development is the view that ongoing changes in brain maturation lead to a period when limbic structures, such as the amygdala and striatum, predominate over prefrontal areas during youth [43, 44]”

    From Towards a youth mental health paradigm: a perspective and roadmap (2023) · cites this paper as [43]

  • Increasing prefrontal control over emotionally reactive subcortical regions enhances capacities to regulate negative emotions (particularly fear) and manage impulsive tendencies.

    “These models propose that increasing prefrontal control over emotionally reactive subcortical regions enhances capacities to regulate negative emotions (particularly fear) and manage impulsive tendencies (reward and approach [15,16,18]).”

    From Positive and Negative Emotion Regulation in Adolescence: Links to Anxiety and Depression (2019) · cites this paper as [18]

Cites

Flagged first, then by citations

Research works printed but not linked: 1

  1. Cohen, 2016, When does a juvenile become an adult? Implications for law and policy, Temple Law Rev., 769

Cited by

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Related

Authors
Casey, B. J., Heller, A. S., Gee, D. G., & Cohen, A. O.
Affiliations
  • Yale University (US)
  • University of Miami (US)
  • New York University (US)
Corresponding author
Casey, B.J.
ORCID
Venue
Neuroscience Letters
Publisher
Elsevier BV
Published
2019-02
Volume
693
Pages
29-34
ISSN
0304-3940 (ISSN-L)
DOI
10.1016/j.neulet.2017.11.055
PMC
PMC5984129
OpenAlex
W2774011664
Cited by
485
References
51
Citations by year
2026: 92 · 2025: 65 · 2024: 67 · 2023: 69 · 2022: 60 · 2021: 53 · 2020: 35 · 2019: 35 · 2018: 8 · 2016: 1
FWCI
2.39
Type
journal article
Language
en
Open access
Licence
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations
  • Neuroscience Letters (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • the MacArthur Foundation Research Network on Law and Neuroscience (U01 DA041174)
  • (DGG) (DP5 OD021370)
  • National Science Foundation Graduate and Postdoctoral Research Fellowship
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
  • Social Sciences › Psychology › Clinical Psychology › Child and Adolescent Psychosocial and Emotional Development
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
Keywords
adolescence, emotional reactivity, emotion regulation, limbic system, cognitive control, self-regulation, early adulthood
MeSH terms
Adolescent, Adult, Brain, Brain Mapping, Child, Child Development, Cognition, Emotions, Humans, Neural Pathways, Adolescent Development, Young Adult, Functional Neuroimaging

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