CoChat
Sign Up
Cited by 67Neural and Behavioral Psychology StudiesChild and Adolescent Psychosocial and Emotional DevelopmentNeurotransmitter Receptor Influence on Behavior

Testosterone during puberty shifts emotional control from pulvinar to anterior prefrontal cortex

Open access
Tyborowska, Anna, Volman, Inge, Smeekens, Sanny, Toni, Ivan, Roelofs, Karin·2016·The Journal of Neuroscience
DOI 10.1523/jneurosci.3874-15.2016PMC PMC6604884
Open this paper in CoChat — free accountOpen PDF

Abstract

UNLABELLED: Increased limbic and striatal activation in adolescence has been attributed to a relative delay in the maturation of prefrontal areas, resulting in the increase of impulsive reward-seeking behaviors that are often observed during puberty. However, it remains unclear whether and how this general developmental pattern applies to the control of social emotional actions, a fundamental adult skill refined during adolescence. This domain of control pertains to decisions involving emotional responses. When faced with a social emotional challenge (e.g., an angry face), we can follow automatic response tendencies and avoid the challenge or exert control over those tendencies by selecting an alternative action. Using an fMRI-adapted social approach-avoidance task, this study identifies how the neural regulation of emotional action control changes as a function of human pubertal development in 14-year-old adolescents (n = 47). Pubertal maturation, indexed by testosterone levels, shifted neural regulation of emotional actions from the pulvinar nucleus of the thalamus and the amygdala to the anterior prefrontal cortex (aPFC). Adolescents with more advanced pubertal maturation showed greater aPFC activity when controlling their emotional action tendencies, reproducing the same pattern consistently observed in adults. In contrast, adolescents of the same age, but with less advanced pubertal maturation, showed greater pulvinar and amygdala activity when exerting similarly effective emotional control. These findings qualify how, in the domain of social emotional actions, executive control shifts from subcortical to prefrontal structures during pubertal development. The pulvinar and the amygdala are suggested as the ontogenetic precursors of the mature control system centered on the anterior prefrontal cortex. SIGNIFICANCE STATEMENT: Adolescents can show distinct behavioral problems when emotionally aroused. This could be related to later development of frontal regions compared with deeper brain structures. This study found that when the control of emotional actions needs to be exerted, more mature adolescents, similar to adults, recruit the anterior prefrontal cortex (aPFC). Less mature adolescents recruit specific subcortical regions, namely the pulvinar and amygdala. These findings identify the subcortical pulvino-amygdalar pathway as a relevant precursor of a mature aPFC emotional control system, opening the way for a neurobiological understanding of how emotion control-related disorders emerge during puberty.

AI snapshot

Written from the paper’s full text.

TL;DR

In 14-year-olds, testosterone-indexed pubertal maturation shifted neural control of emotional action tendencies from the pulvinar and amygdala to the anterior prefrontal cortex (aPFC). More mature adolescents resembled adults by recruiting aPFC during affect-incongruent trials, whereas less mature adolescents recruited subcortical pulvino-amygdalar regions.

Key findings

  • In 47 14-year-olds (21 males), affect-incongruent versus congruent trials produced behavioral congruency effects: longer reaction times and more errors (RT Valence × Response: F(1,43) = 17.44, p < 0.001, ηp² = 0.289; ER: F(1,43) = 4.721, p = 0.035, ηp² = 0.099). Testosterone did not significantly interact with behavioral congruency (F(1,43) = 0.097, p = 0.757).
  • Testosterone positively modulated the right aPFC congruency effect (local maximum 40, 58, −6; SVC p = 0.04) and negatively modulated thalamus/pulvinar (local maximum −8, −20, 16; p < 0.001) and right amygdala (26, −2, −14; SVC p = 0.026). Confirmatory pulvinar ROI effects were bilateral (left SVC pFWE = 0.028; right SVC pFWE = 0.037).
  • Testosterone predicted stronger aPFC congruency effects in participants with weaker pulvinar effects (Congruency × Region × Testosterone: F(1,45) = 18.17, p < 0.001, ηp² = 0.288) and weaker amygdala effects (F(1,45) = 17.72, p < 0.001, ηp² = 0.282); effects were present in boys and girls.
  • VBM found no significant testosterone-related gray matter differences in aPFC, pulvinar, or amygdala. Amygdala-pulvinar connectivity changed with combined testosterone and error rates (right thalamic ROI SVC pFWE = 0.043; right pulvinar confirmatory SVC pFWE = 0.022). Testosterone correlated with PDS scores (r = 0.29, p = 0.048).

Methods

  • Cross-sectional fMRI study of 49 recruited 14-year-old right-handed adolescents; 2 were excluded for poor MRI image quality, leaving 47 participants (21 males). Pubertal maturation was indexed by salivary testosterone (two samples 2 h apart after 10:00 A.M.; first measurement used) and the Pubertal Development Scale.
  • Participants performed an fMRI-adapted social approach-avoidance task with happy and angry faces and joystick approach/avoid responses; affect-congruent conditions were approach-happy and avoid-angry, and affect-incongruent conditions were approach-angry and avoid-happy.
  • Imaging used a 3T multiecho EPI sequence and SPM8. Analyses included random-effects multiple regression with testosterone and cortisol covariates, ROI analyses for aPFC and amygdala, psychophysiological interaction analysis with right amygdala seed, and VBM; fMRI inferences used cluster-level FWE p < 0.05 and ROI SVC p < 0.05.

Limitations

  • Stated: the anatomical specificity of the pulvinar effect is limited by cluster-level statistics because the cluster included anterior and medial thalamic nuclei and the caudate nucleus; future studies are needed to differentiate their contributions.
  • Stated: broad extension to adolescent behavior in emotionally arousing situations is speculative and may require stronger social emotional challenges, such as the zooming version of the approach-avoidance task.
  • Evident: the cross-sectional, single-age design cannot directly test a longitudinal developmental transition; the paper itself calls for longitudinal studies to test whether affective disorders relate to altered transition between pulvino-amygdalar and aPFC control systems.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1523/jneurosci.3874-15.2016

Cites

82 of 82 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

0 of 54 cited sources checked · 0 supported · 0 flagged

  • Findingown data

    The congruency effect in the right aPFC was positively modulated by testosterone.

    “The congruency effect in the right aPFC (local maximum: 40, 58, Ϫ6) was positively modulated by testosterone, indicating that adolescents with high testosterone levels showed a stronger aPFC effect for incongruent compared with congruent trials.”
    Quote in the paperSubstantial claim
  • Findingown data

    The congruency effect in the thalamus showed a significant negative modulation by testosterone.

    “In contrast, the congruency effect in the thalamus (local maximum: Ϫ8, Ϫ20, 16) and right amygdala (local maximum: 26, Ϫ2, Ϫ14) showed significant negative modulations by testosterone”
    Quote in the paperSubstantial claim
  • Findingown data

    Behavioral congruency effects did not significantly interact with testosterone.

    “These behavioral congruency effects did not significantly interact with testosterone (F (1,43) ϭ 0.097, p ϭ 0.757) or gender (F (1,43) ϭ 0.008, p ϭ 0.928).”
    Quote in the paperNot a substantial claim
  • Findingown data

    The congruency effect in the right amygdala showed a significant negative modulation by testosterone.

    “In contrast, the congruency effect in the thalamus (local maximum: Ϫ8, Ϫ20, 16) and right amygdala (local maximum: 26, Ϫ2, Ϫ14) showed significant negative modulations by testosterone”
    Quote in the paperSubstantial claim
  • Findingown data

    A confirmatory ROI analysis of the pulvinar indicated a bilateral significant modulatory effect of testosterone.

    “A confirmatory ROI analysis of the pulvinar (mask extracted from the Automated Talairach Atlas) indicated a bilateral significant modulatory effect of testosterone (local maximum left: Ϫ10, Ϫ24, 16; voxel extent: 14; SVC p FWE ϭ 0.028; local maximum right: 24, Ϫ24, 12; voxel extent: 8; SVC p FWE ϭ 0.037).”
    Quote in the paperSubstantial claim
  • May combine two claims. 14
  • Classified as probably not a substantial claim. 10

  • May combine two claims.

    Findingown data

    Individuals with high testosterone levels showed relatively stronger aPFC congruency effects, whereas participants with low testosterone levels showed relatively stronger congruency effects in the pulvinar and amygdala.

    “In summary, individuals with high testosterone levels showed relatively stronger aPFC congruency effects, whereas participants with low testosterone levels showed relatively stronger congruency effects in the pulvinar and amygdala (Fig. 2).”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    Regardless of pubertal maturation, adolescents had matched performance in exerting emotional control, irrespective of aPFC or amygdala-pulvinar circuitry involvement.

    “On the other hand, regardless of pubertal maturation, adolescents had matched performance in exerting emotional control and, as such, irrespective of aPFC or amygdala-pulvinar circuitry involvement.”
    Quote in the paperSubstantial claim

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

    Study design and conductnone given

    For ROI analyses, a small volume correction (SVC; p < 0.05) was performed.

    “For ROI analyses, a small volume correction (SVC; p Ͻ 0.05) was performed.”
    Quote in the paperNot a substantial claim

  • Classified as probably not a substantial claim.

    Study design and conductown data

    Whole-brain analysis inferences were made at the cluster level (p FWE < 0.05), based on a cluster-forming threshold of p < 0.001 (uncorrected).

    “Whole-brain analysis inferences were made at the cluster level ( p FWE Ͻ 0.05), based on a cluster-forming threshold of p Ͻ 0.001 (uncorrected).”
    Quote in the paperSubstantial claim

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

    Study design and conductown data

    Testosterone values between the first and second measurement did not differ significantly either for boys or girls.

    “Testosterone values between the first and second measurement did not differ significantly either for boys (t (19) ϭ Ϫ0.99, p ϭ 0.333) or girls (t (25) ϭ Ϫ0.66, p ϭ 0.514).”
    Quote in the paperNot a substantial claim

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

    Study design and conductown data

    Two participants were excluded due to technical problems (poor MRI image quality), resulting in 47 participants included in the final analyses.

    “Two participants were excluded due to technical problems (poor MRI image quality), resulting in 47 participants (21 males) who were included in the final analyses.”
    Quote in the paperNot a substantial claim

  • Classified as probably not a substantial claim.

    Study design and conductnone given

    Activations were corrected for multiple comparisons using familywise error (FWE).

    “Activations were corrected for multiple comparisons using familywise error (FWE).”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationown data

    Adolescents with more advanced pubertal maturation showed greater aPFC activity when controlling their emotional action tendencies, reproducing the same pattern consistently observed in adults.

    “Adolescents with more advanced pubertal maturation showed greater aPFC activity when controlling their emotional action tendencies, reproducing the same pattern consistently observed in adults.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Study design and conductown data

    The study design minimized the effects of diurnal fluctuations on testosterone level estimation by sampling this hormone in duplicate, taken 2 h apart, after 10:00 A.M., resulting in consistent measurements across these two time points.

    “The study design minimized the effects of those fluctuations on testosterone level estimation by sampling this hormone in duplicate, taken 2 h apart, after 10:00 A.M., resulting in consistent measurements across these two time points.”
    Quote in the paperSubstantial claim

  • Classified as probably not a substantial claim.

    Premisecitation

    Recent diffusion tensor imaging studies have shown that during early development connectivity among subcortical structures is more prevalent than during later development.

    “Recent diffusion tensor imaging studies have shown that, during early development, connectivity among subcortical structures is more prevalent than during later development (Simmonds et al., 2014;Baker et al., 2015).”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Simmonds et al., 2014

      Not checked in the free run.

    • cites Baker et al., 2015

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S2 (checkable). May combine two claims.

    Interpretationreasoning

    These results are relevant for neurobiological models of pubertal development, qualifying the circuits implicated in the maturation of emotional action control.

    “These results are relevant for neurobiological models of pubertal development, qualifying the circuits implicated in the maturation of emotional action control.”
    Quote in the paperNot a substantial claim

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

    Premisecitation

    The zooming effect has been shown to enhance the congruency effect and is especially sensitive in capturing failures in emotion action control in various psychopathologies.

    “The zooming effect (the angry face becomes larger-approach or smaller-avoid, depending on the response) has been shown to enhance the congruency effect and is especially sensitive in capturing failures in emotion action control in various psychopathologies (Roelofs et al., 2009b(Roelofs et al., , 2010;;von Borries et al., 2012).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Roelofs et al., 2009b

      Not checked in the free run.

    • cites von Borries et al., 2012

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    The pulvinar facilitates fast emotional saliency detection and threat recognition.

    “Furthermore, the pulvinar connects the superior colliculus with the amygdala (Morris et al., 1999;Tamietto et al., 2012), and facilitates fast emotional saliency detection and threat recognition (Ward et al., 2005(Ward et al., , 2007;;Padmala et al., 2010;Nguyen et al., 2013a).”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Ward et al., 2005

      Not checked in the free run.

    • cites Ward et al., 2007

      Not checked in the free run.

    • cites Padmala et al., 2010

      Not checked in the free run.

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

    Premisecitation

    Chronic failures in emotion action control are common in various psychopathologies, such as social anxiety and aggression-related disorders.

    “Chronic failures in emotion action control are common in vari-ous psychopathologies, such as social anxiety (Roelofs et al., 2009b(Roelofs et al., , 2010) ) and aggression-related disorders (von Borries et al., 2012).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Roelofs et al., 2009b

      Not checked in the free run.

    • cites von Borries et al., 2012

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    The centromedial amygdala shows connectivity patterns with subcortical regions, including the pulvinar, whereas the lateral basal amygdala shows connectivity patterns with prefrontal areas.

    “The centromedial amygdala shows connectivity patterns with subcortical regions, including the pulvinar, whereas the lateral basal amygdala shows connectivity patterns with prefrontal areas (Roy et al., 2009;Bzdok et al., 2013).”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Roy et al., 2009

      Not checked in the free run.

    • cites Bzdok et al., 2013

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Previous work has shown that testosterone is more closely related to physicians' ratings of pubertal maturation than self-reports, providing an objective and validated proxy of the actual pubertal stage.

    “In fact, previous work has shown that testosterone is more closely related to physicians' ratings of pubertal maturation than self-reports, providing an objective and validated proxy of the actual pubertal stage (Huang et al., 2012).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Huang et al., 2012

      Not checked in the free run.

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

    Premisecitation

    The anterior and medial thalamic nuclei and the caudate nucleus are also involved in goal-directed and stimulus-response actions.

    “These regions are also involved in goal-directed and stimulus-response actions (Packard and Knowlton, 2002;Ostlund and Balleine, 2008;Bradfield et al., 2013;Parnaudeau et al., 2015).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Packard and Knowlton, 2002

      Not checked in the free run.

    • cites Ostlund and Balleine, 2008

      Not checked in the free run.

    • cites Bradfield et al., 2013

      Not checked in the free run.

  • May combine two claims.

    Interpretationown data

    These findings qualify and extend the notion of a developmental shift in executive control from subcortical to prefrontal regions.

    “These findings qualify and extend the notion of a developmental shift in executive control from subcortical to prefrontal regions (Blakemore, 2008;Ernst and Fudge, 2009;Crone and Dahl, 2012).”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Blakemore, 2008

      Not checked in the free run.

    • cites Ernst and Fudge, 2009

      Not checked in the free run.

    • cites Crone and Dahl, 2012

      Not checked in the free run.

  • May combine two claims.

    Interpretationown data

    Developmentally more mature adolescents, in a manner similar to that of adults, recruit the aPFC during the control of emotional action tendencies, whereas less mature adolescents recruit the pulvinar and amygdala.

    “Developmentally more mature adolescents, in a manner similar to that of adults, recruit the aPFC during the control of emotional action tendencies, whereas less mature adolescents recruit the pulvinar and amygdala.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    The choice of testosterone levels as an objective and physiological marker of pubertal development is supported by previous work and by the fact that this hormone is mechanistically involved in neuronal reorganization during adolescence.

    “The choice of testosterone levels as an objective and physiological marker of pubertal development is supported by previous work (Shirtcliff et al., 2009;Huang et al., 2012), and by the fact that this hormone is mechanistically involved in neuronal reorganization during adolescence (Sisk and Zehr, 2005;Schulz et al., 2009;Herting et al., 2014).”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Shirtcliff et al., 2009

      Not checked in the free run.

    • cites Huang et al., 2012

      Not checked in the free run.

    • cites Sisk and Zehr, 2005

      Not checked in the free run.

  • May combine two claims.

    Study design and conductown data

    The study design minimized the effects of testosterone level fluctuations, as can be seen in consistent measurements across two time points, sampled 2 h apart.

    “The study design minimized the effects of testosterone level fluctuations (Albertsson-Wikland et al., 1997;Ankarberg and Norjavaara, 1999), as can be seen in consistent measurements across two time points, sampled 2 h apart.”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Albertsson-Wikland et al., 1997

      Not checked in the free run.

    • cites Ankarberg and Norjavaara, 1999

      Not checked in the free run.

21 of 21

  • The paper relies on this without support.

    It remains unclear whether and how the general developmental pattern of frontostriatal imbalance applies to the control of social emotional actions.

    “However, it remains unclear whether and how this general developmental pattern applies to the control of social emotional actions, a fundamental adult skill refined during adolescence.”

  • The paper relies on this without support.

    It remains unclear whether and how the pulvinar is involved in emotional processing when the aPFC is not yet sufficiently mature to implement flexible goal-directed control of emotional action tendencies.

    “However, it remains unclear whether and how the pulvinar is involved in emotional processing when the aPFC is not yet sufficiently mature to implement flexible goal-directed control of emotional action tendencies.”

  • The paper relies on this without support.

    How emotional action control is neurally implemented during puberty is largely unexplored.

    “This study addresses the largely unexplored issue of how emotional action control is neurally implemented during puberty.”

  • The paper relies on this without support.

    The emotional control demands evoked by the AA task are rather mild.

    “at least within the rather mild emotional control demands evoked by the AA task.”

  • The paper relies on this without support.

    The design isolates puberty-related cerebral changes without generic age-related differences in executive control development.

    “This controlled situation is a major advantage of the current experimental design, focused on isolating puberty-related cerebral changes without generic age-related differences in executive control development.”
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?

  • In 14-year-old adolescents, higher testosterone levels were associated with greater control over emotional actions and increased recruitment of the anterior prefrontal cortex.

    “Higher testosterone levels were associated with greater control over emotional actions and increased recruitment of the anterior prefrontal cortex.”

    From Does puberty mark a transition in sensitive periods for plasticity in the associative neocortex? (2017) · cites this paper as Tyborowska et al., 2016

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

Each contradiction between two passages listed here was confirmed by an independent check.

  • Shortest echo time reported as both 9.3 and 9.4 ms

    Minor

    The acquisition parameters list the shortest echo time as 9.3 ms, but the preprocessing description calls it 9.4 ms.

1 of 1

Cites

Flagged first, then by citations

Cited by

Sorted by citations

Related

Authors
Tyborowska, A., Volman, I., Smeekens, S., Toni, I., & Roelofs, K.
Affiliations
Radboud University Nijmegen (NL)
ORCID
Venue
The Journal of Neuroscience
Publisher
Society for Neuroscience
Published
2016-06-08
Volume
36
Issue
23
Pages
6156-6164
ISSN
  • 0270-6474 (ISSN-L)
  • 1529-2401
DOI
10.1523/jneurosci.3874-15.2016
PMC
PMC6604884
OpenAlex
W2410259914
Semantic Scholar
3042509380d0d23366dbc4fdb696385a44837b64
Cited by
67
References
82
Citations by year
2026: 2 · 2025: 9 · 2024: 1 · 2023: 8 · 2022: 3 · 2021: 5 · 2020: 9 · 2019: 16 · 2018: 9 · 2017: 1 · 2016: 3
FWCI
6.15
Type
journal article
Language
en
Open access
Locations
  • Journal of Neuroscience (publishedVersion)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • UCL Discovery (University College London) (submittedVersion)
  • Radboud Repository (Radboud University) (submittedVersion)
  • DSpace (Open University in the Netherlands) (submittedVersion, cc-by)
  • Radboud Repository (Radboud University) (submittedVersion, other-oa)
Funders
Nederlandse Organisatie voor Wetenschappelijk Onderzoek (ERC_StG2012_313749, 453-12-001)
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 › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Keywords
testosterone, puberty, pubertal development, anterior prefrontal cortex, pulvinar, amygdala, approach-avoidance task, social-emotional behavior, executive function, adolescent brain development
MeSH terms
Adolescent, Brain Mapping, Emotions, Female, Humans, Hydrocortisone, Image Processing, Computer-Assisted, Male, Movement, Neural Pathways, Oxygen, Photic Stimulation, Psychomotor Performance, Surveys and Questionnaires, Reaction Time, Saliva, Sexual Maturation, Testosterone, Prefrontal Cortex, Pulvinar

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Claims read by deepseek-v4.1-flash under definition version 3 (extract-v3) on 2026-10-10.

Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-10-10.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review