Cited by 258Neural and Behavioral Psychology StudiesNeurotransmitter Receptor Influence on BehaviorChild and Adolescent Psychosocial and Emotional Development

Longitudinal changes in behavioral approach system sensitivity and brain structures involved in reward processing during adolescence

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Urošević, Snežana, Collins, Paul, Muetzel, Ryan, Lim, Kelvin, Luciana, Monica·2012·Developmental Psychology

Abstract

Figure 2 was distorted in production. The correct version is presented in the erratum.] Adolescence is a period of radical normative changes and increased risk for substance use, mood disorders, and physical injury. Researchers have proposed that increases in reward sensitivity (i.e., sensitivity of the behavioral approach system [BAS]) and/or increases in reactivity to all emotional stimuli (i.e., reward and threat sensitivities) lead to these phenomena. The present study is the first longitudinal investigation of changes in reward (i.e., BAS) sensitivity in 9- to 23-year-olds across a 2-year follow-up. Support was found for increased reward sensitivity from early to late adolescence, and evidence was found for decline in the early 20s. This decline is combined with a decrease in left nucleus accumbens (Nacc) volume, a key structure for reward processing, from the late teens into the early 20s. Furthermore, we found longitudinal increases in sensitivity to reward to be predicted by individual differences in the Nacc and medial orbitofrontal cortex (OFC) volumes at baseline in this developmental sample. Similarly, increases in sensitivity to threat (i.e., behavioral inhibition system sensitivity) were qualified by sex, with only females participants experiencing this increase, and predicted by individual differences in lateral OFC volumes at baseline.

Integrity signals

Registry

Crossref · 10.1037/a0027502

Cites

94 of 94 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

0 of 38 cited sources checked · 0 supported · 0 flagged

  • Findingown data

    Longitudinal increases in Nacc volumes predicted longitudinal increases in BAS Drive scores.

    “longitudinal increases in Nacc volumes from Time 1 to Time 2 significantly predicted longitudinal increases in BAS Drive scores from Time 1 to Time 2, change R2 = .03, p = .039”
    Quote in the paperSubstantial claim
  • Findingown data

    Left Nacc volume decreased from Time 1 to Time 2 across the whole sample.

    “there was a significant main effect of time on the left Nacc with volumes decreasing for the whole sample from Time 1 to Time 2”
    Quote in the paperSubstantial claim
  • Findingown data

    BAS Reward Responsiveness scores increased from Time 1 to Time 2 across the whole sample.

    “there was a significant increase in BAS Reward Responsiveness scores from Time 1 to Time 2 for the whole sample”
    Quote in the paperSubstantial claim
  • Findingown data

    The decrease in left Nacc volume is approximately 8% from late adolescents' Time 1 mean to young adults' Time 2 mean.

    “This decrease is approximately 8% of the left Nacc volume when calculated from the late adolescents' Time 1 mean to the young adults' Time 2 mean”
    Quote in the paperSubstantial claim
  • Findingown data

    Left medial OFC volume at Time 1 had a unique effect on BAS Total change, controlling for right medial OFC and Step 1 predictors.

    “The left medial OFC volume at Time 1 had a significant unique effect controlling for all Step 1 predictors including right medial OFC volume, partial r = .21, p = .012.”
    Quote in the paperSubstantial claim
  • May combine two claims. 26
  • Classified as probably not a substantial claim. 13
  • May combine two claims.

    Findingown data

    At Time 1, early adolescents had lower BAS Reward Responsiveness scores than late adolescents and young adults; at Time 2, the age groups did not differ.

    “At Time 1, early adolescents exhibited lower scores than both late adolescents and young adults (ps ≤ .02). At Time 2, the groups' scores did not differ.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    No significant effects of lateral OFC, medial OFC, or amygdala volumes on BAS Drive change were found.

    “There were no significant effects of lateral OFC, medial OFC and amygdala volumes on BAS Drive score changes from Time 1 to Time 2.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingown data

    At Time 2, late adolescents had greater left Nacc volumes than young adults; there was no age group effect at Time 1.

    “There was a significant effect of age group on left Nacc volumes at Time 2, F (2, 143) = 4.37, p = .014, ηp2 = .06, but not at Time 1. Bonferroni-corrected post-hoc analyses yielded greater left Nacc volumes for late adolescents compared to young adults (p = .008) at Time 2.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    Early adolescents had lower BAS Total scores than late adolescents and young adults, while late adolescents and young adults did not differ.

    “yielded lower BAS Total scores for early adolescents as compared to both late adolescents (p = .008) and young adults (p = .003) across the Time 1 and Time 2 assessments; the latter two groups did not differ from each other”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    Females had greater left amygdala volume than males at Time 2, with no difference at Time 1.

    “a significant interaction of time by sex on the left amygdala, with females exhibiting greater left amygdala volume than males at Time 2 (p = .017) and no difference at Time 1”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingown data

    In cross-sectional analyses, early adolescents aged 9-12 showed lower BAS Drive and BAS Total scores than late adolescents aged 13-17 and young adults aged 18-23, while late adolescents and young adults did not differ.

    “Additionally, in cross-sectional analyses, we found early adolescents (i.e., ages 9 to 12) to exhibit lower levels of BAS Drive and the BAS Total as compared to late adolescents (i.e., ages 13 to 17) and young adults (i.e., ages 18 to 23), with no differences between the two latter age groups.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    Early adolescents had lower BAS Drive scores than late adolescents and young adults, while late adolescents and young adults did not differ.

    “yielded lower BAS Drive scores for early adolescents as compared to both late adolescents (p = .005) and young adults (p < .001), who did not differ from each other”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    Early adolescent females showed lower threat reactivity than late adolescent and young adult females, with no difference between the latter two groups.

    “Furthermore, early adolescent females exhibited lower reactivity to threat compared to late adolescent and young adult females, with no difference between the two latter groups.”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationown data

    The cross-sectional age pattern alternatively suggests age-cohort effects.

    “Alternatively, the pattern suggests age-cohort effects.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Preliminary cross-sectional evidence indicates decreases in BAS sensitivity in elderly populations.

    “Interestingly, there is also preliminary cross-sectional evidence for decreases in BAS sensitivity in elderly populations (Jorm et al., 1999).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Jorm et al., 1999

      Not checked in the free run.

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

    Study design and conductnone given

    All automatically generated volumes were visually inspected for accuracy, and manual corrections were carried out as needed.

    “All automatically generated volumes were visually inspected for accuracy, and manual corrections using FreeSurfer tools were carried out as needed.”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    The BIS/BAS scales predict relevant prospective clinical symptoms.

    “and relevant prospective clinical symptoms (e.g., Meyer, Johnson, & Winters, 2001)”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Meyer, Johnson, & Winters, 2001

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Adolescents compared to adults exhibit greater ventral striatal activation after winning money and increased Nacc activity during risk-taking.

    “adolescents, compared to adults, exhibit greater ventral striatal activation (which includes Nacc) after winning money (Ernst et al., 2005) and increased activity in the Nacc during risk-taking (Galvan et al., 2006).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Ernst et al., 2005

      Not checked in the free run.

    • cites Galvan et al., 2006

      Not checked in the free run.

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

    Study design and conductown data

    There were no significant demographic differences between Time 2 completers and non-completers, except completers were slightly younger.

    “There were no significant differences in demographic information between participants who completed the Time 2 assessment versus those who did not, except that individuals who completed the Time 2 assessment were slightly younger than non-completers”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Premisecitation

    The multifaceted nature of reward sensitivity is supported by factor analyses of BAS items and by Carver and White's original formulation.

    “The multifaceted nature of reward sensitivity is supported by multi-factor solutions in factor analyses of the BAS scales' items (Cooper et al., 2007) and by Carver and White's original formulation of the scales (1994).”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Cooper et al., 2007

      Not checked in the free run.

    • cites Carver & White, 1994

      Not checked in the free run.

  • May combine two claims.

    Interpretationcitation

    The present cross-sectional finding that certain aspects of reward sensitivity are stable from late adolescence into young adulthood is consistent with prior longitudinal evidence of two-year stability in BAS sensitivity during the mid-twenties.

    “The present cross-sectional findings of stability of certain aspects of reward sensitivity (e.g., persistence in reward pursuit) from late adolescence into young adulthood are consistent with prior longitudinal findings of two-year stability in BAS sensitivity during mid-twenties (Takahashi et al., 2007).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Takahashi et al., 2007

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    The medial OFC is implicated in processing the expected value of reinforcers, and the lateral OFC in processing punishers.

    “The medial OFC and lateral OFC have been implicated in the processing of the expected value of reinforcers and punishers, respectively (Kringelbach & Rolls, 2004; but for different view see Morrison & Salzman, 2009).”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Kringelbach & Rolls, 2004

      Not checked in the free run.

    • cites Morrison & Salzman, 2009

      Not checked in the free run.

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

    Study design and conductown data

    Analyses controlled for scanner upgrade status and sex.

    “which examined effects of continuous covariate age, controlling for scanner upgrade status and sex”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductcitation

    FreeSurfer morphometric procedures exhibit good test-retest reliability across scanner manufacturers and field strengths.

    “FreeSurfer morphometric procedures exhibit good test-retest reliability across scanner manufacturers and across field strengths (Han et al., 2006).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Han et al., 2006

      Not checked in the free run.

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

    Premisecitation

    The BIS/BAS scales correlate with EEG indices of approach and withdrawal affective styles.

    “the BIS/BAS scales correlate with EEG indices of approach and withdrawal affective styles (Harmon-Jones & Allen, 1997; Sutton & Davidson, 1997)”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Harmon-Jones & Allen, 1997

      Not checked in the free run.

    • cites Sutton & Davidson, 1997

      Not checked in the free run.

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

    Premisecitation

    BAS Drive measures persistence in reward pursuit, BAS Fun Seeking measures desire for novel rewards and impulsive approach, and BAS Total is a composite index of overall reward sensitivity.

    “The BAS Drive is proposed to measure persistence in pursuit of rewards, the BAS Fun Seeking a mix of desire for novel rewards and impulsive approach to rewards, and the BAS Total, as a composite measure of the three scales, an index of overall reward sensitivity (Carver & White, 1994).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Carver & White, 1994

      Not checked in the free run.

  • May combine two claims.

    Interpretationown data

    Persistence in reward pursuit and overall reward sensitivity remain elevated from late adolescence into young adulthood, while positive affective responses to rewards begin to decline in the early twenties.

    “Thus, the present study suggests that persistence in pursuit of rewards and overall reward sensitivity remain elevated from the late teens into young adulthood, even while positive affective responses to rewards (i.e., BAS Reward Responsiveness) start to decrease in the early twenties.”
    Quote in the paperSubstantial claim
  • Classified as probably not a substantial claim.

    Premisecitation

    The BIS/BAS scales predict experimental responses to rewards and punishments.

    “as well as predict experimental responses to rewards and punishments (e.g., Carver & White, 1994)”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Carver & White, 1994

      Not checked in the free run.

  • May combine two claims.

    Study design and conductown data

    Scanner upgrade status had a significant main effect on left Nacc but no interaction with age and/or time, so it does not account for the observed age by time interaction.

    “there was a significant main effect of scanner upgrade status, F (1, 145) = 9.26, p = .003, ηp2 = .06, but no significant interaction effects of scanner upgrade status by age and/or time. Thus, this scanner upgrade effect does not account for the observed age by time interaction.”
    Quote in the paperSubstantial claim
  • Classified as probably not a substantial claim.

    Study design and conductnone given

    Volumes of each region were corrected for total brain volume prior to analysis.

    “Volumes of each region were corrected for total brain volume prior to analysis and represented as ratios of ROI volume to total brain volume.”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    One other study also failed to find a sex difference in reward sensitivity during adolescence.

    “It should be noted that one other study has also failed to find this sex difference in reward sensitivity during adolescence (Giles & Price, 2008).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Giles & Price, 2008

      Not checked in the free run.

  • May combine two claims.

    Interpretationown data

    The sex-difference pattern partially replicates prior findings of greater threat sensitivity in females and suggests a more specific time interval for the emergence of this sex difference, namely the transition from early to late adolescence.

    “This pattern of sex differences partially replicates prior findings of greater threat sensitivity in females (e.g., Knyazev, 2004; Vermeersch et al., 2009) and extends prior studies by suggesting a more specific time interval for the emergence of sex differences in threat sensitivity, i.e., the transition from early adolescence to late adolescence.”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Knyazev, 2004

      Not checked in the free run.

    • cites Vermeersch et al., 2009

      Not checked in the free run.

  • May combine two claims.

    Interpretationown data

    While reward sensitivity peaks in adolescence for both males and females, only females appear to show similar increases in threat sensitivity.

    “In other words, whereas sensitivity to reward peaks in adolescence for males and females, it appears that only females experience similar increases in sensitivity to threat.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Interpretationown data

    The overall sex-difference pattern implies greater emotional reactivity in females than males and increasing threat sensitivity in females but not males during the transition from early adolescence to young adulthood.

    “The overall pattern of the present sex difference findings implies greater emotional reactivity for females compared to males, and increasing sensitivity to threat for females and not males, during transition from early adolescents to young adulthood.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Study design and conductreasoning

    Specialized preprocessing, a unique longitudinal processing procedure, and using scanner upgrade as a covariate ensure that observed brain volume effects are above and beyond scanner upgrade effects.

    “However, use of specialized preprocessing to account for differences in image distortion before and after the upgrade, use of a unique longitudinal processing procedure to minimize methodological variance, and the use of scanner upgrade as a covariate in all relevant analyses, ensure that the observed brain volume effects are above and beyond effects explained by the scanner upgrade.”
    Quote in the paperSubstantial claim
  • Classified as probably not a substantial claim.

    Study design and conductnone given

    An MR scanner upgrade occurred during the second assessment.

    “There was also an MR scanner upgrade that occurred in the midst of the second assessment.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Premisecitation

    When controlling for total brain volume, cross-sectional analyses have revealed sex differences in striatum volumes during adolescence but not in amygdala volumes.

    “However, when controlling for total brain volume, cross-sectional analyses have only revealed sex differences in striatum volumes during adolescence and not in amygdala volumes (e.g., Giedd et al., 1997).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Giedd et al., 1997

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    BAS and BIS hypersensitivities have been linked to greater risks for mood and anxiety disorders, respectively.

    “Both BAS and BIS hypersensitivities have been linked to greater risks for mood and anxiety disorders, respectively (e.g., Depue & Iacono, 1989; Fowles, 1987; Gray, 1991, 1994; Pinto-Meza et al., 2006; Urošević, Abramson, Harmon-Jones, & Alloy, 2008).”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Depue & Iacono, 1989

      Not checked in the free run.

    • cites Fowles, 1987

      Not checked in the free run.

    • cites Gray, 1991, 1994

      Not checked in the free run.

  • May combine two claims.

    Interpretationown data

    Both longitudinal and cross-sectional analyses support that reward sensitivity is elevated during adolescence, with potentially different trajectories for different aspects in the early twenties.

    “Both the present longitudinal and cross-sectional analyses support that reward sensitivity is elevated during adolescence, but with potential different trajectories for different aspects of reward sensitivity during early 20's.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Study design and conductown data

    The sample was predominantly Caucasian and of middle to upper-middle socio-economic background.

    “Given the present sample's predominantly Caucasian and middle to upper-middle socio-economic background, replications in samples of different ethnic and socio-economic background are also needed to establish greater generalizability of the present findings.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Study design and conductcitation

    FreeSurfer outputs were visually inspected and manually edited when necessary, and automated procedures have been found to be as reliable as manual procedures in prior studies.

    “Another potential limitation is the use of automatized process for subcortical segmentation and cortical parcellation; however, FreeSurfer's outputs were visually inspected and manually edited when necessary and these automatized procedures have been found to be just as reliable as manual procedures in prior studies (e.g., Fischl et al., 2002).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Fischl et al., 2002

      Not checked in the free run.

36 of 36
  • The paper relies on this without support.

    Longitudinal data on changes in BAS and BIS sensitivities in adolescence is lacking in the published literature.

    “Longitudinal data with assessments of BAS and BIS sensitivities could address these questions but is lacking in the published literature.”
  • The paper relies on this without support.

    Longitudinal data on structural changes in brain regions relevant for reward and threat processing during adolescence are sparse.

    “Longitudinal data on the structural changes in brain regions relevant for the processing of reward (and threat) during adolescence are also sparse.”
  • The paper relies on this without support.

    There is a paucity of longitudinal data assessing structural changes within reward circuitry and whether structural changes relate to variation in reward sensitivity.

    “There is a paucity of longitudinal data assessing structural changes within reward circuitry, and whether structural changes relate to variation in reward sensitivity.”
  • The paper relies on this without support.

    The cross-sectional age differences in BAS Total and BAS Drive reflect developmental change rather than age-cohort effects.

    “This patterning suggests that BAS-Drive scores, like the BAS Total, either increase markedly from early adolescence to late adolescence and then persist into young adulthood, or that there are significant age-cohort effects.”
  • The paper relies on this without support.

    The left Nacc decrease from late teens to early twenties reflects developmental change rather than cohort effects.

    “This pattern of results suggests that there is a decrease in the left Nacc volume that occurs in the transition from the late teens to early twenties, but likely over a more protracted time period than the two-year follow-up captured by this study”
5 of 5

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Every reported test result, recomputed from its test statistic and degrees of freedom. A result shows as not adding up only once an independent check has confirmed it.

  • ConsistentF(1, 52) = 6.35reported p = .015 · recomputed p = .015

    “F (1, 52) = 6.35, p = .015”

  • ConsistentF(2, 143) = 4.37reported p = .014 · recomputed p = .014

    “F (2, 143) = 4.37, p = .014”

  • ConsistentF(1, 145) = 9.26reported p = .003 · recomputed p = .003

    “F (1, 145) = 9.26, p = .003”

3 of 3

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Authors
Urošević, S., Collins, P., Muetzel, R., Lim, K., & Luciana, M.
Affiliations
University of Minnesota (US)
Venue
Developmental Psychology
Published
2012-09
Volume
48
Issue
5
Pages
1488-1500
ISSN
  • 0012-1649 (ISSN-L)
  • 1939-0599
OpenAlex
W1966407031
Cited by
258
References
88
Citations by year
2026: 9 · 2025: 8 · 2024: 15 · 2023: 24 · 2022: 11 · 2021: 12 · 2020: 57 · 2019: 16 · 2018: 24 · 2017: 21 · 2016: 14 · 2015: 20 · 2014: 14 · 2013: 9 · 2012: 3
FWCI
7.53
Type
journal article
Language
en
Open access
Locations
  • Developmental Psychology (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • National Institute of Mental Health (T32 MH 017069)
  • National Institute on Drug Abuse (Grant R01 DA 017843)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
  • Social Sciences › Psychology › Clinical Psychology › Child and Adolescent Psychosocial and Emotional Development
Keywords
reward sensitivity, behavioral approach system, behavioral inhibition system, threat sensitivity, adolescence, nucleus accumbens, medial orbitofrontal cortex, lateral orbitofrontal cortex, brain structure volume, individual differences, sex differences, longitudinal development, substance use risk
MeSH terms
Adolescent, Age Factors, Analysis of Variance, Brain, Brain Mapping, Child, Cross-Sectional Studies, Female, Humans, Image Processing, Computer-Assisted, Inhibition, Psychological, Longitudinal Studies, Magnetic Resonance Imaging, Male, Reward, Sex Factors, Time Factors, Adolescent Development, Young Adult

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