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Cited by 156Neurotransmitter Receptor Influence on BehaviorNeural and Behavioral Psychology StudiesSchizophrenia research and treatment

Dopaminergic modulation of incentive motivation in adolescence: age-related changes in signaling, individual differences, and implications for the development of self-regulation

Open access
Luciana, Monica, Wahlstrom, Dustin, Porter, James N., Collins, Paul F.·2012·Developmental Psychology
DOI 10.1037/a0027432PMC PMC3341492
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Abstract

Behavioral activation that is associated with incentive-reward motivation increases in adolescence relative to childhood and adulthood. This quadratic developmental pattern is generally supported by behavioral and experimental neuroscience findings. It is suggested that a focus on changes in dopamine neurotransmission is informative in understanding the mechanism for this adolescent increase in reward-related behavioral activation and subsequent decline into adulthood. Evidence is presented to indicate that incentive-reward motivation is modulated by mesoaccumbens dopamine, and that it increases in adolescence before declining into adulthood because of normative developmental changes at the molecular level. Potential mechanisms of variation in functional mesoaccumbens dopamine transmission are discussed with a focus on the interplay between tonic and phasic modes of dopamine transmission in modulating both general incentive-motivational biases and the efficacy of reward learning during exposure to novel reward experiences. Interactions between individual difference factors and these age-related trends are discussed.

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Written from the paper’s full text.

TL;DR

This review argues that adolescent incentive-reward motivation follows a quadratic trajectory—rising above childhood and adulthood—and proposes that normative changes in mesoaccumbens dopamine transmission, especially tonic versus phasic signaling, help explain this pattern and its individual differences. It integrates human behavioral/neuroimaging and animal evidence but concludes that direct human tests of the dopamine model are still lacking.

Key findings

  • Adolescents show heightened incentive-reward motivation and behavioral activation relative to children and adults, with self-reported sensation-seeking peaking around ages 12–15 in a cross-sectional study of over 900 individuals aged 10–30 (Steinberg et al., 2008), and mid-adolescents (ages 13–17) reporting higher reward responsivity than younger adolescents (ages 9–12) or young adults (ages 18–23) in the authors’ lab.
  • Epidemiological data cited show that 21.1% of U.S. youth have consumed alcohol and 7.5% have tried marijuana before age 13, rising to 72.5% and 36.8%, respectively, by the end of high school (Eaton et al., 2010).
  • Animal evidence indicates adolescent-specific dopamine changes: slow spike firing (3–5 Hz) increases from postnatal days 24–27, peaks around day 48, and declines through day 70; basal DA concentrations show late-adolescent peaks; and D1/D2 receptor densities decline by 35–50% from adolescence to adulthood depending on region.
  • The review proposes that tonic DA levels (extracellular concentrations around 5–20 nM) modulate general incentive-motivational bias and response vigor, while phasic DA bursts (up to 1 mM) support reward learning; individual differences in basal mesoaccumbens DA are hypothesized to place adolescents at lower, optimal, or excessive risk for reward-seeking outcomes.

Methods

  • Narrative review/synthesis of behavioral, epidemiological, animal, and human neuroimaging/pharmacological literature on adolescent incentive motivation and dopamine function; no new primary data are reported.
  • Evidence includes rodent and primate studies of DA firing, receptor density, transporter density, and reward behavior, plus human self-report, fMRI, and PET studies summarized in Tables 1 and 2.
  • Main analysis is conceptual integration, proposing a developmental cascade linking tonic DA, phasic DA, reward learning, and prefrontal-striatal maturation.

Limitations

  • The authors state that the discussion is restricted to the incentive-reward motivational system and its subcortical VTA-NAcc DA substrate, omitting interactions with cognitive control, behavioral inhibition, and adaptive emotional self-regulation.
  • The authors state that the human functional neuroimaging literature is contradictory regarding elevated adolescent NAcc responsivity, that the association relies nearly exclusively on animal research, and that primary mechanisms within the mesoaccumbens DA system are unclear.
  • Evident from the text: this is not a systematic review or meta-analysis; human fMRI studies vary widely in task design, analysis, and sample size, and direct human pharmacological/neurobehavioral testing of the DA model in adolescents remains a future direction.

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Integrity signals

Registry

Crossref · 10.1037/a0027432

Cites

176 of 176 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

0 of 168 cited sources checked · 0 supported · 0 flagged

  • Findingcitation

    Nucleus accumbens volumes increase from early to mid-adolescence and then decline into adulthood.

    “We recently observed increases in nucleus accumbens volumes from early to mid-adolescence and then a decline into adulthood (Urosevic et al., under review).”
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    • cites Urosevic et al., under review

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  • Premisecitation

    Incentive-reward motivation is modulated by mesoaccumbens dopamine.

    “We present evidence to indicate that incentive-reward motivation is modulated by mesoaccumbens dopamine and that it increases in adolescence before declining into adulthood due to normative developmental changes at the molecular level.”
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    • cites Depue & Collins, 1999

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    • cites Wise, 2004

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  • Interpretationreasoning

    The adolescent increase in reward-related behavioral activation and subsequent decline into adulthood is due to normative developmental changes at the molecular level.

    “We present evidence to indicate that incentive-reward motivation is modulated by mesoaccumbens dopamine and that it increases in adolescence before declining into adulthood due to normative developmental changes at the molecular level.”
    Quote in the paperNot a substantial claim
  • Premisecitation

    Genetic variation accounted for one third of the variance in behavioral activation system activity.

    “At least one longitudinal twin study reported that genetic variation accounted for one third of the variance in behavioral activation system activity (Takashi, Yamagata, Kijima, Shigemasu, Ono, & Ando, 2007).”
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    • cites Takashi, Yamagata, Kijima, Shigemasu, Ono, & Ando, 2007

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  • Premisereasoning

    Incentive-reward motivation increases in adolescence relative to childhood and adulthood, following a quadratic developmental pattern that peaks in adolescence.

    “Behavioral activation that is associated with incentive-reward motivation increases in adolescence relative to childhood and adulthood. This quadratic developmental pattern is generally supported by behavioral and experimental neuroscience findings.”
    • Also stated in: § Abstract · plain
      “Our assertion is that adolescents experience an age-related increase in incentive motivation that is above and beyond what they experience in childhood and above and beyond levels experienced in adulthood (see quadratic pattern illustrated in Figure 1).”
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    Findingown data

    Mid-adolescents (ages 13-17) report increases in reward responsivity relative to ages 9-12 and relative to young adulthood (ages 18-23).

    “In our lab, we have observed that mid-adolescents (ages 13–17) report increases in reward responsivity (from Carver and White’s (1994) BIS/BAS questionnaire) relative to levels reported earlier in the adolescent period (around ages 9–12) and relative to levels reported later, during young adulthood (ages 18–23) (Urosevic, Collins, Muetzel, Lim & Luciana, in press).”
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    Findingnone given

    Caudate, amygdala and hippocampus did not show similar quadratic trends in volume.

    “Regions such as the caudate, amygdala and hippocampus did not show similar trends.”
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    Premisecitation

    Adolescents have high levels of social affiliation and spend more time with peers than with parents.

    “In addition, adolescents (relative to both children and adults) have high levels of social affiliation and spend more time with peers than with parents, validating the idea that social acceptance and affiliation are strong natural rewards for this age group (Csikszentmihalyi, Larson & Prescott, 1977; Sebastian, Viding, Williams & Blakemore, 2010; Steinberg, 2008).”
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    • cites Csikszentmihalyi, Larson & Prescott, 1977

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    • cites Sebastian, Viding, Williams & Blakemore, 2010

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    • cites Steinberg, 2008

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    Premisecitation

    Adolescents report high levels of sensation-seeking relative to children and adults, peaking in early-to-mid adolescence (roughly ages 12-15) and declining thereafter.

    “Steinberg and colleagues recently demonstrated that adolescents report high levels of sensation-seeking relative to children and adults. This tendency appeared to peak in early-to- mid adolescence (roughly between the ages of 12–15) and declined thereafter, as evidenced by a large-scale cross-sectional study of over 900 individuals who ranged in age from 10 to 30 years of age (Steinberg et al., 2”
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    Premisecitation

    Structural plasticity in the NAcc has been hypothesized to account for drug sensitization effects in psychostimulant-exposed individuals given that medium spiny neuron density increases after repeated cocaine ingestions.

    “Structural plasticity in the NAcc has been hypothesized to account for drug sensitization effects in psychostimulant-exposed individuals given that medium spiny neuron density increases after repeated cocaine ingestions (Robinson & Kolb, 2004).”
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    Premisecitation

    A single sexual encounter in a sexually naïve female activates NAcc neurons and sexual behavior increases c-Fos expression in the NAcc core, but not the shell.

    “A single sexual encounter in a sexually naïve female activates NAcc neurons (Meisel, Camp & Robinson, 1993; Joppa, Meisel & Gardner, 1995; Kohlert & Meisel, 1999) and sexual behavior increases c-Fos expression in the NAcc core, but not the shell (Bradley & Meisel, 2001).”
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    • cites Meisel, Camp & Robinson, 1993

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    • cites Joppa, Meisel & Gardner, 1995

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    Premisecitation

    DA cell bodies are abundant in midbrain regions (VTA, SN) and project to mesostriatal, mesolimbic, and mesocortical systems.

    “Thus, while DA cell bodies are abundant in midbrain regions (ventral tegmental area, VTA; substantia nigra, SN), they project to adjacent midbrain and striatal sites (mesostriatal system), to structures historically defined as core to the limbic system (mesolimbic system), and to the cortex (mesocortical system) (Bjorklund & Dunnett, 2007).”
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    Premisecitation

    Estradiol administration in adult females decreases synaptic density in medium spiny neurons of the NAcc core and alters the morphology of spines in that region.

    “Estradiol administrations in adult females decreases synaptic density in medium spiny neurons of the NAcc core and alter the morphology of spines in that region.”
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    • cites Staffend, Loftus, & Meisel, 2011

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    Premisecitation

    When depolarized, dopamine cells display two firing rates: tonic single-spike firing (2-10 Hz) and phasic bursts of 2-6 action potentials (15-30 Hz).

    “When depolarized, dopamine cells display two firing rates. One is represented by single-spike firing (in the 2–10 Hz frequency, termed “tonic”); the other is characterized by bursts of 2–6 action potentials (in the 15–30 Hz frequency; “phasic”) (Grace and Bunney, 1984 a, b; Wanat, Willuhn, Clark & Phillips, 2009).”
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    • cites Grace and Bunney, 1984 a, b

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    • cites Wanat, Willuhn, Clark & Phillips, 2009

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    Premisecitation

    Synaptogenesis is maximal in early childhood throughout the cortex with a gradual pruning of synapses during late childhood and adolescence.

    “Synaptogenesis is maximal in early childhood throughout the cortex with a gradual pruning of synapses during the late childhood and adolescent periods (Bourgeois, Goldman-Rakic, & Rakic, 1994; Gogtay et al., 2004).”
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    Premisenone given

    Phasic firing is rapid and transient, results in DA concentrations of as much as 1 mM, and acts locally within the synaptic cleft.

    “Phasic firing is rapid and transient, and results in DA concentrations of as much as 1 mM. It leads to high amplitude release of DA into neural synapses and, like extracellular DA from tonic release, is regulated by reuptake mechanisms as well as catabolic enzymes. The net result is that phasic DA acts locally within the synaptic cleft.”
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    Premisecitation

    The pruning process, inferred from age-related changes in gray matter volumes and cortical thickness, appears regionally variant and unfolds in a posterior-to-anterior gradient.

    “The pruning process, inferred from age-related changes in gray matter volumes and cortical thickness, appears to be regionally variant and unfolds in a posterior-to-anterior gradient (Gogtay et al., 2004).”
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    Premisecitation

    The tonic mode is low in amplitude and steady, underpins basal DA neuron firing patterns, and results in extracellular DA concentrations ranging from 5 to 20 nM.

    “The tonic mode is lowin amplitude and steady, and underpins basal DA neuron firing patterns, resulting in extracellular DA concentrations ranging from 5 to 20 nM.”
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    Premisecitation

    Dopamine has both neurotransmitter and neuromodulatory effects.

    “Dopamine (DA) has both neurotransmitter and neuromodulatory effects.”
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    • cites Kazmarek & Levitan, 1987

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    Premisecitation

    Studies of adolescent brain development focus on declines in gray matter volume throughout the cortex, taken as an index of synaptic pruning, on increases in white matter volume, and on connectivity patterns between regions.

    “Studies of adolescent brain development focus on declines in gray matter volume throughout the cortex, which is taken as an index of synaptic pruning (Giedd, Clasen, Lenroot, Greenstein, Wallace, et al., 2006; Gogtay, Giedd, Lusk, Hayashi, Greenstein et al., 2004), on increases in white matter volume (Schmithorst & Yan, 2010), and on connectivity patterns between regions (Asato, Terwilliger, Wu &”
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    Premisecitation

    Tonic activity has been conceptualized as inhibitory to phasic signals, though it has also been suggested that phasic signals potentiate tonic levels.

    “Tonic activity has been conceptualized as inhibitory to phasic signals (Goto et al. 2007), though it has also been suggested that phasic signals potentiate tonic levels (Niv, Joel & Dayan, 2006).”
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    Premisecitation

    Schultz (2000) demonstrated that phasic DA activity increases in the context of unexpected rewards and in response to reward during initial phases of instrumental reward learning, and that tonic DA levels transiently decline when anticipated rewards are not delivered or when animals encounter aversive stimuli.

    “Schultz (2000) demonstrated that phasic DA activity increases in the context of unexpected rewards and in response to reward during initial phases of instrumental reward learning, and that tonic DA levels transiently decline when anticipated rewards are not delivered or when animals encounter aversive stimuli.”
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    • cites Schultz (2000)

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    Interpretationcitation

    Experience can alter synaptic structure, strength of responding, and neurochemistry in the NAcc.

    “While this particular example highlights a pathological process, it similarly illustrates the manner in which experience can alter synaptic structure, strength of responding, and neurochemistry in this region.”
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    Premisecitation

    DA acts on D1-like and D2-like receptors found presynaptically on the spines of projection neurons and postsynaptically on the heads of dendritic spines contacted by glutamatergic terminals.

    “DA acts on D1-like and D2-like receptors (Beaulieu & Gainetdinov, 2011) found presynaptically on the spines of projection neurons (Caille, Durmartin & Bloch, 1996; Hersch, Ciliax, Gutekunst, Rees, Heilman, Yung, et al., 1995) and postsynaptically on the heads of dendritic spines contacted by glutamatergic terminals (Levey, Hersch, Rye, Sunahara, Niznik, Kitt, et al., 1983).”
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    • cites Caille, Durmartin & Bloch, 1996

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    • cites Hersch et al., 1995

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    Premisecitation

    Phasic activity is triggered by environmentally salient events and, within the striatal region, is dependent on glutamatergic excitatory input to DA neurons.

    “Phasic activity is triggered by environmentally salient events (see Schulz, 2000, Willuhn, Wanat, Clark & Phillips, 2010 and Wanat et al. 2009 for reviews) and, within the striatal region, is dependent on glutaminergic excitatory input to DA neurons from sources such as the pontine tegmentum, ventral pallidum, and subthalamic nucleus.”
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    • cites Willuhn, Wanat, Clark & Phillips, 2010

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    • cites Wanat et al. 2009

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    Premisecitation

    The VTA-to-NAcc (mesoaccumbens) projection is particularly relevant to incentive-reward motivation because the NAcc is a core node for behavioral activation; it has been estimated that 75% of this projection is dopaminergic.

    “The VTA-to-NAcc (mesoaccumbens) projection is particularly relevant to this review given that the latter structure represents a core node for behavioral activation associated with incentive-reward motivation; it has been estimated that 75% of this projection is dopaminergic (Swanson, 1982).”
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    Premisecitation

    Teicher et al. (1995) found strong evidence that both D−1 and D−2 receptors are overproduced then pruned during early adolescence in the corpus striatum (nigrostriatal system) but little evidence for receptor pruning in the nucleus accumbens during the same period.

    “They found strong evidence that both D−1 and D−2 receptors are overproduced then pruned during early adolescence in the corpus striatam (nigrostriatal system) but little evidence for receptor pruning in the nucleus accumbens during the same period.”
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    • cites Teicher, Andersen & Hostetter (1995)

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    Interpretationcitation

    These reward experiences drive both incentive-reward learning and phasic DA responding, and sufficiently potent learning experiences may lead to further alterations in tonic DA levels as bouts of phasic DA responses accumulate.

    “These experiences would then drive both incentive-reward learning and phasic DA responding, and sufficiently potent learning experiences may lead to further alterations in tonic DA levels as bouts of phasic DA responses accumulate (Niv, 2007).”
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    • cites Niv, 2007

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    Interpretationreasoning

    Tonic DA signals code individual differences in incentive motivation, propelling individuals at sufficient levels to engage rewarding experiences.

    “Thus, tonic DA signals code individual differences in incentive motivation, propelling individuals at sufficient levels to engage rewarding experiences.”
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    Premisecitation

    D1 and D2 densities peak in subcortical structures such as the striatum and NAcc in late childhood to early adolescence, as do the densities of D2-like D3 and D4 receptors.

    “D1 and D2 densities peak in subcortical structures such as the striatum and NAcc in late childhood to early adolescence, as do the densities of D2-like D3 and D4 receptors (Andersen, Thompson, Krenzel & Teicher, 2002; Tarazi, Tomasini, & Baldessarini, 1998b).”
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    • cites Andersen, Thompson, Krenzel & Teicher, 2002

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    • cites Tarazi, Tomasini, & Baldessarini, 1998b

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    Interpretationreasoning

    As phasic DA signaling becomes more reliable with advancing age and as the prefrontal cortex achieves its full maturational potential, the organism can maximally benefit from this informational stream in making decisions in potentially risky contexts.

    “As phasic DA signaling becomes more reliable with advancing age (Robinson, Zitzman, Smith, & Spear, 2011) and as the prefrontal cortex achieves its full maturational potential, the organism can maximally benefit from this informational stream in making decisions in potentially risky contexts.”
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    • cites Robinson, Zitzman, Smith, & Spear, 2011

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    Interpretationreasoning

    Elevated tonic DA levels promote incentive motivation and response vigor, directing action in contexts where initial cues for reward learning experiences are ambiguous or absent, a context that may characterize early adolescence.

    “These models may be integrated through a proposed developmental cascade through which elevated tonic DA levels that promote incentive motivation and response vigor serve to direct action in contexts where initial cues for reward learning experiences are ambiguous or simply absent. This context may characterize early adolescence.”
    Quote in the paperSubstantial claim

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    Premisecitation

    Tonic release has bidirectional effects on VTA-prefrontal inputs through D2 receptors: increases attenuate PFC afferents while decreases facilitate them, perhaps enabling switches to new response strategies when current responses fail to yield anticipated rewards.

    “Tonic release has bidirectional effects on VTA-prefrontal inputs through the action of D2 receptors. Increases attenuate the activity of PFC afferents while decreases facilitate them, perhaps enabling switches to new response strategies when current responses fail to yield anticipated rewards (Goto & Grace, 2005).”
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    Premisecitation

    These signals permit an accurate calculation of expected value to be achieved during learning, allowing an organism to make probabilistic judgments about potential outcomes during decision-making.

    “These signals permit an accurate calculation of expected value to be achieved during learning, allowing an organism to make probabilistic judgments about potential outcomes during decision-making (Schulz, 2000; Tobler et al. 2007).”
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    • cites Schulz, 2000

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    Premisecitation

    Non-contingent systemic administrations of drugs of abuse (nicotine, alcohol, cannabinoids, opiates, amphetamine and cocaine) consistently increase extracellular tonic levels of DA in the NAcc, while drugs with low abuse potential do not.

    “For instance, non-contingent systemic administrations of drugs of abuse (nicotine, alcohol, cannabinoids, opiates, amphetamine and cocaine) consistently increase extracellular tonic levels of DA in the NAcc, while drugs with low abuse potential do not (Wanat et al., 2009).”
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    Premisecitation

    Willuhn et al. (2010) suggest that different time scales of dopamine transmission may have different functions: distinct aspects of phasic signaling may relate to reinforcement learning and approach behavior, while tonic signaling enables motivational and motor systems but not reinforcement learning.

    “Willuhn et al. (2010) suggest that different time scales of dopamine transmission may have different functions. Distinct aspects of phasic signaling may relate to both reinforcement learning and approach behavior, while tonic signaling enables motivational and motor systems but not reinforcement learning.”
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    Premisecitation

    There is an optimal level of activity at which DA energizes behavior; an inverted-U-shaped performance function has been proposed to characterize individual differences in DA mediation of reward-based learning.

    “Importantly, there is an optimal level of activity at which DA energizes behavior. An inverted-U-shaped performance function (Yerkes & Dodson, 1908) has been proposed to characterize individual differences in DA mediation of reward-based learning (Cohen, Krohn-Grimberghe, Elger, & Weber 2007).”
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    Premisecitation

    The medial orbitofrontal region is among the last cortical brain regions to reach full synaptic maturity but is in receipt of outcome-related signals from the striatum during reward learning.

    “The medial orbitofrontal region, for instance, is among the last cortical brain regions to reach full synaptic maturity (Gogtay et al. 2004) but is in receipt of outcome-related signals from the striatum during reward learning (Tobler, O’Doherty, Dolan & Schulz, 2007).”
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    • cites Tobler, O’Doherty, Dolan & Schulz, 2007

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    Interpretationcitation

    Receptor stimulation by tonic DA activity may index the individual's ongoing incentive-motivational disposition, whereas phasic signals primarily influence encoding of stimulus and response reward associations by modulating synaptic plasticity.

    “Overall, then, receptor stimulation by tonic DA activity may index the individual’s ongoing incentive-motivational disposition (Willuhn et al. 2010; Niv, 2007) whereas phasic signals primarily influence encoding of stimulus and response reward associations by modulating synaptic plasticity in response to naturally occurring rewards, novel events, and reward learning experiences.”
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    Interpretationreasoning

    Higher levels of incentive-motivation (accompanying higher levels of tonic DA) energize exploratory and approach behaviors that bring the individual into contact with reinforcing experiences of reward acquisition, each with specific stimulus and response associations.

    “By definition, higher levels of incentive-motivation (accompanying higher levels of tonic DA) energize exploratory and approach behaviors that bring the individual into contact with reinforcing experiences of reward acquisition, each of which has specific stimulus and response associations.”
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    Premisecitation

    Primate and rodent research generally indicates the most extensive changes in DA transmission during the prenatal period into early childhood, with more subtle but measurable changes in adolescence and declines in DA functional activity thereafter.

    “Primate and rodent research generally indicates the most extensive changes in DA transmission during the prenatal period into early childhood, as full synaptic capacity develops. There appear to be more subtle but measurable changes in adolescence and declines in DA functional activity thereafter.”
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    Premisecitation

    DA receptor density declines from adolescence to adulthood by 35-50%, depending on region, and this decline is accompanied by dramatic changes in DA basal activity.

    “The decline in receptor density from adolescence to adulthood is in the range of 35–50%, depending on region, and is accompanied by dramatic changes in DA basal activity (Andersen et al. 2002).”
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    • cites Andersen et al. 2002

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    Interpretationcitation

    The pattern of greater amygdala activation to negative feedback in adults than adolescents suggests less sensitivity to punishment for adolescents.

    “suggesting less sensitivity to punishment for adolescents”
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    Premisecitation

    Robinson et al. (2011) found that early adolescent rats have a baseline rate of DA fluctuation similar to adult rats but an unreliable coupling of phasic DA responses to novel stimuli and a non-habituating phasic DA responsivity to repeated brief social interactions, unlike adult rats.

    “Robinson et al. (2011), who studied phasic DA fluctuations in early adolescent rats and reported a baseline rate of fluctuation similar to adult rats but an unreliable coupling of phasic DA responses to novel stimuli, along with a non-habituating phasic DA responsivity to repeated brief social interactions with other rats (unlike adult rats).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Robinson et al. (2011)

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Both D1 and D2 densities are heightened during adolescence relative to adulthood, a pattern that characterizes both the cortex and subcortical regions.

    “Both D1 and D2 densities are heightened during adolescence relative to adulthood, a pattern that characterizes both the cortex and subcortical regions (Lidow & Rakic, 1992; Seeman, Bzowej, Guan, Bergeron, Becker, &”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Lidow & Rakic, 1992

      Not checked in the free run.

    • cites Seeman, Bzowej, Guan, Bergeron, Becker, &

      Not checked in the free run.

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

    Premisenone given

    Analytic strategies vary from whole-brain analysis to a priori region-of-interest approaches with variation in the stringency of applied statistical thresholds.

    “Analytic strategies similarly vary from whole-brain analysis to a priori region-of-interest approaches with variation in the stringency of applied statistical thresholds.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation

    Bjork et al. (2004; 2010) used a measure explicitly designed to elicit incentive motivation and failed to find significant age differences.

    “The strongest contrary evidence comes from Bjork et al. (2004; 2010), who used a measure explicitly designed to elicit incentive motivation and failed to find significant age differences.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Bjork et al. (2004; 2010)

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Interpretationreasoning

    The conditions that elicit reliable region-specific elevations in activation for adolescents remain to be clarified.

    “although the conditions that elicit reliable region-specific elevations in activation for adolescents remain to be clarified.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    There was an adolescent-specific peak in activation in a VMPFC/subcallosal region during the decision phase and in the ventral striatum/caudate during the outcome phase.

    “there was an adolescent-specific peak in activation in a VMPFC/subcallosal region during the decision phase of the task and in the ventral striatum/caudate during the outcome phase.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites van Leijenhorst, Gunther Moor, et al. (2010)

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    Under conditions that elicit particularly strong incentive-motivation in adolescents, such as peer interaction, adolescents may exhibit stronger neural responses to both reward anticipation and reward delivery and may show heightened ventral striatal responses.

    “under conditions that elicit particularly strong incentive-motivation in adolescents, i.e., peer interaction, adolescents may exhibit stronger neural responses to both reward anticipation (also concordant with Geier, Terwilliger, Teslovich, Velanova, & Luna, 2010) and reward delivery and may show heightened ventral striatal responses.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Geier et al., 2010

      Not checked in the free run.

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

    Interpretationnone given

    Individual differences in mesoaccumbens dopamine transmission predict the specific outcomes of normative adolescent elevations in incentive-motivation and associated behavioral activation, as well as the eventual adult phenotypes.

    “individual differences in mesoaccumbens dopamine transmission predict the specific outcomes of normative adolescent elevations in incentive-motivation and associated behavioral activation, as well as the eventual adult phenotypes.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation

    Individuals with relatively low levels of basal DA synthesis showed relatively poorer reversal learning from unexpected rewards relative to punishments, but improved their performance significantly following administration of a D2 receptor agonist.

    “individuals with relatively low levels of basal DA synthesis showed relatively poorer reversal learning from unexpected rewards relative to punishments, but improved their performance significantly following administration of the D−2 receptor agonist.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Cools et al. (2009)

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S4 (based). May combine two claims.

    Interpretationnone given

    Various aspects of DA neurotransmission are under both genetic and environmental influence and thus capable of forming a foundation for individual differences, as well as normative trends, in levels of incentive-reward motivation and associated behavioral activation.

    “various aspects of DA neurotransmission are under both genetic and environmental influence and thus capable of forming a foundation for individual differences, as well as normative trends, in levels of incentive-reward motivation and associated behavioral activation.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S4 (based). May combine two claims.

    Interpretationnone given

    Incentive-reward motivational systems show a period of elevated activity between childhood and adolescence and a decline from adolescence into young adulthood.

    “incentive-reward motivational systems show a period of elevated activity between childhood and adolescence and a decline from adolescence into young adulthood.”
    Quote in the paperNot a substantial claim

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

    Interpretationreasoning

    Adolescent-limited elevations in mesoaccumbens DA transmission would be predicted to differentially affect individuals depending on their baseline pre-adolescent levels.

    “adolescent-limited elevations in mesoaccumbens DA transmission would be predicted to differentially affect individuals, depending on their baseline pre-adolescent levels”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationcitation

    High baseline DA synthesis individuals were more impaired by administration of a D2 receptor agonist, supporting the hypothesis that induction of significantly increased activity in an already high functioning DA system results in an overdose behavioral reaction.

    “These individuals were also more impaired by the administration of a D−2 receptor agonist, supporting the hypothesis that induction of significantly increased activity in an already high functioning DA system results in an “overdose” behavioral reaction”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Cools et al. (2009)

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Hammerer et al. (2010) found that adolescents and young adults were superior to children or elderly adults in their differential classification of task-related outcomes, needed fewer trials to learn from choice outcomes, and learned more from gains than losses.

    “Hammerer et al. (2010) examined the feedback-related negativity component of the ERP during probabilistic learning and found that adolescents and young adults were superior to children or elderly adults in their differential classification of task-related outcomes, that they needed fewer trials to learn from choice outcomes, and that they learned more from gains than losses.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Hammerer et al. (2010)

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S2 (checkable), S4 (based).

    Interpretationreasoning

    Adolescent changes in tonic neuromodulatory activity dopamine within mesostriatal projections may represent a central mechanism that should be further investigated to understand both the nonlinear developmental trend and the individual difference factors that interact with it.

    “adolescent changes in tonic neuromodulatory activity dopamine within mesostriatal projections may represent a central mechanism that should be further investigated to understand both this nonlinear developmental trend and the individual difference factors that interact with it.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationreasoning

    For those entering adolescence with high levels of basal activity, further increases may predispose them toward excessively risky situations, repeated drug and alcohol use, inability to maintain focus in an achievement context, and complaints of chronic boredom.

    “For those entering adolescence with high levels of basal activity, further increases may predispose them toward behavioral engagements with excessively risky situations, repeated drug and alcohol use, inability to maintain focus in an achievement context, and complaints of chronic boredom.”
    Quote in the paperNot a substantial claim

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

    Interpretationnone given

    The mechanisms that underlie the acceleration and subsequent decline of incentive-reward motivational systems are unknown.

    “The mechanisms that underlie this acceleration and subsequent decline are unknown.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationreasoning

    For individuals with low levels of basal mesoaccumbens DA activity, increases during adolescence will increase their absolute levels of incentive-reward motivation and behavioral activation but still place them at relatively lower levels than their peers, resulting in less reward seeking and more limited exploration.

    “For individuals with low levels of basal mesoaccumbens DA activity, increases during the adolescent period will increase their absolute levels of incentive-reward motivation and behavioral activation but still place them at relatively lower levels than their peers, resulting in less reward seeking and more limited exploration”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based). May combine two claims.

    Premisenone given

    Tonic DA levels may be more readily associated with response vigor during effortful behavior and with individual differences in responding to tradeoffs between level of response effort and magnitude of reward.

    “tonic DA levels may be more readily associated with response vigor during effortful behavior, as well as individual differences in responding to tradeoffs between level of response effort and magnitude of reward.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based).

    Interpretationnone given

    Within the animal research literature, the primary mechanisms within the mesoaccumbens dopamine system that may induce adolescent effects are unclear.

    “within the animal research literature the primary mechanisms within the mesoaccumbens dopamine system that may induce these adolescent effects are unclear.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation

    DA synthesis capacity impacts learning rates as well as the behavioral effects of D2 receptor stimulation.

    “it was demonstrated that DA synthesis capacity impacts learning rates as well as the behavioral effects of D2 receptor stimulation.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Cools et al. (2009)

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based).

    Premisenone given

    Phasic signaling is inferred through prediction error as quantified in probabilistic learning paradigms.

    “phasic signaling is inferred through prediction error as quantified in probabilistic learning paradigms”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S2 (checkable), S4 (based).

    Premisenone given

    Few researchers have investigated the potential uniqueness of the adolescent period in terms of the mechanisms that underlie the time-limited heightening of incentive-reward motivation and behavioral activation during adolescence.

    “Few researchers have investigated the potential uniqueness of the adolescent period in terms of the mechanisms that underlie the time-limited heightening of incentive-reward motivation and behavioral activation during adolescence”
    Quote in the paperNot a substantial claim

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

    Interpretationreasoning

    Changes in autoreceptor and transporter function merit particular scrutiny given their roles in regulating extracellular DA.

    “changes in autoreceptor and transporter function merit particular scrutiny given their roles in regulating extracellular DA.”
    Quote in the paperNot a substantial claim

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

    Premisecitation

    Systemic pharmacological agents can carry risks and side effects and can modify both tonic and phasic signaling.

    “systemic pharmacological agents can carry risks and side effects, and also can modify both tonic and phasic signaling (Willuhn et al. 2010).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Willuhn et al. 2010

      Not checked in the free run.

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

    Interpretationnone given

    A comprehensive evaluation of both animal and human research literature clearly indicates a central role for dopamine, in concert with glutaminergic and gabaergic systems, in modulating levels of incentive-reward motivation.

    “Our view is that a comprehensive evaluation of both animal and human research literature clearly indicates a central role for dopamine, in concert with glutaminergic and gabaergic systems, in modulating levels of incentive-reward motivation.”
    Quote in the paperNot a substantial claim
64 of 64

  • The paper relies on this without support.

    Findings from animal models of adolescent dopamine transmission are informative about human adolescent dopamine function.

    “Animal data supports the notion that various aspects of DA transmission change in the course of the mammalian lifespan from childhood to adolescence (see Table 1).”
    “Both primates and rodents exhibit alterations in substrates of DA signaling during adolescence.”

  • The paper relies on this without support.

    Many healthy typically developing teens do not demonstrate unusually strong motivational drives and impulsive response tendencies.

    “many healthy typically developing teens do not apparently demonstrate unusually strong motivational drives and impulsive response tendencies.”

  • The paper relies on this without support.

    Findings from animal research about mesoaccumbens dopamine system activity during adolescence can be generalized to humans.

    “this association has relied nearly exclusively on animal research.”
3 of 3

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?

  • These neurobiological changes underlie profound maturation in motivational and cognitive domains across adolescence.

    “These neurobiological changes underlie the profound maturation in motivational and cognitive domains across adolescence [30–34]”

    From Adolescent nicotine exposure and persistent neurocircuitry changes: unveiling lifelong psychiatric risks (2025) · cites this paper as [31]

    The Neurobiological Foundation and Concluding Comments link adolescent neural and dopamine changes to the development of incentive motivation. The Concluding Comments also describe a developing cognitive-behavioral control system, but treat dopamine’s role as a proposed mechanism and do not establish that the described changes underlie broad cognitive maturation. (LLM, conf=0.83)

    Experimental — accuracy not yet measured

  • Incentive motivation declines from adolescence into adulthood.

    “An accumulation of evidence suggests an increase in incentive motivation from childhood to adolescence and a decline from adolescence into adulthood (Luciana, Wahlstrom, Porter, & Collins, 2012; Steinberg, 2010).”

    From Incentive Motivation, Cognitive Control, and the Adolescent Brain: Is It Time for a Paradigm Shift? (2012) · cites this paper as Luciana, Wahlstrom, Porter, & Collins, 2012

  • Incentive motivation increases from childhood to adolescence.

    “An accumulation of evidence suggests an increase in incentive motivation from childhood to adolescence and a decline from adolescence into adulthood (Luciana, Wahlstrom, Porter, & Collins, 2012; Steinberg, 2010).”

    From Incentive Motivation, Cognitive Control, and the Adolescent Brain: Is It Time for a Paradigm Shift? (2012) · cites this paper as Luciana, Wahlstrom, Porter, & Collins, 2012

  • Adolescents with higher levels of tonic DA levels, higher DA receptor densities, and lower rates of DA clearance and degradation may engage in DA-modulated behaviors (e.g. sensation/novelty seeking) to a larger extent than adolescents with decreased DA signaling and availability.

    “For example, adolescents with higher levels of tonic DA levels, higher DA receptor densities, and lower rates of DA clearance and degradation may engage in DA-modulated behaviors (e.g. sensation/novelty seeking) to a larger extent than adolescents with decreased DA signaling and availability (For review see (Luciana, Wahlstrom et al. 2012)).”

    From Developmental imaging genetics: Linking dopamine function to adolescent behavior (2014) · cites this paper as Luciana, Wahlstrom et al. 2012

  • A U-shaped trajectory also characterizes hormonal levels in striatal regions, with an adolescent peak in the transmission of dopaminergic signals that facilitate incentive motivation.

    “Notably, a U-shaped trajectory also characterizes hormonal levels in striatal regions, with an adolescent peak in the transmission of dopaminergic signals that facilitate incentive motivation (Luciana et al., 2012).”

    From Gaining insight into adolescent vulnerability for social anxiety from developmental cognitive neuroscience (2014) · cites this paper as Luciana et al., 2012

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.

  • Bjork studies are said to show no age differences despite reported NAcc differences

    Minor

    The summary says the Bjork studies failed to find significant age differences, but the paper earlier reports reduced adolescent NAcc activation in both the 2004 and 2010 studies. The earlier statement that performance did not differ does not resolve this contradiction about neural activation.

1 of 1

Cites

Flagged first, then by citations

Research works printed but not linked: 2

  1. Depue RA Collins PF Luciana M Lenzenweger MF 1996 A model of neurobiology–environment interaction in developmental psychopathology Frontiers of developmental psychopathology 44 77 New York Oxford University Press
  2. Tellegen A Waller NG Briggs S Cheek J 1997 Exploring personality through test construction: Development of the multidimensional personality questionnaire Personality measures: Development and evaluation 1 JAI Press

Cited by

Sorted by citations

Related

Authors
Luciana, M., Wahlstrom, D., Porter, J. N., & Collins, P. F.
Affiliations
University of Minnesota (US)
ORCID
Venue
Developmental Psychology
Publisher
American Psychological Association (APA)
Published
2012
Volume
48
Issue
3
Pages
844-861
ISSN
  • 0012-1649 (ISSN-L)
  • 1939-0599
DOI
10.1037/a0027432
PMC
PMC3341492
OpenAlex
W2042170867
Cited by
156
References
176
Citations by year
2026: 6 · 2025: 10 · 2024: 5 · 2023: 22 · 2022: 15 · 2021: 10 · 2020: 7 · 2019: 7 · 2018: 4 · 2017: 9 · 2016: 15 · 2015: 15 · 2014: 16 · 2013: 13 · 2012: 2
FWCI
6.01
Type
journal article
Language
en
Open access
Locations
  • Developmental Psychology (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • National Institute on Drug Abuse (DA017843)
  • National Institute of Mental Health (MH017069)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
  • Health Sciences › Medicine › Psychiatry and Mental health › Schizophrenia research and treatment
Keywords
dopamine, incentive motivation, reward motivation, adolescence, self-regulation, individual differences, reward learning, behavioral activation, age-related changes
MeSH terms
Adolescent, Adolescent Behavior, Aging, Dopamine, Humans, Individuality, Motivation, Nucleus Accumbens, Social Control, Informal, Signal Transduction

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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.

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