Cited by 174Neural and Behavioral Psychology StudiesNeurotransmitter Receptor Influence on BehaviorFunctional Brain Connectivity Studies

A systematic review of fMRI reward paradigms used in studies of adolescents vs. adults: The impact of task design and implications for understanding neurodevelopment

Open access
Richards, Jessica M., Plate, Rista C., Ernst, Monique·2013·Neuroscience & Biobehavioral Reviews

Abstract

The neural systems underlying reward-related behaviors across development have recently generated a great amount of interest. Yet, the neurodevelopmental literature on reward processing is marked by inconsistencies due to the heterogeneity of the reward paradigms used, the complexity of the behaviors being studied, and the developing brain itself as a moving target. The present review will examine task design as one source of variability across findings by compiling this literature along three dimensions: (1) task structures, (2) cognitive processes, and (3) neural systems. We start with the presentation of a heuristic neural systems model, the Triadic Model, as a way to provide a theoretical framework for the neuroscience research on motivated behaviors. We then discuss the principles guiding reward task development. Finally, we review the extant developmental neuroimaging literature on reward-related processing, organized by reward task type. We hope that this approach will help to clarify the literature on the functional neurodevelopment of reward-related neural systems, and to identify the role of the experimental parameters that significantly influence these findings.

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Crossref · 10.1016/j.neubiorev.2013.03.004

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Claims the paper makes

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  • Findingnone given

    Instrumental-reward tasks do not appear to modulate amygdala or insula differentially as a function of age.

    “these instrumental-reward tasks do not seem to modulate amygdala or insula differentially as a function of age.”
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  • Findingcitation

    During test preparation in tasks requiring inhibitory responses, internally generated action, or a manual response, striatal activation during reward trials was greater in adolescents than adults.

    “during test preparation in tasks requiring inhibitory responses/internally generated action (e.g., antisaccade as in Geier et al., 2009b), or a manual response (e.g., Somerville et al., 2010), striatal activation during reward trials was greater in adolescents than in adults.”
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    • cites Somerville et al., 2010 source

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  • Findingcitation

    When the action consists of a time-sensitive response, adolescents activate striatum less than adults.

    “However, when the action consists of time-sensitive response, adolescents activate striatum less than adults (Bjork et al., 2004; Bjork et al., 2010).”
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  • Findingcitation

    During the actual cognitive or motor stage, prefrontal cortical regions including inferior frontal gyrus and dorsolateral prefrontal cortex were more active in youths than adults on non-rewarded trials.

    “During the actual cognitive/motor stage, prefrontal cortical regions (IFG and DLPFC) were more active in youths than in adults on non-rewarded trials (Somerville and Casey, 2010; Van Leijenhorst et al., 2006).”
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  • Findingcitation

    Discrepancies emerged when pubertal status was examined.

    “However, here again, discrepancies emerged when pubertal status was examined (Forbes et al., 2010b).”
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    • cites Forbes et al., 2010b

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    Findingreasoning

    Age did not modulate DLPFC activation in the Cake Gambling task, suggesting DLPFC was not critical to the test.

    “As noted below, age did not modulate activation of DLPFC in this task, suggesting that the DLPFC, notable for its prolonged maturation (Gogtay et al., 2004; Paus, 2005), was not critical to the test.”
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    Findingcitation

    The reward module, comprising striatum and orbitofrontal cortex, showed no age differences in response to evocative faces or during anticipation of passively received probabilistic reward.

    “The reward module (striatum and OFC), on the other hand, showed no age differences in response to evocative faces (regardless of valence) or in anticipation of passively receiving a probabilistic reward.”
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    Findingcitation

    In the feedback stage of passive probabilistic reward tasks, striatal activation to reward receipt was greater in adolescents than in children or adults, while orbitofrontal activation to non-reward receipt was greater in adults than in adolescents.

    “striatal activation was greater in adolescents than in children or adults in response to reward receipt, but OFC activation was greater in adults than in adolescents in response to non-reward receipt.”
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    Findingreasoning

    Discrepant findings in orbitofrontal and medial prefrontal cortex emerged, including greater adult activation in risky versus non-risky decisions and greater adolescent activation in more social and less costly decisions.

    “However, discrepant findings in OFC and mPFC (e.g., greater activation in adults than adolescents in risky vs. non-risky decisions, and greater activation in adolescents than in adults in more social and less costly decisions) did emerge.”
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    Findingcitation

    During the feedback stage, favorable outcomes were associated with greater striatal activation in adolescents than adults, but greater amygdala activation in adults than adolescents.

    “During the feedback stage, favorable outcomes were associated with greater striatal activation in adolescents than adults, but greater activation in the amygdala in adults than adolescents.”
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    Findingcitation

    Taken together, instrumental-reward studies showed lower striatal activation in adolescents during the cue stage in one task and during the test preparation stage of another task.

    “these instrumental-reward studies showed that striatal activation was lower in adolescents during the cue stage in one task (Bjork et al., 2004; Bjork et al., 2010; Geier et al., 2009b), and during the test preparation stage of another task (Bjork et al., 2004; Bjork et al., 2010; Cho et al., 2012).”
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    • cites Geier et al., 2009b

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    Findingreasoning

    In summary, during the cue stage adolescents activate striatum less than adults, but during test preparation for inhibitory action or learning retrieval they activate striatum more than adults, particularly on reward trials.

    “during the cue stage of the trial, adolescents activate the striatum less than adults, but during the test preparation stage (i.e., preparation for inhibitory action, or learning-retrieval), adolescents activate striatum more than adults, particularly in reward-trials.”
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    Findingcitation

    During positive feedback, stronger striatal activation emerged in adolescents compared with adults, and during negative feedback, weaker orbitofrontal activation emerged in adolescents compared with adults.

    “during positive feedback stage, stronger striatal activation (Cohen et al., 2010), and during negative feedback, weaker OFC activation (Van Leijenhorst et al., 2006), emerged in adolescents compared to adults.”
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    Findingown data

    Across all reward-related tasks, the review found mixed results, and task type alone does not explain them.

    “Overall, findings across all the reward-related tasks reveal mixed results that cannot be attributed solely to the type of task.”
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    Premisecitation

    The avoidance module comprises amygdala, hippocampus, and insula, which consistently respond to aversive stimuli.

    “This module is comprised of the amygdala, hippocampus, and insula, which consistently respond to aversive stimuli (Hardin et al., 2009b; Rauch et al., 2003).”
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    Premisecitation

    The triadic model organizes motivated behavior along three interacting dimensions: approach, avoidance, and control.

    “The triadic model considers behavior along three interacting dimensions: approach, avoidance and control.”
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    • cites Ernst and Fudge, 2009

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    Premisenone given

    The control module refers to regulatory processes that modulate subcortical function through top-down cognitive control.

    “The control module refers to regulatory processes that modulate subcortical function, (i.e., the approach and the avoidance systems), through “top-down” cognitive control.”
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    Premisecitation

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

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

    The triadic model was selected over dual-systems models because it may allow greater latitude in interpreting inconsistent findings by modulating three rather than two systems.

    “However, to ground our work, we selected the triadic neural systems model (Ernst and Fudge, 2009) over a dual neural systems model (e.g., Casey et al., 2008), because it may offer greater latitude in interpreting inconsistent findings, as it allows the modulation of three rather than two systems to accommodate various and complex situations.”
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    • cites Casey et al., 2008 source

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    Premisecitation

    There is a relative dearth of research on avoidance behavior in incentive contexts; available evidence maps onto a quadratic function indicating a dip in avoidance response during adolescence when reward is possible.

    “There is a relative dearth of research examining avoidance behavior in the context of incentives; however, the available evidence seems to map onto a quadratic function indicating a dip in avoidance response during adolescence when there is some probability of reward (Ernst et al., 2011).”
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    • cites Ernst et al., 2011 source

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    Premisereasoning

    The dual-systems developmental model focuses on a less efficient control system that fails to optimally regulate an overreactive emotional/motivational system in adolescence relative to adults.

    “The developmental dynamics of this dual-systems model focus on a less efficient control system that does not optimally regulate an overreactive emotional/motivational system in adolescence relative to adults.”
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    Premisereasoning

    In dual-systems models, the cognitive regulatory system is supported by prefrontal cortex exerting top-down influence on subcortical regions, and the emotional/motivational system is driven by subcortical structures including striatum and amygdala.

    “The cognitive regulatory system is supported by the prefrontal cortex which exerts top-down influences on subcortical regions, and the emotional/motivational system is driven by subcortical structures, mainly including the striatum and less centrally the amygdala.”
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    Premisecitation

    Resolving inconsistencies in the developmental reward literature is important for understanding the neural correlates of risky behaviors and risk factors for psychopathology that emerge during adolescence.

    “It is important to resolve these inconsistencies to gain a better understanding of the neural correlates of risky behaviors and risk factors for psychopathology that emerge during adolescence (Galvan, 2010; Paus et al., 2008).”
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    Premisenone given

    Transient factors include mental state, physical state, and context; sustained factors include mental traits, maturation level, genetic make-up, past experiences, and gender.

    “Transient factors may include individual mental state (e.g., depressed, stressed), physical state (e.g., drug action, sleep-deprived), or context (e.g., school vs. home, social vs. non-social). Sustained factors may include individual mental traits (e.g., inhibited temperament), maturation level (age, puberty), genetic make-up, past experiences, or gender.”
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    Premisecitation

    That study used dynamic causal modeling and reported distinct adolescent and adult patterns of connectivity strengths in a network including ventral striatum, thalamus, and insula.

    “This study used a causal modeling approach (dynamic causal modeling) and reported distinct adolescent and adult patterns of connectivity strengths in a discrete network including ventral striatum, thalamus and insula.”
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    • cites Cho et al., 2012

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    Premisenone given

    Dual neural systems models describe a cognitive regulatory system that modulates an emotional/motivational system.

    “In essence, these models describe a cognitive regulatory system that modulates the activity of an emotional/motivational system.”
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    Premisecitation

    Appetitive motivational processes appear to follow a curvilinear developmental trajectory, with reward sensitivity peaking in adolescence.

    “Behaviorally, appetitive motivational processes seem to follow a curvilinear developmental trajectory, whereby reward sensitivity peaks in adolescence (Ernst and Spear, 2009).”
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    • cites Ernst and Spear, 2009

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    Premisecitation

    The reward circuitry is a distributed network classically described as part of the cortico-basal ganglia system.

    “Briefly, the reward circuitry is a distributed network, classically described as part of the cortico-basal ganglia system (Alexander and Crutcher, 1990; Haber, 2003; Parent and Hazrati, 1995).”
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    Premisecitation

    The control module relies on prefrontal cortical structures with specialized functions: inhibition in right inferior prefrontal cortex, working memory and cognitive salience detection in dorsolateral prefrontal cortex, and conflict detection/monitoring/resolution in anterior cingulate cortex.

    “This module relies on prefrontal cortical structures that carry specialized functions, such as inhibition (right inferior prefrontal cortex) (Aron et al., 2004; Chikazoe et al., 2007; Liddle et al., 2001), working memory and cognitive salience detection (dorsolateral prefrontal cortex) (Rubia et al., 2010), and conflict detection, monitoring, and resolution (anterior cingulate cortex) (Amodio and”
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    Premisecitation

    The triadic model posits that all three dimensions are engaged in all motivated behaviors but in different ways depending on context, cognitive demands, and individual characteristics.

    “The model posits that all three dimensions are engaged in all motivated behaviors but in different ways as a function of multiple factors including context (e.g., approach vs. threat), cognitive demands, and individual characteristics (e.g., age, gender, personality, psychiatric status).”
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    • cites Ernst and Fudge, 2009

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    Premisecitation

    According to the Triadic Model, three neural systems collaborate to generate and modulate motivated behaviors.

    “According to the Triadic Model, three neural systems collaborate to generate and modulate motivated behaviors.”
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    Premisecitation

    The triadic functional modules are supported by distributed neural systems that are distinct but largely overlapping and linked by reciprocal interactions.

    “These functional modules are supported by distributed neural systems, which are distinct but largely overlapping, and linked by reciprocal interactions (Ernst and Fudge, 2009).”
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    Premisereasoning

    The central core of reward circuitry includes the ventral striatum and midbrain area, particularly the ventral tegmental area.

    “Its central core includes the ventral striatum and midbrain area, particularly the ventral tegmental area.”
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    Premisecitation

    The approach module comprises subcortical and cortical structures that are major sites of dopamine action, primarily striatum and medial/orbital prefrontal cortices.

    “This neural system comprises subcortical and cortical structures that are major sites of dopamine action, and include primarily the striatum (caudate nucleus, putamen and nucleus accumbens) (e.g., Di Chiara, 2002; Di Chiara and Bassareo, 2007; McClure et al., 2004; Schultz et al., 1998; Wise, 2004) and the medial and orbital prefrontal cortices (Jensen et al., 2003; Kringelbach, 2005).”
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    Premisecitation

    The triadic model partitions neural systems predominantly involved in appetitive response, aversive response, and executive function.

    “The triadic model offers a dynamic rendition of the neural systems involved in goal- directed behaviors and provides a framework for organizing findings along a systematic grid, partitioning the systems involved predominantly (but not selectively) in coding response to appetitive stimuli, response to aversive stimuli, and executive function.”
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    Premisereasoning

    The integrated activity of the triadic systems reaches an equilibrium that determines behavioral output, specific to a situation and modulated by transient and sustained factors.

    “Based on a given level of regional function and connectivity, the integrated activity of the triad reaches an equilibrium that determines behavioral output. This equilibrium is specific to a given situation (e.g., deciding on a course of action), but is modulated by both transient and sustained factors.”
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    Premisereasoning

    These transient and sustained factors contribute to large inter-individual variability in behavioral responses.

    “These factors are critical as they contribute to the large inter-individual variability of behavioral responses.”
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    Premisecitation

    The triadic modules are reward/approach, aversion/avoidance, and regulatory/control.

    “Their respective functions consist of a reward/approach module, an aversion/avoidance module, and a regulatory/control module.”
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    Premisecitation

    The most consistent findings on intrinsic connectivity development are an increase in long-range connections at the expense of short-range connections and enhanced selectivity and specialization of connections.

    “The most consistent findings have been the increase with development of long-range connections at the expense of short-term connections, and the enhanced selectivity and specialization of connections.”
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    Premisenone given

    Reward-related information is processed through glutamatergic projections from OFC and ACC and dopaminergic projections from midbrain to ventral striatum.

    “Reward-related information is processed across a circuitry involving large glutamatergic projections from the orbitofrontal cortex (OFC) and anterior cingulate cortex (ACC), as well as massive dopaminergic projections from the midbrain onto the ventral striatum.”
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    Premisenone given

    Other structures such as amygdala, hippocampus, lateral habenular nucleus, and raphe modulate reward circuitry.

    “Other important structures, such as the amygdala, hippocampus, lateral habenular nucleus and regions of the raphe, modulate this circuitry.”
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    Interpretationreasoning

    Possible reasons for these inconsistencies include variability in reward type and experimental paradigms, in addition to sample characteristics.

    “Possible reasons for these inconsistencies may be the variability in the type of rewards (e.g., points, candies, money; abstract vs. concrete) and the experimental paradigms that have been used in functional neuroimaging studies to probe the neural basis of reward functioning, in addition to sample characteristics.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: Reward task design is a source of discrepancies across developmental fMRI findings.
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    Premisecitation

    In the Cake Gambling task, dorsolateral prefrontal and orbitofrontal cortex were more activated to low than high probability trials, and these activations were not influenced by age.

    “the dorsolateral PFC (DLPFC) and OFC were both more activated to low probability than high probability trials, but these activations were not influenced by age”
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    Premisenone given

    Rarely are trials analyzed as whole trials without separating different stages within trials.

    “Rarely are the trials analyzed as whole trials, without separating the different stages (events) within trials (e.g., anticipation vs. feedback).”
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    Premisenone given

    Performance on instrumental tests is determined by criteria independent of incentives, although incentives modulate performance.

    “Performance on these instrumental tests is determined by criteria that are independent of the incentives, although incentives modulate performance.”
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    Premisecitation

    This shift putatively facilitates preferential recruitment of the reward module at the expense of the control module in incentive contexts and underlies the peak in reward-related traits and behaviors during adolescence.

    “This shift putatively facilitates preferential recruitment of the reward module at the expense of the control module in the context of incentives (Ernst et al., 2006), and underlies the peak in reward-related traits and behaviors (e.g., reward sensitivity, risk-taking, novelty seeking) that typically emerges during adolescence.”
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    • cites Ernst et al., 2006 source

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    Premisecitation

    Central to the Triadic Model is a shift in triadic balance during adolescence that varies across contexts.

    “Central to the Triadic Model is the notion of a shift in the triadic balance during adolescence that varies across contexts.”
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    Interpretationreasoning

    Orbitofrontal and ventromedial prefrontal cortex may modulate emotional reactivity to disappointing or non-rewarding outcomes more strongly in adults than adolescents, whereas amygdala and striatal responses to aversive and appetitive stimuli are less moderated by control systems in adolescents and therefore more active.

    “OFC/vPFC modulates emotional reactivity in the context of disappointing/non-rewarding outcomes more strongly in adults than in adolescents, whereas the amygdala and striatum, in response to aversive and appetitive stimuli respectively, are not as moderated by control systems in adolescents relatively to adults, and, therefore, are more active among adolescents than adults.”
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    Premisenone given

    The two passive tasks differed in the probability of rewarding stimulus presentation and in the type of reward used, faces versus monetary reward.

    “these two passive tasks differed on the probability of rewarding stimulus presentation and the type of reward presented (i.e., faces vs. monetary reward).”
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    Interpretationcitation

    The shift in triadic balance may also underlie a unique adolescent-related sensitivity to uncertainty and ambiguity.

    “Of note, this shift in the triadic balance may also underlie a unique adolescent-related sensitivity to uncertainty and ambiguity, as suggested by Tymula et al. (2012).”
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    Interpretationcitation

    Combining aspects of the three task types can enable researchers to address additional questions, such as the influence of self-agency on reward processes.

    “Combining aspects of these three types of reward tasks can enable researchers to address additional questions, such as the influence of self-agency on reward processes (Bar-Haim et al., 2009b; Bar-Haim et al., 2009a).”
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    Premisecitation

    A few studies have started to examine preparation and anticipation separately by separating them temporally, but none have compared adolescents to adults.

    “A few studies have started to examine these two types of processes separately by separating them temporally, but none have compared adolescents to adults (Bjork et al., 2012; Bjork et al., 2008).”
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    • cites Bjork et al., 2012 source

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    Interpretationcitation

    Two different aversive stimuli across passive reward tasks produced different age-related neural patterns: adolescents showed exaggerated amygdala activation to fearful faces, while adults showed enhanced orbitofrontal activation to reward omission.

    “two different types of aversive stimuli (fearful faces, reward omission) across the two passive reward tasks yielded different patterns of age-related neural activation in response to aversive stimuli or outcomes, with adolescents showing exaggerated amygdala activation to fearful faces, and adults showing enhanced OFC activation to reward omission.”
    Quote in the paperSubstantial claim
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    Premisenone given

    Three basic task structures have been used to contrast reward-related processes in youths versus adults: passive reward tasks, instrumental-reward tasks, and reward decision-making tasks.

    “Three basic task structures, outlined below, have been used to contrast reward-related processes in youths relative to adults: (1) passive reward tasks, (2) instrumental-reward tasks and (3) reward decision-making tasks.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The three task categories (passive, instrumental, decision-making) adequately capture the reward paradigms used in developmental fMRI studies.
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    Interpretationreasoning

    Reward decision-making tasks are probably the most complex because they involve a number of different behavioral reward-related processes.

    “This type of task is probably the most complex task as it involves a number of different behavioral reward-related processes, each providing opportunities for experimental manipulations.”
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    Premisecitation

    In Van Leijenhorst and colleagues' 2009 slot machine study, right anterior insula activation during reward anticipation decreased linearly with age from early adolescence to adulthood.

    “In anticipation of a probabilistic reward, a negative linear relationship was found between activation in the right anterior insula (MNI 42, 12, −3) and age from early adolescence to adulthood.”
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    • cites Van Leijenhorst and colleagues (2009)

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    Interpretationnone given

    Instrumental-reward paradigms offer flexibility in manipulating parameters such as test difficulty and nature of actions.

    “These instrumental-reward paradigms offer flexibility in allowing for the manipulation of many parameters of great interest, such as difficulty level of the test, which can inform motivation, or the nature of the actions involved in the test (e.g., cognitive, motor, perceptual).”
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    Interpretationreasoning

    Decision-making reward tasks permit researchers to test the neural basis of varying preferences among risky, novel, or delayed options, rather than execution of an objectively correct or incorrect response.

    “Overall, decision-making reward tasks, as defined here, permit researchers to test the neural basis of varying preferences among a range of risky (i.e., probabilistic), novel, or delayed options, rather than execution of an objectively correct or incorrect response.”
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    Premisecitation

    In a recent behavioral study, adolescents appeared ambiguity-tolerant and uncertainty-averse compared to adults.

    “In this recent behavioral study, adolescents appeared ambiguity-tolerant and, paradoxically, uncertainty-averse compared to adults.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Tymula et al., 2012 source

      Not checked in the free run.

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

    Premisenone given

    Sex differences in functional changes in reward-related neural systems during adolescence have not been studied systematically, and sample sizes are usually too small to examine sex effects.

    “Similarly, sex differences in functional changes in reward-related neural systems during adolescence have not been studied systematically, and sample sizes are usually too small to examine sex effects.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisereasoning

    In reward research, one strategy decomposes reward-related behavior into sequential stages including anticipation and feedback.

    “In the context of reward, one strategy is to decompose a simple “reward-related behavior” into its sequential parts (including pre- and post-reward receipt), which are often referred to as different stages of reward processing, (i.e., anticipation stage or feedback stage).”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S2 (checkable).

    Premisereasoning

    Research questions probing neural basis of different aspects of reward processing require tailored reward paradigms that manipulate factors under scrutiny and control for factors of no interest.

    “Thus, research questions probing the neural basis of different aspects of reward processing necessarily require tailored reward paradigms that can (1) manipulate the factors under scrutiny and (2) control for factors of no interest.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Interpretationreasoning

    The preparation stage is often labeled anticipation and includes both anticipation and preparation-for-action, which are often impossible to differentiate in existing instrumental-reward designs.

    “Of note, the “preparation” stage is often labeled as anticipation. Indeed, this stage clearly includes both anticipation and preparation-for-action, both processes being often impossible to differentiate within existing instrumental-reward task designs.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Premisecitation

    Jarcho et al. (2012) found that neural activity differed by age when reward receipt was prescribed by the task (no-choice condition), but was not influenced by age when decision-making was required (choice condition).

    “This study found that neural activity differed by age when the reward-receipt was prescribed by the task (no-choice condition), but was not influenced by age when decision-making was required (choice condition).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Jarcho et al., 2012 source

      Not checked in the free run.

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

    Interpretationreasoning

    The first version of the Cake Gambling task was framed as reward decision-making, but the authors classify it as instrumental-reward because it has an uncontroversial correct response (largest slice of cake).

    “For example, the first version of the Cake Gambling task (Van Leijenhorst et al., 2006) has been framed as making a decision for the reward underlying the largest piece of cake, leading this task to be referred to as a “reward decision-making task”; however, we place this task in the category of “instrumental-reward tasks”, because there is an uncontroversial correct and incorrect response, the”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Van Leijenhorst et al., 2006 source

      Not checked in the free run.

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

    Interpretationreasoning

    The boundary between instrumental-reward and decision-making tasks can be subtle and controversial.

    “However, the boundary between an instrumental-reward task and a decision-making task can be subtle and subject to controversy.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based).

    Interpretationnone given

    Instrumental-reward tasks do not inform decision-making per se, a fundamental aspect of motivated behavior.

    “However, these instrumental-reward tasks do not inform decision-making per se, a fundamental aspect of motivated behavior.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationreasoning

    The paradoxical uncertainty-averse finding in adolescents is provocative given substantial evidence that adolescence is a period of peak risk taking.

    “The paradoxical uncertainty-averse finding in adolescents is provocative, given the substantial evidence of adolescence as a period of peak in risk taking.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S2 (checkable), S3 (load-bearing).

    Premisenone given

    The cognitive neuroscience approach parses complex behaviors into elementary functional units that are more easily manipulated, measurable, and amenable to scientific scrutiny.

    “The cognitive neuroscience approach to the study of complex behaviors parses out these behaviors into more elementary functional units of behavior/cognition. These elemental units are more easily manipulated and measurable, and more amenable to scientific scrutiny.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Interpretationreasoning

    More difficult test performance may require more preparation; orthogonal manipulation of cognitive demands and reward level may dissociate preparation-for-action from anticipation during the preparation stage.

    “However, one may reason that the more difficult the test performance will be, the more preparation may be necessary; therefore, orthogonal manipulations of the cognitive demands (effort level) and the reward level may be a way to dissociate the contribution of both types of processes (preparation-for-action vs. anticipation) during the “preparation” stage.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Premisecitation

    The lateral prefrontal cortex is a key neural substrate underlying value integration and planning, and its activation would be expected to play a different role in decision-making versus instrumental-reward tasks.

    “A key neural substrate underlying value integration and planning is the lateral prefrontal cortex (Kable and Glimcher, 2009), and activation of this region would be expected to play a different role in tasks of decision-making vs. instrumental-reward tasks.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Kable and Glimcher, 2009 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    In Bjork et al. 2004, in response to non-losses versus losses, both groups activated putamen with deactivation to losses, and only adults activated medial prefrontal cortex.

    “In response to non-losses vs. losses, both groups activated putamen (deactivation to losses), and only adults activated medial PFC (Tal 1, 53, −6).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Bjork et al., 2004 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    In Smith et al. 2011, rewarded versus non-rewarded targets showed positive linear age relationships with reward-induced activation in sustained attention regions and negative linear relationships in visuospatial attention regions.

    “the comparison of neural activation in response to rewarded vs. non-rewarded targets revealed positive linear relationships of age with reward-induced activation in regions implicated in sustained attention (DLPFC, Tal 40, 44, 15; ventromedial OFC, Tal −29, 26, −2), but negative linear relationships between age and reward-induced activation in regions coding for visuospatial attention (putamen, Ta”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Smith et al. (2011) source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    In Geier et al. 2009b, orbitofrontal cortex showed a group difference only during saccade execution, with a stronger response to neutral trials in adolescents than adults.

    “The OFC showed a group difference only during saccade execution, with a stronger response to neutral trials in adolescents than adults (Tal −25, 44, −4).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Geier et al. (2009b)

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Reward and incentives have been shown to improve perceptual, cognitive, and motor performance as well as neural efficiency in animal and human studies.

    “Reward/incentives have been shown to improve perceptual, cognitive and motor performance as well as neural efficiency in the animal and human literature (Ding and Hikosaka, 2007; Pleger et al., 2008; Savine and Braver, 2010; Weil et al., 2010).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Ding and Hikosaka, 2007

      Not checked in the free run.

    • cites Pleger et al., 2008 source

      Not checked in the free run.

    • cites Savine and Braver, 2010

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    In Smith et al. 2011, adolescents responded faster to rewarded than non-rewarded targets, while adults showed no such difference.

    “Adolescents also responded significantly faster to rewarded targets relative to non-rewarded targets, while no such difference was found among adults”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Smith et al. (2011) source

      Not checked in the free run.

  • May combine two claims.

    Interpretationcitation

    In terms of neural engagement, adolescents compared with adults might show reward as less effective at recruiting sustained attention regions but more effective at recruiting visuospatial attention regions.

    “Interpreted in terms of neural engagement, adolescents compared to adults might show that reward is less effective at recruiting regions involved in sustained attention, but more effective at recruiting regions involved in visuospatial attention.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Interpretationcitation

    These findings support a theory of a peak during adolescence in neural response to reward, which might boost cognitive and motor function needed to obtain reward.

    “These findings support the theory of a peak during adolescence in neural response to reward, which in turn might boost the cognitive/motor function needed to perform correctly to obtain the reward.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Premisecitation

    In the Pirate task, during feedback, adolescents showed greater reward-induced nucleus accumbens activation than children or adults, and lower orbitofrontal activation to correct trials than adults, but no significant differences from adults across the whole trial.

    “During the feedback stage of this task, adolescents showed greater reward-induced activation of the nucleus accumbens compared with children or adults, and lower OFC activation (peak coordinates not available) in response to correct trials compared with adults, but showed no significant differences from adults in analyses conducted across the whole trial.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Galvan et al., 2006 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Cho et al. 2012 replicated the striatal findings, with putamen showing the largest adolescent-adult difference during preparation for gain versus neutral cues.

    “A more recent study by Cho, Fromm, and colleagues (Cho et al., 2012) replicated these striatal findings, although the putamen (MNI 26, −4, 12) was the region showing the largest difference between adolescents and adults during the preparation stage (gain cues vs. neutral cues).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Cho et al., 2012

      Not checked in the free run.

  • May combine two claims.

    Interpretationcitation

    Stronger activation in the youngest group suggests greater difficulty performing the antisaccade task or greater reliance on medial prefrontal structures.

    “A stronger activation in the youngest group suggests greater difficulty in performing the antisaccade task (Luna et al., 2001, 2004), or greater reliance on medial prefrontal structures.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Luna et al., 2001, 2004

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

  • May combine two claims.

    Premisecitation

    In Geier et al. 2009b, regions typically recruited in antisaccade tasks were less active in adolescents than adults on neutral trials, but showed no group differences on reward trials.

    “Regions typically recruited in antisaccade tasks tended to be less active among adolescents than adults in response to neutral trials, but showed no group differences to reward trials”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Geier et al. (2009b)

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    In Cho et al. 2012, motor cortex was more activated in adults than adolescents, possibly reflecting a stronger incentive effect on motor preparation in adults.

    “The motor cortex (MNI −38, −4, 56) was also more activated in adults than in adolescents, perhaps reflecting a stronger incentive effect on motor preparation in adults than in adolescents.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Cho et al., 2012

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    In Somerville et al. 2010, right inferior frontal gyrus activation decreased linearly with age, but this correlation disappeared after controlling for performance.

    “A linear decrease in rIFG activation with age was also reported, but this correlation with age vanished after controlling for performance.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Somerville et al. (2010) source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    In the WOF task, ventral striatum, amygdala, and dorsolateral prefrontal cortex were also activated by the risky-selection contrast, but similarly in both age groups.

    “Other regions, such as ventral striatum, amygdala, and DLPFC, were also activated by this contrast, but in a similar way for both age groups (Ernst et al., 2005).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Ernst et al., 2005

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Analysis of whole trials revealed greater striatal activation in positive trials in adolescents than adults, but lower orbitofrontal activation in children than adults, with adolescents not differing from adults.

    “Analysis of the trials as a whole revealed greater striatal activation in positive trials in adolescents than in adults, but lower OFC activation in children than in adults, with the adolescents not differing from the adults (Galvan et al., 2006).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Galvan et al., 2006 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    In the WOF task, nucleus accumbens within ventral striatum was more activated in adolescents than adults, with higher activation to gain.

    “the nucleus accumbens (MNI −16, 20, −4), within the ventral striatum, was more activated in adolescents compared to adults (higher activation to gain).”
    Quote in the paperSubstantial claim
  • Classified as probably not a substantial claim. May combine two claims.

    Interpretationreasoning

    Discrepancies may be due to the various cognitive processes engaged by different tasks, some serving reward receipt, some independent, and some possibly interfering with obtaining reward.

    “Discrepancies may be due to the various types of cognitive processes that are engaged in the different tasks, some at the service of receiving the reward, some independent, and some possibly interfering with getting the reward.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Interpretationcitation

    Thus, although learning did not differ between adolescents and adults, medial prefrontal cortex was recruited more efficiently as age increased.

    “Thus, whereas learning did not differ between adolescents and adults, medial PFC was recruited more efficiently as age increased.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Premisecitation

    In the Card Guessing Game, the adult response lay between the two adolescent groups and did not differ from either.

    “The adult response lay between the responses of the two adolescent groups, and did not differ from either group.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Forbes et al., 2010b

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    In the modified Cake Gambling task, during feedback in the gain condition, no linear age associations were found, but right caudate nucleus activation was greater in adolescents than adults or children.

    “During the feedback stage in the gain condition, no linear associations of brain activation with age were found, but a region of significantly greater activation in adolescents relative to adults or children was detected in the right caudate nucleus (MNI 21, 18, 9).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Van Leijenhorst et al., 2010 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    In the Game of Chicken, group differences emerged only in the low-penalty versus no-penalty contrast, where adolescents showed no brain activation differences while adults activated posterior medial prefrontal cortex and striatum more to risky than non-risky conditions.

    “Group differences emerged only in the low-penalty (risky) vs. no-penalty (not risky) contrast, for which adolescents showed no differences in brain activation, while the adults activated a number of regions, including posterior medial PFC and striatum, greater in response to risky relative to non-risky conditions.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Bjork et al., 2007 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    In the hypothetical discount task, during selection, the cost of delay was associated with higher activation of ventral striatum, putamen/thalamus, and superior parietal lobule in adolescents when selecting immediate reward, and temporal regions during delayed choices.

    “The neuroimaging data of the selection stage found that this cost was associated with higher activation of the ventral striatum (Tal −7, 26, −13), putamen/thalamus (Tal −22, −15, 4), and superior parietal lobule (Tal 25, −63, 53) in adolescents when selecting immediate reward, and temporal regions during delayed choices.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Christakou et al., 2011 source

      Not checked in the free run.

  • May combine two claims.

    Interpretationcitation

    These findings might suggest a unique effect of puberty on reward processes, although fully dissociating age from puberty remains challenging.

    “These findings might suggest a unique effect of puberty on reward processes, although a full dissociation of the effects of age from puberty remains challenging.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Forbes et al., 2010b

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    Adolescents also tend to show reduced control system functioning relative to adults, but this lesser reliance on control can be reversed when adolescents are rewarded for engaging control functions.

    “Adolescents also tend to display reduced control system functioning relative to adults, but this lesser reliance on the control system can be reversed when adolescents are rewarded specifically for engaging these control functions.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Premisecitation

    In the Card Guessing Game, the mid/late pubertal group showed a hypoactive caudate nucleus but hyperactive medial prefrontal cortex in response to win feedback.

    “The mid/late pubertal group evidenced a hypoactive caudate nucleus (MNI 10, −5, 15), but hyperactive medial PFC (BA 32, MNI 10, 23, 28) in response to a win-feedback.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Forbes et al., 2010b

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    In the Card Guessing Game, significant group differences were present only in the feedback stage, not in the anticipation stage.

    “Significant group differences were present only in the feedback stage, and not in the anticipation stage.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Forbes et al., 2010b

      Not checked in the free run.

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

    Premisecitation

    Sex-related differences have been reported in structural brain maturation.

    “Sex-related differences are noted in structural brain maturation (e.g. Lenroot et al., 2007; Pangelinan et al., 2011; Sowell et al., 2007).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Lenroot et al., 2007 source

      Not checked in the free run.

    • cites Pangelinan et al., 2011 source

      Not checked in the free run.

    • cites Sowell et al., 2007 source

      Not checked in the free run.

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

    Premisenone given

    Longitudinal studies have major drawbacks, including cost and potential confounds such as familiarity with repeated instruments, attrition, and cohort effects.

    “However, a major drawback of longitudinal studies is their cost difficulty, as well as potential confounds (e.g., familiarity with instruments repeated over time, attrition, cohort effects).”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Interpretationreasoning

    The BOLD signal to anticipation affects the neural response to feedback, since similar neural structures are recruited during both stages.

    “the neural response to feedback is affected by the BOLD signal to anticipation, given that similar neural structures are recruited in both stages.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Premisecitation

    fMRI activation does not distinguish inhibitory from excitatory neuronal firing, and assigning an excitatory or inhibitory role requires additional measures like behavior or functional connectivity.

    “Activation does not differentiate between the firing of inhibitory vs. excitatory neurons and the implication of an excitatory role vs. inhibitory role requires the use of qualifying variables, such as behavior or functional connectivity.”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Durston et al., 2006 source

      Not checked in the free run.

    • cites Poldrack, 2010 source

      Not checked in the free run.

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

    Premisecitation

    Resting-state connectivity studies across development are beginning to appear.

    “studies of resting state connectivity across development are starting to emerge (Fair et al., 2009; Stevens et al., 2009)”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Fair et al., 2009 source

      Not checked in the free run.

    • cites Stevens et al., 2009 source

      Not checked in the free run.

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

    Premisereasoning

    Cross-sectional studies can reveal only differences between age groups and are less able to delineate developmental processes.

    “Cross-over studies can only reveal differences between age groups and are less successful at delineating the process of development.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Premisenone given

    A longitudinal within-subjects design allows researchers to assess continuity and discontinuity within the same individuals over time and gives more statistical power than a between-subjects design.

    “Indeed the longitudinal design permits researchers to assess continuities and discontinuities of development within the same individuals over time, using a within-subjects design which provides more statistical power than between-subjects designs.”
    Quote in the paperSubstantial claim
99 of 99
  • The paper relies on this without support.

    No prior review provides comprehensive side-by-side comparisons of reward paradigms, sample characteristics, and results.

    “Many reviews on adolescent behavior address discrepancies in the literature, but given the limitations posed by issues of space and parsimony, none provide comprehensive side by side comparisons of the various paradigms, various samples (size, age and gender), and results.”
  • The paper relies on this without support.

    Reward task design is a source of discrepancies across developmental fMRI findings.

    “The goal of this review is to gather all the reward-related fMRI studies that have examined differences in reward function between adolescents and adults and examine reward task design as one source of discrepancies across studies.”
  • The paper relies on this without support.

    The three task categories (passive, instrumental, decision-making) adequately capture the reward paradigms used in developmental fMRI studies.

    “Three basic task structures, outlined below, have been used to contrast reward-related processes in youths relative to adults: (1) passive reward tasks, (2) instrumental-reward tasks and (3) reward decision-making tasks.”
  • The paper relies on this without support.

    In the real world, rewards are rarely obtained without some behavior by the individual to access or receive them.

    “rewards are rarely obtained in the real-world in the absence of some kind of behavior on the part of the individual in order to access or receive the reward.”
  • The paper relies on this without support.

    Developmental changes in reward-related behaviors occur during adolescence.

    “the developmental changes in reward-related behaviors that are seen during adolescence”
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?

  • Several reviews have discussed methodological differences across these studies that may have contributed to the inconsistent findings.

    “Since that 2008 publication, several reviews have discussed methodological differences across these studies that may have contributed to the inconsistent findings (see Galvan, 2010, Richards et al., 2013).”

    From The dual systems model: Review, reappraisal, and reaffirmation (2016) · cites this paper as Richards et al., 2013

  • In dual systems models, maturation of reward centers including the striatum occurs early in adolescence around puberty and is hypothesized to increase reward sensitivity and sensation seeking.

    “Within this framework, the maturation of reward centers in the brain, localized to midline dopaminergic regions, including the striatum, is thought to occur early in adolescence, around the time of puberty, and is hypothesized to evoke an increase in reward sensitivity that results in more frequent sensation seeking [for reviews, see 23, 24].”
  • Adolescence coincides with a peak in reward sensitivity.

    “One of the most prominent and well-documented neurobiological characteristics of adolescence is that it coincides with a peak in reward sensitivity [for review, see 23, 24].”
  • A recent review of reward tasks in adolescents identified sub-types of fMRI reward paradigms and found neural differences related to specific features from each sub-type.

    “A recent review of reward tasks in adolescents identified sub-types of fMRI reward paradigms (i.e. passive reward tasks, instrumental-reward tasks, decision making tasks) and found neural differences related to specific features from each sub-type (Richards et al., 2013).”
  • The role of ventral striatum in response to rewards across development is complex and in some cases conflicting, with some studies finding increases in activation peaking during adolescence, whereas others find attenuations.

    “The role of ventral striatum in response to rewards across development is complex and in some cases conflicting, with some studies finding increases in activation in this region peaking during adolescence, whereas others find attenuations [20,23,38].”

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 et al.'s lower striatal activation is placed in two different stages

    Minor

    The synthesis assigns the Bjork et al. (2004) finding to the cue stage, whereas its earlier description explicitly places the lower adolescent activation in the test-preparation stage. The review treats those as distinct stages.

  • A study with an adult group is later classified as pediatric-only

    Minor

    The review describes Forbes et al. (2010b) as comparing two pediatric groups with adults, but later lists it among studies assessed only in pediatric samples.

2 of 2

Cites

1 retracted

Flagged first, then by citations

Cited by

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Authors
Richards, J. M., Plate, R. C., & Ernst, M.
Affiliations
  • University of Maryland, College Park (US)
  • University of Wisconsin–Madison (US)
Venue
Neuroscience & Biobehavioral Reviews
Publisher
Elsevier BV
Published
2013-06
Volume
37
Issue
5
Pages
976-991
ISSN
0149-7634 (ISSN-L)
OpenAlex
W129603234
Cited by
174
References
136
Citations by year
2026: 1 · 2025: 7 · 2024: 6 · 2023: 10 · 2022: 13 · 2021: 9 · 2020: 12 · 2019: 12 · 2018: 25 · 2017: 14 · 2016: 18 · 2015: 27 · 2014: 17 · 2013: 3
FWCI
1.85
Type
journal article
Language
en
Open access
Locations
  • Neuroscience & Biobehavioral Reviews (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • National Institutes of Health
  • National Institute on Alcohol Abuse and Alcoholism (R21AA017685)
  • National Institute of Mental Health (ZIAMH002781)
  • National Institute on Drug Abuse (R01DA018647, R01DA019405, R01DA023384, T32DA028855)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
Keywords
reward processing, brain development, adolescents, adults, task design, triadic model, motivated behavior, developmental neuroimaging
MeSH terms
Adolescent, Adult, Aging, Brain, Cognition, Decision Making, Humans, Image Processing, Computer-Assisted, Magnetic Resonance Imaging, Oxygen, Reward

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 2026-10-06.

Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-10-06.

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