Neural networks involved in adolescent reward processing: an activation likelihood estimation meta-analysis of functional neuroimaging studies

May combine two claims.

Adolescents compared with adults show increased activation likelihood in bilateral ventral and dorsal striatum, insula, OFC, ACC, PCC, frontal opercular regions, paracingulate gyrus, subcallosal cortex, right amygdala, right occipital pole, and left lateral occipital cortex.

“However, in support of our predictions, contrast analyses revealed an increased likelihood for activation in adolescents compared with adults in the bilateral ventral and dorsal striatum, insula, OFC, anterior cingulate cortex (ACC), PCC, frontal opercular regions, paracingulate gyrus, subcallosal cortex; right amygdala, right occipital pole; and left lateral occipital cortex.”

• Also stated in: § Comparing Adolescent and Adult Reward Processing · plain

  “In our contrast analysis (using the coordinates for adult processing provided by Liu et al. (2011)), adolescents exhibited increased likelihood for activation in a large region that encompassed portions of the ventral and dorsal striatum, subcallosal cortex, insula, orbitofrontal region, and amygdala as well as the ACC, PCC, and paracingulate region.”

• Also stated in: § Comparing Adolescent and Adult Reward Processing · boosted

  “Other regions that showed strong likelihoods of activations in adolescents relative to adults include the insula, amygdala, putamen, and anterior cingulate cortex.”

• cites Liu et al. (2011) sourceNot checked yet

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• AssumptionRests on an assumption: The adult coordinates from Liu et al. (2011) are comparable to the adolescent coordinates for the purpose of contrast analysis.
• AssumptionRests on an assumption: The differences between adolescent and adult reward processing in the contrast analysis are not due to differences in tasks or sample characteristics between the adolescent and adult datasets.

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

Two independent researchers identified studies investigating reward processing during adolescence.

“Two independent researchers identified studies investigating reward processing during adolescence.”

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These regions collectively code hedonic drive, outcome-based behavioral flexibility and learning, and incentive salience.

“Importantly, these regions collectively code hedonic drive (nucleus accumbens, OFC, amygdala), outcome-based behavioral flexibility and learning (putamen; paracingulate), and incentive salience (insula, amygdala, ACC).”

May combine two claims.

In adolescents, reward-based behavior is strongly driven by incentive salience and concordant activation within the salience network.

“Findings suggest that in adolescents, reward-based behavior is strongly driven by incentive salience and concordant activation within what has been termed the salience network.”

Classified as probably not a substantial claim.

Significance in the overall, stage, and valence ALE analyses was determined using a cluster-level inference corrected threshold of p<0.05, 5000 thresholding permutations, and an uncorrected p-value of <0.001 as the cluster forming threshold.

“Significance in the overall, stage, and valence ALE analyses was determined using a cluster-level inference corrected threshold of p<0.05, 5000 thresholding permutations, and an uncorrected p-value of < 0.001 as the cluster forming threshold (Eickhoff et al., 2012).”

• cites Eickhoff et al., 2012Not checked yet

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Positive valence yields more consistent processing in PCC, accumbens, and lateral occipital cortex, suggesting a link between the limbic-motor interface and self-referential cognitive activity mediated by the PCC.

“Relative to negative valence, positive valence yields more consistent processing in the PCC, accumbens, and lateral occipital cortex, suggesting a link between the limbic-motor interface that allows approach to incentive-based stimuli (Depue and Collins, 1999) and the facilitation of self-referential cognitive activity that is mediated by the PCC (Johnson et al., 2002; Kelley et al., 2002).”

• cites Depue and Collins, 1999 sourceNot checked yet

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• cites Johnson et al., 2002 sourceNot checked yet

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• cites Kelley et al., 2002 sourceNot checked yet

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Adolescents and adults varied in activations during reward processing, as supported by descriptive comparisons and contrast analysis.

“A major finding of the current analysis is that adolescents and adults varied in activations during reward processing as supported by descriptive comparisons between our overall ALE and findings reported by Liu et al. (2011) as well as our contrast analysis.”

• cites Liu et al. (2011) sourceNot checked yet

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• AssumptionRests on an assumption: The adult coordinates from Liu et al. (2011) are comparable to the adolescent coordinates for the purpose of contrast analysis.
• AssumptionRests on an assumption: The differences between adolescent and adult reward processing in the contrast analysis are not due to differences in tasks or sample characteristics between the adolescent and adult datasets.

May combine two claims.

Adolescent behavior is strongly influenced by the salience of anticipated rewards and by amygdala-based valuation of outcomes.

“In contrast, the prominence of the insula, amygdala, and putamen in adolescents’ stage-related processing suggests that adolescent behavior is strongly influenced by the salience of anticipated rewards and by amygdala-based valuation of outcomes.”

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In adolescents, incentive-related behavior may be more strongly bound to stimulus salience or to the physical arousal generated by the stimulus context.

“These findings suggest that in adolescents, incentive-related behavior may be more strongly bound to stimulus salience or to the physical arousal generated by the stimulus context.”

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

There are dissociable neural underpinnings of 'wanting' (incentive motivation) and 'liking' (the pleasure of reward consumption).

“A related theory finds evidence for dissociable neural underpinnings of ‘wanting,’ or incentive motivation, and ‘liking,’ the pleasure of reward consumption (Robinson and Berridge, 1993; Berridge, 2009).”

• cites Robinson and Berridge, 1993Not checked yet

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• cites Berridge, 2009 sourceNot checked yet

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This readiness may be evolutionarily adaptive in guiding behavior toward future goals, but may also place adolescents at risk of poor decision-making in motivationally salient contexts.

“This readiness may be evolutionarily adaptive in guiding behavior toward future goals, but may also place adolescents at risk of poor decision-making in motivationally salient contexts (Luciana et al., 2012).”

• cites Luciana et al., 2012Not checked yet

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The ACC is rich in dopamine receptors and recognized as a core node within the incentive motivational system, suggesting a possible neurochemical basis for the aggregation of regions that showed stronger activation likelihoods in adolescents relative to adults.

“Importantly, the ACC is rich in dopamine receptors and recognized as a core node within the incentive motivational system (Depue and Collins, 1999; Haber, 2003; Berridge, 2004), suggesting the possibility of a neurochemical basis for the aggregation of regions that showed stronger activation likelihoods in adolescents relative to adults.”

• cites Depue and Collins, 1999 sourceNot checked yet

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• cites Haber, 2003 sourceNot checked yet

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• cites Berridge, 2004 sourceNot checked yet

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The patterning of findings is notable given the predominance of limbic and striatal regions and the relative absence of higher cortical regions with the exception of the lateral occipital cortex.

“Although there were no regions where adults showed a greater activation likelihood relative to adolescents, the patterning of our findings is notable given the predominance of limbic and striatal regions and the relative absence of higher cortical regions with the exception of the lateral occipital cortex, which plays a crucial role in stimulus recognition (Grill-Spector et al., 2001).”

• cites Grill-Spector et al., 2001Not checked yet

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• AssumptionRests on an assumption: The absence of significant higher cortical activation in adolescents is not due to insufficient power or methodological limitations.

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Risky behavior during the adolescent period is not specific to humans; adolescent compared with adult rats show increased risk-taking, novelty seeking, and voluntary alcohol consumption.

“risky behavior during the adolescent period is not specific to humans; for example, adolescent as compared to adult rats show increased risk-taking, novelty seeking, and voluntary alcohol consumption (Doremus et al., 2005; Spear, 2011; Wilmouth & Spear, 2009).”

• cites Doremus et al., 2005 sourceNot checked yet

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• cites Spear, 2011 sourceNot checked yet

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• cites Wilmouth & Spear, 2009 sourceNot checked yet

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Classified as probably not a substantial claim.

Positive reward valence and negative reward valence yield distinct functional activation patterns.

“positive reward valence and negative reward valence, which refer to the subjective states associated with gain or loss, yield distinct functional activation patterns and as a result are sometimes measured separately (Liu et al., 2007).”

• cites Liu et al., 2007Not checked yet

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In adolescents, reward processing is driven more strongly by limbic, paralimbic, and striatal regions without reliable contributions from higher cortical regions.

“The lack of significance of these regions in the current ALE suggests that in adolescents, reward processing is driven more strongly by limbic, paralimbic, and striatal regions without reliable contributions from higher cortical regions.”

• AssumptionRests on an assumption: The absence of significant higher cortical activation in adolescents is not due to insufficient power or methodological limitations.

May combine two claims.

Findings were not inordinately influenced by inclusion of relatively young participants; all ALE analyses repeated excluding participants below age 12 did not vary.

“Finally, to exclude the possibility that findings were inordinately influenced by the inclusion of relatively young participants, all ALE analyses were repeated excluding participants below the age of 12. Findings did not vary from what is described above.”

• Also stated in: § Limitations · plain

  “Running the analyses with and without studies that included individuals under age 12 revealed negligible differences in regions activated or regions found in the adolescent versus adults contrast.”

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

Studies were deemed eligible based on prespecified criteria including empirical data-based design, standard stereotactic space, fMRI, whole-brain peak activation coordinates, adolescent participants ages 8 to 18, and exclusion of special populations.

“Studies were deemed eligible for inclusion if they met the following criteria: 1) studies were empirical and data-based, and could not be review articles, 2) results were reported in standard stereotactic space (either in Talairach or Montreal Neurological Institute, MNI, space), 3) studies employed fMRI”

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

The adult reward processing ALE from Liu et al. (2011) was reproduced as a validation check of the procedures.

“using the coordinates for the overall adult reward processing ALE provided by Liu and colleagues (2011) and the thresholding parameters outlined in their manuscript, we reproduced the findings reported in their study as a validation check of our procedures.”

• cites Liu et al., 2011 sourceNot checked yet

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Findings on adolescent reward processing are inconsistent; studies have found both hyper- and hypo-activation in the ventral striatum and interconnected regions during different stages of motivational processing.

“findings are inconsistent. Studies have found both hyper- and hypo-activation in the VS and interconnected regions during different stages of motivational processing (e.g., Bjork et al., 2010; Geier et al., 2010)”

• cites Bjork et al., 2010 sourceNot checked yet

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• cites Geier et al., 2010 sourceNot checked yet

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Sample overlap was addressed by excluding the dataset with the smaller sample from two sets of studies with overlapping samples.

“As a result, the dataset with the smaller sample within each of these two sets of studies (Bjork et al., 2004; Telzer et al., 2013b) was excluded from the current analyses.”

• cites Bjork et al., 2004 sourceNot checked yet

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• cites Telzer et al., 2013bNot checked yet

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Pooling data across studies that assess similar constructs allows spatial coordinates to be identified that show consistent activation patterns across hundreds of participants, allowing the most robust findings to be discerned.

“Pooling data across studies that assess similar constructs allows spatial coordinates to be identified that show consistent activation patterns across hundreds of participants, allowing the most robust findings to be discerned.”

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

All ALEs were replicated in post hoc analyses excluding ten studies that included subjects younger than 12 to verify that results were not inordinately impacted by inclusion of these younger participants.

“all ALEs were replicated in post hoc analyses excluding the ten studies that included subjects younger than 12 in their sample (see Table 1) to verify that results were not inordinately impacted by inclusion of these younger participants.”

May combine two claims.

Adolescents may be highly sensitive to stimulus salience and to visceral experiences as they anticipate reward-based outcomes.

“These findings suggest that adolescents may be highly sensitive to stimulus salience and to visceral experiences as they anticipate reward-based outcomes.”

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

Contrast analyses used an uncorrected p-value of <.01 and a minimum cluster size of 60 voxels (480 mm^3) to determine statistical significance against a null distribution derived from 5000 permutations.

“For these analyses, an uncorrected p-value of <.01 and a minimum cluster size of 60 voxels (480 mm^3) were used to determine statistical significance against a null distribution (derived from 5000 permutations).”

Classified as probably not a substantial claim.

Reward processing can be dissociated into appetitive or motivational versus consummatory components.

“Animal studies indicate that reward processing can be dissociated into appetitive or motivational versus consummatory components (Robbins and Everitt, 1996; Ikemoto and Panksepp, 1999).”

• cites Robbins and Everitt, 1996Not checked yet

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• cites Ikemoto and Panksepp, 1999 sourceNot checked yet

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Different patterns of brain activation have been linked to reward anticipation and reward receipt in fMRI reward tasks.

“different patterns of brain activation have been linked to reward anticipation and reward receipt (Knutson et al., 2001).”

• cites Knutson et al., 2001 sourceNot checked yet

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Given the differences found here between adolescent and adult reward processing, this and similar meta-analyses of adolescent reward processing can guide hypothesis testing for future studies focusing on adolescents.

“Given the differences found here between adolescent and adult reward processing, this and similar meta-analyses of adolescent reward processing can guide hypothesis testing for future studies focusing on adolescents.”

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

Recent models of adolescent brain development predict peak levels of activation in the striatal-limbic system and lower-than-adult levels of frontal control.

“Recent models of adolescent brain development predict peak levels of activation in the striatal-limbic system, particularly in the pursuit or receipt of positive incentives, and lower-than-adult levels of frontal control as indexed by activation differences in the lateral prefrontal and parietal cortices in adolescents relative to both children and adults (Casey et al., 2008; Steinberg, 2010; Luci”

• cites Casey et al., 2008 sourceNot checked yet

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• cites Steinberg, 2010 sourceNot checked yet

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• cites Luciana et al., 2012Not checked yet

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ROI analyses limit detection of non-hypothesized findings, which in the context of ALE analysis would overly weigh regions with specific functional hypotheses.

“This is because ROI analyses limit detection of non-hypothesized findings, which in the context of ALE analysis would overly weigh regions with specific functional hypotheses.”

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

The dorsolateral prefrontal cortex in concert with parietal regions is integral to the brain's executive control network.

“The dorsolateral prefrontal cortex in concert with parietal regions is integral to the brain's executive control network, as discerned from studies of the brain's intrinsic functional connectivity (Beckmann et al., 2005; Seeley et al., 2007; Heine et al., 2012).”

• cites Beckmann et al., 2005 sourceNot checked yet

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• cites Seeley et al., 2007 sourceNot checked yet

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• cites Heine et al., 2012Not checked yet

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

Findings from discrete studies have suggested relative peaks in limbic and striatal activation in adolescents during reward processing and reward-based learning, but these findings are not definitive.

“Findings from discrete studies have suggested relative peaks in limbic and striatal activation in adolescents during reward processing and reward-based learning (c.f., Galvan et al., 2006; Cohen et al., 2010) but these findings are not definitive.”

• cites Galvan et al., 2006 sourceNot checked yet

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• cites Cohen et al., 2010 sourceNot checked yet

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Small sample sizes can impact meta-analytic findings due to the skewed nature of the sample of studies included.

“While the field of fMRI research is moving toward larger samples, small sample sizes can impact meta-analytic findings due to the skewed nature of the sample of studies included (Pereira and Ioannidis, 2011).”

• cites Pereira and Ioannidis, 2011Not checked yet

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These regions are interconnected with the ventral striatum and form core components of the brain's incentive salience system.

“These regions are interconnected with the ventral striatum and form core components of the brain's incentive salience system (Menon and Uddin, 2010).”

• cites Menon and Uddin, 2010 sourceNot checked yet

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The current study would be underpowered (power = .359) to detect an effect size of d = .20.

“of d =.20, the current study would be underpowered at .359).”

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The insula is a critical component of the brain's salience network and participates in interoceptive awareness, representation of physiological states associated with risk, and integration of such states with behavior during risky contexts.

“The insula is a critical component of the brain's salience network (Craig, 2009; Menon and Uddin, 2010) and participates in interoceptive awareness, the representation of physiological states associated with risk (Xue et al., 2010), and integration of such states with behavior during risky contexts that are characterized by uncertainty (Singer et al., 2009).”

• cites Craig, 2009 sourceNot checked yet

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• cites Menon and Uddin, 2010 sourceNot checked yet

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• cites Xue et al., 2010 sourceNot checked yet

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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).”

• cites Richards et al., 2013 sourceNot checked yet

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

In adults, the executive control network recruits sustained attention, working memory monitoring and manipulation processes, and flexibility.

“In adults, the executive control network recruits sustained attention, working memory monitoring and manipulation processes, and flexibility so that behavioral options can be assessed relative to the current environmental context, past experience, and outcome contingencies (Seeley et al., 2007) prior to response initiation.”

• cites Seeley et al., 2007 sourceNot checked yet

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The putamen may contribute to learning of outcome contingencies and modulates motor responses based on reward outcomes.

“Similarly, the putamen may contribute to the learning of outcome contingencies and modulates motor responses based on reward outcomes (Hori et al., 2009; Muranishi et al., 2011).”

• cites Hori et al., 2009Not checked yet

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• cites Muranishi et al., 2011Not checked yet

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The amygdala is a core node within the mesolimbocortical dopamine system and serves to modulate ventral striatal activity.

“The amygdala has been long-recognized as a core node within the mesolimbocortical dopamine system (Berridge, 2004) and serves to modulate ventral striatal activity (Ernst and Fudge, 2009).”

• cites Berridge, 2004 sourceNot checked yet

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• cites Ernst and Fudge, 2009 sourceNot checked yet

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In adolescents, the executive control network continues to mature, with increasing within-network functional connectivity evident with increasing age.

“In adolescents, this network continues to mature (Fair et al., 2007; Sherman et al., 2014), such that increasing within-network functional connectivity is evident with increasing age.”

• cites Fair et al., 2007 sourceNot checked yet

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• cites Sherman et al., 2014Not checked yet

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In reward contexts, the nucleus accumbens region of the ventral striatum acts as a motivation-to-behavior interface, facilitating approach behavior.

“In reward contexts, the nucleus accumbens region of the ventral striatum acts as a motivation-to-behavior interface, facilitating approach behavior by integrating information provided by excitatory inputs from the amygdala as well as other regions (Spear, 2011).”

• cites Spear, 2011 sourceNot checked yet

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