Cognitive flexibility in adolescence: Neural and behavioral mechanisms of reward prediction error processing in adaptive decision making during development
Open accessAbstract
Adolescence is associated with quickly changing environmental demands which require excellent adaptive skills and high cognitive flexibility. Feedback-guided adaptive learning and cognitive flexibility are driven by reward prediction error (RPE) signals, which indicate the accuracy of expectations and can be estimated using computational models. Despite the importance of cognitive flexibility during adolescence, only little is known about how RPE processing in cognitive flexibility deviates between adolescence and adulthood. In this study, we investigated the developmental aspects of cognitive flexibility by means of computational models and functional magnetic resonance imaging (fMRI). We compared the neural and behavioral correlates of cognitive flexibility in healthy adolescents (12-16years) to adults performing a probabilistic reversal learning task. Using a modified risk-sensitive reinforcement learning model, we found that adolescents learned faster from negative RPEs than adults. The fMRI analysis revealed that within the RPE network, the adolescents had a significantly altered RPE-response in the anterior insula. This effect seemed to be mainly driven by increased responses to negative prediction errors. In summary, our findings indicate that decision making in adolescence goes beyond merely increased reward-seeking behavior and provides a developmental perspective to the behavioral and neural mechanisms underlying cognitive flexibility in the context of reinforcement learning.
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Written from the paper’s full text.
TL;DR
Adolescents (12–16 years) and adults performed a probabilistic reversal learning task during fMRI; computational modeling showed adolescents learned faster from negative reward prediction errors (RPEs) than adults. This behavioral difference was accompanied by altered RPE-related anterior insula responses, mainly increased responses to negative RPEs in adolescents.
Key findings
- Overall task performance did not differ between groups: adults made 73.83% ± 4.4% correct responses and adolescents 73.38% ± 4.6% (t(34) = .296, p = .769); reversals also did not differ (adults 23.35 ± 8.80, adolescents 26.11 ± 8.31; t(34) = −.965, p = .341).
- The risk-sensitive model with anticorrelated valuation (RSAV) outperformed the other models, and adolescents had a significantly increased learning rate for negative RPEs in chosen objects (αc−: adults .49 ± .05, adolescents .69 ± .05; t(34) = −2.816, p = .04, corrected); other parameters did not differ significantly.
- fMRI showed a significant group difference in the right anterior insula (peak MNI x = 33, y = 18, z = 3; t = 4.60, k = 33), with increased activation for decreasing RPEs in adolescents.
- Exploratory binning of RPEs showed the anterior insula difference was driven by negative RPEs (adolescents vs adults: t(34) = −4.08, p < .001, corrected), while neutral (p = .734) and positive (p = .142) RPEs did not differ significantly.
Methods
- Thirty-seven subjects participated; one adolescent was excluded for excessive movement (> 2.5 mm scan-to-scan motion). Final groups were 19 adolescents aged 12–16 years (14.7 ± 1.3, 10 females) and 17 adults aged 20–29 years (25.6 ± 2.4, 10 females).
- Participants performed a probabilistic reversal learning task during fMRI: two runs of 60 trials each, plus 20 null trials per run; one stimulus was correct with 80% reward probability and the other with 20%, with reversals after at least 6 correct choices (maximum 10, randomly determined).
- Three reinforcement learning models were compared (Rescorla–Wagner, risk-sensitive, and RSAV); parameters were estimated by maximum log-likelihood using a genetic search algorithm, compared with AIC and Bayesian model selection. fMRI analysis used SPM8, with model-derived RPEs entered as a parametric modulator at feedback; group comparisons were restricted to RPE-processing areas and used p < .05 cluster-extent FWE (voxel height p < .001).
Limitations
- The paper states that the adolescent group had a relatively large age range (12–16 years), so the design cannot detect differences that may occur only early or late in adolescence.
- The paper states that the relatively small sample size prevented analysis of age-related changes within adolescence; larger samples and/or longitudinal designs are needed.
- Evident from the text: the study is cross-sectional, and for fMRI the authors estimated one single set of canonical model parameters for all participants rather than individual parameters, so neural analyses were not designed to model individual behavioral differences.
Model-written summary. Check it against the paper before relying on it.
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Cites
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Claims the paper makes
0 of 65 cited sources checked · 0 supported · 0 flagged
- Findingown data
The other model parameters (αc+, αu+, αu−, τ) did not differ significantly between adolescents and adults.
“whereas the other parameters did not differ significantly (αc+: adults: .45 ± .10, adolescents: .62 ± .07, t(34) = − 1.336, p = .95; αu+: adults: .72 ± .08, adolescents: .78 ± .07, t(34) = − .581, p = 1.00; αu−: adults: .58 ± .06, adolescents: .63 ± .04, t(34) = − .636, p = 1.00; τ: 2.4 ± .2, adolescents: 1.9 ± .2, t(34) = 1.595, p = .60).”
Quote in the paperNot a substantial claim - Findingown data
In the anterior insula, there was a significant RPE-effect across all subjects.
“The repeated measures ANOVA with factors group (adolescents, adults) and RPE (negative, neutral, positive) revealed a significant RPE-effect (indicating that the aIns is modulated by RPEs across all subjects, F(2,34) = 40.37, p < .001)”
Quote in the paperNot a substantial claim - Findingown data
RPEs were significantly anticorrelated with activity in the bilateral anterior insula, bilateral dorsomedial prefrontal cortex, and dorsolateral prefrontal cortex.
“The bilateral anterior insula (aIns), bilateral dorsomedial prefrontal cortex (dmPFC), and the dorsolateral prefrontal cortex were significantly anticorrelated with RPEs (decreasing RPEs elicit more activity, Table 2, Fig. 3A).”
Quote in the paperSubstantial claim - Findingown data
Within the RPE network, adolescents had a significantly altered RPE-response in the anterior insula.
“The fMRI analysis revealed that within the RPE network, the adolescents had a significantly altered RPE-response in the anterior insula.”
- Also stated in: § fMRI analysis · plain
“We found one significant cluster in the right aIns (peak MNI x = 33, y = 18, z = 3; t = 4.60, k = 33, Fig. 3B) which showed increased activation for decreasing RPEs in adolescents.”
- Also stated in: § Discussion · plain
“In the group comparison, we found a significantly different activation in the aIns.”
Quote in the paperSubstantial claim - Also stated in: § fMRI analysis · plain
- Findingown data
The groups did not differ in the number of reversals performed.
“The groups also did not differ in the number of reversals which they performed. The adults switched on average 23.35 (± 8.80) times and the adolescents reversed 26.11 (± 8.31) times (t(34) = − .965, p = .341).”
Quote in the paperNot a substantial claim
- Findingown data
Adolescents learned faster from negative reward prediction errors (RPEs) than adults.
“Using a modified risk-sensitive reinforcement learning model, we found that adolescents learned faster from negative RPEs than adults.”
- Also stated in: § Model comparison and parameters · plain
“Post-hoc t-tests revealed that adolescents had a significantly increased learning rate for negative RPEs in chosen objects (αc−: adults: .49 ± .05, adolescents: .69 ± .05, t(34) = − 2.816, p = .04, multiple comparison corrected, Fig. 2)”
- Also stated in: § Discussion · plain
“By using an advanced reinforcement learning model, we found that adolescents learn more quickly from negative RPEs than adults.”
Quote in the paperSubstantial claim- Rests on an assumption: The adolescent and adult groups did not differ on unmeasured variables that could confound the comparison of RPE processing.
- Also stated in: § Model comparison and parameters · plain
- Findingown data
In the anterior insula, there was no significant group effect across all RPE bins.
“but no significant group effect (indicating that the group difference was not caused by generally increased or decreased responses across all RPE bins, F(1,34) = 1.77, p = .193).”
Quote in the paperSubstantial claim - Findingown data
In the anterior insula, there was a significant group-by-RPE interaction.
“a significant group-by-RPE interaction (indicating that only some RPE bins differ between groups, F(2,34) = 4.60, p = .013)”
Quote in the paperSubstantial claim - Findingown data
RPEs were positively correlated with activity in the putamen, ventromedial prefrontal cortex, amygdala, and posterior cingulate.
“In our main effect analysis of RPEs in cognitive flexibility, we found areas which are typically positively correlated with RPEs (increasing RPEs elicit more activity) such as the putamen, ventromedial prefrontal cortex (vmPFC), amygdala and the posterior cingulate (Table 2).”
Quote in the paperSubstantial claim - Findingown data
The boundaries of the RPE bins did not differ between the groups.
“The boundaries did not differ between the groups (lower: t(34) = .64, p = .527; upper: t(34) = .70, p = .490).”
Quote in the paperNot a substantial claim - Findingown data
Adolescents showed a marginally decreased number of punishments before switching compared to adults.
“Interestingly, we found a marginally decreased number of punishments before the adolescents switched (t(34) = 1.71, p = .097, adolescents: 1.56 ± 0.22, adults: 1.71 ± 0.30).”
Quote in the paperNot a substantial claim - Findingown data
Neutral and positive RPEs did not elicit significantly different anterior insula responses between adolescents and adults.
“Neutral (t(34) = 1.18, p = .734) and positive RPEs (t(34) = 2.06, p = .142) were not significantly different.”
Quote in the paperSubstantial claim - Findingown data
The anterior insula group difference was mainly driven by increased responses to negative prediction errors in adolescents.
“This effect seemed to be mainly driven by increased responses to negative prediction errors.”
- Also stated in: § fMRI analysis · plain
“Post-hoc t-tests of the three bins revealed that the interaction was caused by a significantly increased response to negative RPEs in adolescents compared to adults (t(34) = − 4.08, p < .001, corrected for multiple comparisons, Fig. 3C).”
- Also stated in: § Discussion · plain
“the differential activation was mainly driven by the most negative RPEs, while neutral or positive RPEs did not elicit significantly different responses per se.”
Quote in the paperSubstantial claim - Also stated in: § fMRI analysis · plain
- Findingown data
In the context of cognitive flexibility, adolescents are more sensitive to negative reward prediction errors than adults.
“we were able to show that in the context of cognitive flexibility, adolescents are more sensitive to negative RPEs than adults.”
Quote in the paperSubstantial claim - Premisecitation
RPE-like signals are encoded by dopaminergic midbrain neurons.
“It is well established that RPE-like signals are encoded by dopaminergic midbrain neurons (Schultz, 2002; Schultz et al., 1997).”
Quote in the paperSubstantial claim0 of 2 sources checked - Premisecitation
RPE signals are projected to a decision making network including striatal, prefrontal, and insular regions.
“Such RPE signals are projected to a decision making network including striatal, prefrontal, and insular regions (e.g., Blakemore and Robbins, 2012; Bromberg-Martin et al., 2010; Gläscher et al., 2009).”
Quote in the paperNot a substantial claim0 of 3 sources checked - Premisecitation
Reinforcement learning theory suggests that cognitive flexibility and adaptive learning are driven by reward prediction error signals.
“The reinforcement learning (RL) theory (Sutton and Barto, 1998) suggests that cognitive flexibility and adaptive learning are driven by reward prediction error (RPE) signals.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Sutton and Barto, 1998
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- Interpretationown data
The anterior insula neural responses support the behavioral finding that adolescents were more sensitive to negative RPEs.
“The neural responses of the aIns support our behavioral finding that adolescents were more sensitive to negative RPEs: the differential activation was mainly driven by the most negative RPEs, while neutral or positive RPEs did not elicit significantly different responses per se.”
Quote in the paperSubstantial claim - Interpretationreasoning
Adolescents adjust their behavior more quickly after feedbacks that are worse than expected.
“This implies that adolescents adjust their behavior more quickly after feedbacks which are worse than they expected.”
Quote in the paperSubstantial claim - Premisecitation
The anterior insula is known to show specific activation patterns during adolescence.
“it is known to show specific activation patterns during adolescence (Smith et al., 2014).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Smith et al., 2014 source
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- Premisecitation
The anterior insula is crucially involved in RPE processing.
“Additionally, we hypothesized the anterior insular activity to be altered, because this region is crucially involved in RPE processing (Pessiglione et al., 2006; Seymour et al., 2004; Voon et al., 2010; Wittmann et al., 2008)”
- Also stated in: § Discussion · plain
“It has been found to process RPEs (Pessiglione et al., 2006; Seymour et al., 2004; Voon et al., 2010; Wittmann et al., 2008)”
Quote in the paperSubstantial claim0 of 3 sources checked - Also stated in: § Discussion · plain
- Premisecitation
In previous studies on healthy adults, neural correlates of RPEs in probabilistic reversal learning tasks positively correlated with striatal and ventromedial prefrontal areas and negatively correlated with dorsomedial prefrontal cortex and anterior insula.
“The neural correlates of RPEs in probabilistic reversal learning tasks have been successfully examined in previous studies on healthy adults and found to positively correlate with mainly striatal and ventromedial prefrontal areas, and to negatively correlate with areas such as the dorsomedial prefrontal cortex and the anterior insula (Gläscher et al., 2009; Hampton et al., 2006; Hauser et al., 201”
Quote in the paperSubstantial claim0 of 3 sources checked- cites Gläscher et al., 2009
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- cites Hampton et al., 2006 source
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- cites Hauser et al., 2014a, b
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- Premisecitation
Feedback-driven learning processes can be described by using an RPE-learning model.
“Computationally, these feedback-driven learning processes can well be described by using a RPE-learning model because the subjects learn entirely based on the feedback (e.g., Gläscher et al., 2009; Hauser et al., 2014a).”
Quote in the paperSubstantial claim0 of 2 sources checked- cites Gläscher et al., 2009
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- cites Hauser et al., 2014a
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- Interpretationown data
The use of reinforcement learning methods to study cognitive flexibility may be more sensitive to differences in the learning process than common behavioral analyses.
“This suggests that the use of reinforcement learning methods to study cognitive flexibility may be more sensitive to differences in the learning process than common behavioral analyses.”
Quote in the paperSubstantial claim - Premisecitation
The anterior insula is highly relevant for error processing.
“it is highly relevant for error processing (Dosenbach et al., 2006)”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Dosenbach et al., 2006 source
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- Premisecitation
Individual risk sensitivity can be assessed by using different learning rates for positive and negative RPEs when risk or outcome variance is not explicitly available.
“In a seminal paper by Niv et al. (2012), the authors showed that tasks, where risk or outcome variance is not explicitly available, individual risk sensitivity can be assessed by using different learning rates for positive and negative RPEs.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Niv et al., 2012 source
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- Premisecitation
In their fMRI analysis, Javadi et al. only analyzed responses in the anterior cingulate, ventral striatum and vmPFC.
“Moreover, in their fMRI analysis, the authors only analyzed responses in the anterior cingulate, ventral striatum and the vmPFC (Javadi et al., 2014a, b).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Javadi et al., 2014a, b
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- Interpretationcitation
It cannot be determined whether Javadi et al.'s anterior insula showed similar developmental changes in reward prediction error processing.
“Therefore, it cannot be determined whether their aIns showed similar developmental changes in RPE processing.”
Quote in the paperNot a substantial claim - Premisecitation
The Rescorla-Wagner model does not differentiate between learning from positive and negative reward prediction errors.
“In their behavioral modeling, Javadi et al. (2014a) used a Rescorla–Wagner model which does not differentiate between learning from positive and negative RPEs (Krugel et al., 2009; Rescorla and Wagner, 1972).”
Quote in the paperSubstantial claim0 of 2 sources checked- cites Krugel et al., 2009 source
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- cites Rescorla and Wagner, 1972
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- Interpretationreasoning
Javadi et al. could not detect an increased learning rate for negative reward prediction errors.
“Therefore, it is evident that the authors could not detect an increased learning rate for negative RPEs.”
Quote in the paperSubstantial claim - Premisecitation
Javadi et al. found increased decision noise in their adolescent sample compared to healthy adults.
“The authors (Javadi et al., 2014a) found an increased decision noise in their adolescent sample compared to healthy adults.”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Javadi et al., 2014a
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- Premisecitation
Models that update both options are better suited to model probabilistic reinforcement learning tasks.
“We and others previously demonstrated that models which update both options are better suited to model such a probabilistic reinforcement learning tasks (Gläscher et al., 2009; Hauser et al., 2014a).”
Quote in the paperSubstantial claim0 of 2 sources checked- cites Gläscher et al., 2009
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- cites Hauser et al., 2014a
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- Interpretationown data
The difference in sensitivity to negative reward prediction errors between adolescents and adults is likely caused by an altered response of the anterior insula.
“Our neuroimaging results suggest that this difference is likely to be caused by an altered response of the aIns.”
Quote in the paperSubstantial claim - Premisecitation
In reversal learning tasks, feedback about the chosen object also informs about the value of the unchosen stimulus.
“In reversal learning tasks, the feedback about the chosen object also informs about the value of the unchosen stimulus. Therefore, we and others used RPEs also to update the unchosen option (Gläscher et al., 2009; Hauser et al., 2014a).”
Quote in the paperSubstantial claim0 of 2 sources checked- cites Gläscher et al., 2009
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- cites Hauser et al., 2014a
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- Premisecitation
Javadi et al. did not find any differences in prediction error processing in their regions-of-interest.
“However, the authors did not find any differences in prediction error processing in their regions-of-interest - despite their large adolescent sample.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Javadi et al., 2014a
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- Premisecitation
The anterior insula indicates feedback errors with high reliability.
“it indicates (feedback) errors with a high reliability (Dosenbach et al., 2006)”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Dosenbach et al., 2006 source
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- Premisecitation
Only few studies have investigated RPE processing in adolescents.
“Despite the importance of RPE processing in adolescence, only few studies have investigated RPE processing in adolescents (Christakou et al., 2011; Cohen et al., 2010; Javadi et al., 2014a; van den Bos et al., 2012).”
Quote in the paperSubstantial claim0 of 3 sources checked - Interpretationown data
Decision making in adolescence goes beyond merely increased reward-seeking behavior, at least in the context of cognitive flexibility.
“This novel finding suggests that decision making in adolescence goes beyond merely increased reward-seeking behavior—at least in the context of cognitive flexibility.”
Quote in the paperSubstantial claim - Study design and conductown data
The study's adolescent group had a relatively large age range of 12-16 years.
“In this study, the age spectrum of our adolescent group had a relatively large age range (12–16 years).”
Quote in the paperSubstantial claim - Study design and conductreasoning
With the study's approach, differences that may occur only early or late in adolescence cannot be detected.
“With our approach, however, we are not able to detect differences which may only occur early or late in adolescence.”
Quote in the paperSubstantial claim - Premisecitation
The anterior insula receives dopaminergic innervations.
“It is well established that the aIns receives dopaminergic innervations (Gaspar et al., 1989) and processes dopamine-associated RPEs.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Gaspar et al., 1989 source
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- Study design and conductown data
Given the relatively small sample size, the study could not examine age-related changes during adolescence.
“Additionally, given the relatively small sample size, we were also not able to look at age-related changes during adolescence.”
Quote in the paperSubstantial claim
- May combine two claims. 9
- The quote only partly states this claim. 1
- Classified as probably not a substantial claim. 26
May combine two claims.
Findingown dataBoth groups performed the probabilistic reversal learning task equally well, with no significant difference in correct responses.
“Both groups performed the task equally well with 73.83% (± 4.4%) correct responses in adults and 73.38% (± 4.6%) in adolescents (t(34) = .296, p = .769).”
Quote in the paperNot a substantial claimThe quote only partly states this claim.
Findingown dataNo significantly increased activation for positive RPEs was found in adolescents compared to adults.
“We did not find any significantly increased activation for positive RPEs in adolescents.”
Quote in the paperSubstantial claimMay combine two claims.
Findingown dataThere was a significant difference between the free parameters and a significant interaction between parameters and group.
“We found a significant difference between the free parameters (F(4,136) = 73.45, p < .001) as well as an interaction between the parameters and the group (F(4,136) = 2.851, p = .026).”
Quote in the paperSubstantial claimMay combine two claims.
Findingown dataThe risk-sensitive model with anticorrelated valuation (RSAV) outperformed the other reinforcement learning models across all subjects and in both groups separately.
“The RSAV model clearly outperformed the other models across all subjects, as well as in both groups separately (Table 1).”
Quote in the paperSubstantial claimClassified as probably not a substantial claim.
PremisecitationProbabilistic reversal learning tasks have often been used to test cognitive flexibility.
“To test cognitive flexibility, probabilistic reversal learning tasks have often been used (e.g., Adleman et al., 2011; Britton et al., 2010; Clarke et al., 2004; Klanker et al., 2013; van der Plasse and Feenstra, 2008; Xue et al., 2013).”
Quote in the paperSubstantial claim0 of 3 sources checkedClassified as probably not a substantial claim.
PremisecitationCognitive flexibility has mainly been operationalized by sudden and implicit shifts in reward contingencies that have to be detected based on external feedback.
“In cognitive neuroscience and neuropsychology, cognitive flexibility has mainly been operationalized by sudden and implicit shifts in reward contingencies that have to be detected based on external feedback (Scott, 1962).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Scott, 1962 source
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PremisecitationJavadi et al. report a marginally different switching probability after correctly punished trials, similar to our study.
“Interestingly, the authors report a marginally different switching probability after correctly punished trials—similar as in our study.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
Study design and conductown dataThe study was approved by the local ethics committee and written informed consent was obtained from all adult participants and from adolescent participants and their parents.
“The study was approved by the local ethics committee and all adult participants gave written informed consent. For the adolescent group, the participants and their parents signed the consent form.”
Quote in the paperNot a substantial claimMay combine two claims.
PremisecitationPrevious studies found differential activations between adolescents and adults in striatal areas, but another study did not replicate that finding and instead found differences in connectivity between ventromedial prefrontal cortex and ventral striatum.
“While Cohen et al. (2010) found differential activations between adolescents and adults in striatal areas, van den Bos et al. (2012) were not able to replicate that finding, but found differences in the connectivity between the ventromedial prefrontal cortex and the ventral striatum.”
Quote in the paperSubstantial claim0 of 2 sources checkedProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationPrevious studies found developmental effects in the anterior insula during tasks of cognitive flexibility and in other cognitive domains.
“Previous studies found developmental effects during tasks of cognitive flexibility (e.g., Christakou et al., 2009; Rubia et al., 2006; Smith et al., 2011) and in other cognitive domains (Christakou et al., 2011; Jarcho et al., 2012; Keulers et al., 2011; Masten et al., 2009; Somerville et al., 2011; Van Leijenhorst et al., 2010).”
Quote in the paperNot a substantial claim0 of 3 sources checkedProbably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
InterpretationreasoningIncreased insular activity, especially to negative reward prediction errors, might indicate that adolescents weight emotional information more strongly, leading to faster adaptation from negative feedbacks.
“The increased insular activity (esp. to negative RPEs) might indicate that adolescents weight the emotional information more strongly which then leads to a faster adaptation from negative feedbacks.”
Quote in the paperNot a substantial claim- The authors state this as an assumption: The dorsomedial prefrontal cortex is mainly involved in processing cognitive aspects, whereas the anterior insula processes visceral and emotional information.
May combine two claims.
PremisecitationJavadi et al. did not find any reward prediction error differences in the anterior cingulate, ventral striatum and vmPFC, similar to our study.
“Similar as in our study, they did not find any RPE differences in these areas.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationThe anterior insula has been ascribed a wide variety of functions from processing visceral and emotional information to controlling attention and task demands.
“Unsurprisingly, the aIns has been ascribed to a wide variety of functions from processing visceral and emotional information (Critchley, 2005) to controlling attention and task demands (Dosenbach et al., 2006, 2007; Nelson et al., 2010).”
Quote in the paperNot a substantial claim0 of 3 sources checkedProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationThe anterior insula is involved when a feedback is processed consciously.
“This is also in line with the assumption that the aIns is involved when a feedback is processed consciously (Nelson et al., 2010; Wheeler et al., 2008).”
Quote in the paperNot a substantial claim0 of 2 sources checkedProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationAnterior insula activity often coincides with activation in the dorsomedial prefrontal cortex.
“It is well known that aIns activity often coincides with activation in the dmPFC (cf. Hauser et al., 2014a, 2014b; Nelson et al., 2010; Seymour et al., 2004).”
Quote in the paperNot a substantial claim0 of 3 sources checkedProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationAdolescents are more sensitive to the presence of peers.
“Adolescents are known to be more sensitive to the presence of peers (Chein et al., 2011) and peer rejection (Masten et al., 2009), and show a markedly increased prevalence in psychiatric disorders, such as anxiety, depression or substance abuse (Kessler et al., 2005, 2007).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Chein et al., 2011 source
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Premisenone givenThe developmental importance of the anterior insula has largely been neglected.
“However, the developmental importance of this area has largely been neglected.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationThe anterior insula is one of the most commonly activated areas in human neuroimaging studies.
“The aIns is a central hub in the brain and is one of the most commonly activated areas in human neuroimaging studies (Nelson et al., 2010).”
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PremisecitationThe anterior insula has been associated with processing information about risk.
“Moreover, the aIns has been associated with processing information about risk (Burke and Tobler, 2011; Ishii et al., 2012; Paulus et al., 2003; Preuschoff et al., 2008).”
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Study design and conductcitationSeveral regressors-of-no-interest were entered into the GLM to improve model validity.
“We additionally entered several regressors-of-no-interest into the GLM to improve model validity: choice values (value of chosen object) as parametric modulator at cue presentation, realignment-derived movement parameters, scan-to-scan movements greater than 1 mm, and cardiac pulsations (http://www.translationalneuromodeling.org/tapas/; Glover et al., 2000; Kasper et al., 2009).”
Quote in the paperNot a substantial claim0 of 2 sources checked- cites Glover et al., 2000 source
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- cites Kasper et al., 2009
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PremisecitationReinforcement learning models with anticorrelated valuation fitted this task better than a standard Rescorla-Wagner model in previous work.
“Given that we have previously shown that reinforcement learning models with anticorrelated valuation fitted this task better than a standard Rescorla–Wagner model (Hauser et al., 2014a), we evaluated the risk-sensitive model with an anticorrelated valuation (RSAV) extension as a third model.”
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Study design and conductown dataOne participant was excluded prior to analysis due to excessive movement (> 2.5 mm scan-to-scan motion).
“One participant (13.0 y, m) had to be excluded prior to analysis due to excessive movement (> 2.5 mm scan-to-scan motion).”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationThe anterior insula has a high predictive value for task switching in a similar cognitive flexibility task.
“it has a high predictive value for task switching in a similar cognitive flexibility task (Hampton and O'Doherty, 2007).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Hampton and O'Doherty, 2007
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PremisecitationAdolescents are more sensitive to peer rejection.
“Adolescents are known to be more sensitive to the presence of peers (Chein et al., 2011) and peer rejection (Masten et al., 2009), and show a markedly increased prevalence in psychiatric disorders, such as anxiety, depression or substance abuse (Kessler et al., 2005, 2007).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Masten et al., 2009 source
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PremisereasoningJavadi et al. did not report any analysis of the anterior insula.
“Unfortunately, the authors did not report any analysis of the aIns.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Study design and conductown dataThere was no difference in movement between the adolescent and adult groups during scanning.
“During scanning, there was no difference in movement between both groups (scan-to-scan movement: adults: mean = .079 mm ± .021; adolescents: mean = .076 mm ± .016; t(34) = .496, p = .623).”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
PremisecitationThe anterior insula is activated in a wide variety of cognitive and emotional tasks and forms the important salience network in resting state literature.
“It is activated in a wide variety of cognitive and emotional tasks (Dosenbach et al., 2006) and forms the important salience network in resting state literature (Menon and Uddin, 2010).”
Quote in the paperNot a substantial claim0 of 2 sources checkedProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationThe anterior insula has been associated with depression, anxiety or substance abuse.
“It has also been associated with depression, anxiety or substance abuse (for reviews cf. Craig, 2009; Naqvi and Bechara, 2009).”
Quote in the paperNot a substantial claim0 of 2 sources checkedProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationThe anterior insula is involved in social rejection.
“It is strongly involved in empathy-related processes (Singer et al., 2004, 2009) and social rejection (Masten et al., 2009).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Masten et al., 2009 source
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationThe anterior insula is strongly involved in empathy-related processes.
“It is strongly involved in empathy-related processes (Singer et al., 2004, 2009) and social rejection (Masten et al., 2009).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Singer et al., 2004, 2009
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
Probably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationAdolescents show a markedly increased prevalence in psychiatric disorders such as anxiety, depression or substance abuse.
“Adolescents are known to be more sensitive to the presence of peers (Chein et al., 2011) and peer rejection (Masten et al., 2009), and show a markedly increased prevalence in psychiatric disorders, such as anxiety, depression or substance abuse (Kessler et al., 2005, 2007).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Kessler et al., 2005, 2007
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
Probably not a substantial claim: may not pass S3 (load-bearing).
InterpretationreasoningIncreased insular sensitivity to negative reward prediction errors might affect not only decision making but also other areas in which adolescence is a unique period, such as social interactions or psychiatric disorders.
“Therefore, an increased insular sensitivity to negative RPEs might not only affect decision making, but also other areas in which adolescence reflects a unique period, such as in social interactions or psychiatric disorders.”
Quote in the paperNot a substantial claim- The authors state this as an assumption: Reward prediction error-like signals reflect a general neural update signal in a variety of domains, not only in decision making.
The paper relies on this without support.
The adolescent and adult groups did not differ on unmeasured variables that could confound the comparison of RPE processing.
“The adolescent group consisted of 19 participants between 12 and 16 years (14.7 y ± 1.3, 10 females). The adult group consisted of 17 participants between 20 and 29 years (25.6 y ± 2.4, 10 females).”
The authors state this as an assumption.
The dorsomedial prefrontal cortex is mainly involved in processing cognitive aspects, whereas the anterior insula processes visceral and emotional information.
“However, it is assumed that the dmPFC is mainly involved in processing cognitive aspects, whereas the aIns rather processes visceral and emotional information (Nelson et al., 2010).”
The authors state this as an assumption.
Reward prediction error-like signals reflect a general neural update signal in a variety of domains, not only in decision making.
“RPE-like signals are assumed to reflect a general neural update signal in a variety of domains, not only in decision making (Friston, 2010; Iglesias et al., 2013).”
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?
Adolescents learn faster from negative reward prediction errors than adults and recruit the right AI more during probabilistic reversal learning.
“These asymmetries are evident in studies demonstrating that adolescents learn faster from negative reward prediction errors than adults, and recruit the right AI to a greater degree during probabilistic reversal learning89.”
From Cognitive and behavioural flexibility: Neural mechanisms and clinical considerations (2021) · cites this paper as [89]
During a probabilistic reversal learning task requiring cognitive flexibility, the right anterior insular cortex shows increased task-related responses to negative reward prediction errors in adolescents compared with adults.
“During a probabilistic reversal learning task requiring cognitive flexibility, the right anterior insular cortex (rAI) shows increased task-related responses to negative reward prediction errors in adolescents compared with adults (53).”
From Brain Mechanisms Supporting Flexible Cognition and Behavior in Adolescents With Autism Spectrum Disorder (2021) · cites this paper as [53]
Statistics that don’t add up
Each reported p-value recomputed from its test statistic and degrees of freedom.
Inconsistent p-value: F(2,34) = 4.60, p = .013
MinorThe paper reports p = .013 here; recomputing from the test statistic and its degrees of freedom gives p = .017. The check cannot tell whether the statistic or the p-value is the misprint.
Reported p = .013 · recomputed p = .017
“F(2,34) = 4.60, p = .013”
Statistics recomputed
Every reported test result, recomputed from its test statistic and degrees of freedom. A result shows as not adding up only once an independent check has confirmed it.
- Doesn’t add upF(2, 34) = 4.6reported p = .013 · recomputed p = .017
“F(2,34) = 4.60, p = .013”
- Consistentt(34) = 0.496reported p = .623 · recomputed p = .623
“t(34) = .496, p = .623”
- Consistentt(34) = 0.64reported p = .527 · recomputed p = .526
“t(34) = .64, p = .527”
- Consistentt(34) = 0.7reported p = .49 · recomputed p = .489
“t(34) = .70, p = .490”
- Consistentt(34) = 0.296reported p = .769 · recomputed p = .769
“t(34) = .296, p = .769”
- Consistentt(34) = -0.965reported p = .341 · recomputed p = .341
“t(34) = − .965, p = .341”
- Consistentt(34) = 1.71reported p = .097 · recomputed p = .096
“t(34) = 1.71, p = .097”
- ConsistentF(4, 136) = 73.45reported p < .001 · recomputed p < .001
“F(4,136) = 73.45, p < .001”
- ConsistentF(4, 136) = 2.851reported p = .026 · recomputed p = .026
“F(4,136) = 2.851, p = .026”
- Consistentt(34) = -2.816reported p = .04 · recomputed p = .008
“t(34) = − 2.816, p = .04”
The paper states a correction for multiple tests
- Consistentt(34) = -1.336reported p = .95 · recomputed p = .190
“t(34) = − 1.336, p = .95”
The paper states a correction for multiple tests
- Consistentt(34) = -0.581reported p = 1 · recomputed p = .565
“t(34) = − .581, p = 1.00”
The paper states a correction for multiple tests
- Consistentt(34) = -0.636reported p = 1 · recomputed p = .529
“t(34) = − .636, p = 1.00”
The paper states a correction for multiple tests
- Consistentt(34) = 1.595reported p = .6 · recomputed p = .120
“t(34) = 1.595, p = .60”
The paper states a correction for multiple tests
- ConsistentF(2, 34) = 40.37reported p < .001 · recomputed p < .001
“F(2,34) = 40.37, p < .001”
- ConsistentF(1, 34) = 1.77reported p = .193 · recomputed p = .192
“F(1,34) = 1.77, p = .193”
- Consistentt(34) = -4.08reported p < .001 · recomputed p < .001
“t(34) = − 4.08, p < .001”
- Consistentt(34) = 1.18reported p = .734 · recomputed p = .246
“t(34) = 1.18, p = .734”
The paper states a correction for multiple tests
- Consistentt(34) = 2.06reported p = .142 · recomputed p = .047
“t(34) = 2.06, p = .142”
The paper states a correction for multiple tests
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
Incorrect denominator degrees of freedom for the RPE-bin ANOVA
MinorWith 36 participants in two groups and three RPE bins, the within-subject RPE effect and group-by-RPE interaction should have denominator degrees of freedom of 2 × (36 − 2) = 68, not 34. The paper reports 34 for both tests.
Reported 34 · recomputed 68
“F(2,34) = 40.37, p < .001), a significant group-by-RPE interaction (indicating that only some RPE bins differ between groups, F(2,34) = 4.60, p = .013)”
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- Authors
- Hauser, T. U., Iannaccone, R., Walitza, S., Brandeis, D., & Brem, S.
- Affiliations
- Wellcome Centre for Human Neuroimaging (GB)
- University of Zurich (CH)
- Corresponding author
- Hauser, Tobias U.
- Venue
- NeuroImage
- Publisher
- Elsevier BV
- Published
- 2015-01
- Volume
- 104
- Pages
- 347-354
- ISSN
- 1053-8119 (ISSN-L)
- PMC
- PMC4330550
- OpenAlex
- W2088333881
- Semantic Scholar
- 8130c15ff61aa1abdd0d9c20356489a71c12290d
- Cited by
- 203
- References
- 91
- Citations by year
- 2026: 11 · 2025: 25 · 2024: 21 · 2023: 21 · 2022: 19 · 2021: 24 · 2020: 22 · 2019: 14 · 2018: 15 · 2017: 12 · 2016: 12 · 2015: 7
- FWCI
- 5.72
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- NeuroImage (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Zurich Open Repository and Archive (University of Zurich) (acceptedVersion, other-oa)
- UCL Discovery (University College London) (submittedVersion)
- Repository for Publications and Research Data (ETH Zurich) (submittedVersion, cc-by-nc-sa)
- Zurich Open Repository and Archive (University of Zurich) (submittedVersion, other-oa)
- ETH Zürich Research Collection
- Zurich Open Repository and Archive (University of Zurich)
- Funders
- Swiss National Science Foundation (320030_130237, 151641)
- Hartmann Müller Foundation (1460)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Social Sciences › Decision Sciences › General Decision Sciences › Decision-Making and Behavioral Economics
- Keywords
- cognitive flexibility, adolescence, reward prediction error, adaptive decision-making, probabilistic reversal learning, risk-sensitive reinforcement learning, anterior insula, neural development, computational modeling
- MeSH terms
- Adolescent, Brain, Brain Mapping, Child, Cognition, Decision Making, Female, Humans, Learning, Magnetic Resonance Imaging, Male, 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.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
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