Maturation of limbic corticostriatal activation and connectivity associated with developmental changes in temporal discounting
Abstract
Temporal discounting (TD) matures with age, alongside other markers of increased impulse control, and coherent, self-regulated behaviour. Discounting paradigms quantify the ability to refrain from preference of immediate rewards, in favour of delayed, larger rewards. As such, they measure temporal foresight and the ability to delay gratification, functions that develop slowly into adulthood. We investigated the neural maturation that accompanies the previously observed age-related behavioural changes in discounting, from early adolescence into mid-adulthood. We used functional magnetic resonance imaging of a hypothetical discounting task with monetary rewards delayed in the week to year range. We show that age-related reductions in choice impulsivity were associated with changes in activation in ventromedial prefrontal cortex (vmPFC), anterior cingulate cortex (ACC), ventral striatum (VS), insula, inferior temporal gyrus, and posterior parietal cortex. Limbic frontostriatal activation changes were specifically associated with age-dependent reductions in impulsive choice, as part of a more extensive network of brain areas showing age-related changes in activation, including dorsolateral PFC, inferior parietal cortex, and subcortical areas. The maturational pattern of functional connectivity included strengthening in activation coupling between ventromedial and dorsolateral PFC, parietal and insular cortices during selection of delayed alternatives, and between vmPFC and VS during selection of immediate alternatives. We conclude that maturational mechanisms within limbic frontostriatal circuitry underlie the observed post-pubertal reductions in impulsive choice with increasing age, and that this effect is dependent on increased activation coherence within a network of areas associated with discounting behaviour and inter-temporal decision-making.
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The handful of studies that include a behavioral measure or control for behavioral differences in reward sensitivity across development all report both greater recruitment of the striatum during anticipation of reward and higher reward sensitivity among adolescents compared to adults, reflected in the behavioral outcomes.
“While most reward processing tasks used in neuroimaging studies do not include a behavioral measure or control for behavioral differences in reward sensitivity across development, the handful of studies that do (Barkley-Levenson and Galvan, 2014, Christakou et al., 2011, Geier et al., 2010, Padmanabhan et al., 2011, Somerville et al., 2011) all report both greater recruitment of the striatum”
From The dual systems model: Review, reappraisal, and reaffirmation (2016) · cites this paper as Christakou et al., 2011
Despite occasional inconsistencies in the literature, self-reported sensation seeking, behavioral measures of reward sensitivity, and neuroimaging studies of reward processing support the contention that reward sensitivity reaches its apex during adolescence.
“In summary, despite occasional inconsistencies in the literature, self-reported sensation seeking, behavioral measures of reward sensitivity, and neuroimaging studies of reward processing support the contention that reward sensitivity reaches its apex during adolescence (e.g., Barkley-Levenson and Galvan, 2014, Christakou et al., 2011, Collado et al., 2014, Galvan and McGlennen, 2013, MacPherson”
From The dual systems model: Review, reappraisal, and reaffirmation (2016) · cites this paper as Christakou et al., 2011
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).”
From Cognitive flexibility in adolescence: Neural and behavioral mechanisms of reward prediction error processing in adaptive decision making during development (2015) · cites this paper as Christakou et al., 2011
Only a handful of studies have explored age differences in brain activity during a risk-taking task, and evidence for mutual involvement of both lateral prefrontal cortex and striatum during risky decision making is scarce.
“Only a handful of studies (see table 1) have explored age differences in brain activity during the performance of a risk-taking task [97, 101–105], and evidence for mutual involvement of both the IPFC and striatum during risky decision making is scarce.”
From The role of the anterior insula in adolescent decision making (2014) · cites this paper as [103]
Only one study has reported age-related differences as hypothesized by current neurodevelopmental models in both reward-processing and cognitive control regions, and at least for the striatum the age difference was observed only when social context was manipulated.
“Indeed, only one study has reported age-related differences as hypothesized by current neurodevelopmental models (increased engagement of reward processing regions and less engagement of cognitive control regions in adolescents compared to adults) in both regions [103] and, at least for the striatum, the age difference was only observed when social context was manipulated.”
From The role of the anterior insula in adolescent decision making (2014) · cites this paper as [103]
In the hypothetical discount task, the subjective cost of delay was higher in adolescents than adults.
“Performance data showed that this subjective cost of delay was higher in adolescents than in adults.”
From A systematic review of fMRI reward paradigms used in studies of adolescents vs. adults: The impact of task design and implications for understanding neurodevelopment (2013) · cites this paper as Christakou et al., 2011
The authors concluded that ventromedial prefrontal cortex becomes progressively more able to incorporate information about the delay-dependent value of future rewards.
“The authors concluded that ventromedial PFC was progressively more able to incorporate information about the delay-dependent value of future rewards.”
From A systematic review of fMRI reward paradigms used in studies of adolescents vs. adults: The impact of task design and implications for understanding neurodevelopment (2013) · cites this paper as Christakou et al., 2011
In the hypothetical discount task, the only region showing increasing activation with age and with decreased cost was ventromedial prefrontal cortex.
“The only region showing increasing activation with age, and with decreased cost (i.e., larger delays), was the ventromedial PFC (Tal −18, 46, −6).”
From A systematic review of fMRI reward paradigms used in studies of adolescents vs. adults: The impact of task design and implications for understanding neurodevelopment (2013) · cites this paper as Christakou et al., 2011
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.”
From A systematic review of fMRI reward paradigms used in studies of adolescents vs. adults: The impact of task design and implications for understanding neurodevelopment (2013) · cites this paper as Christakou et al., 2011
In the hypothetical discount task, connectivity analyses showed strengthening of functional links between ventromedial prefrontal cortex and ventral striatum with age during selection of immediate options.
“connectivity analyses showed strengthening of functional links between ventromedial PFC and ventral striatum with age during selection of immediate options.”
From A systematic review of fMRI reward paradigms used in studies of adolescents vs. adults: The impact of task design and implications for understanding neurodevelopment (2013) · cites this paper as Christakou et al., 2011
Adolescents, more so than children or adults, show heightened activation in the ventral striatum following the receipt of hedonic rewards, including money, sucrose, and immediate rather than long-term rewards.
“human and rodent research has shown that adolescents, more so than children or adults, show heightened activation in the ventral striatum following the receipt of hedonic rewards, including money, sucrose, and immediate rather than long-term rewards (7, 15, 19, 20).”
From Neural sensitivity to eudaimonic and hedonic rewards differentially predict adolescent depressive symptoms over time (2014) · cites this paper as [15]
Delay discounting generally decreases between young childhood and adulthood, meaning children tend to choose a smaller immediate reward over a larger delayed reward.
“Delay discounting generally decreases between young childhood and adulthood, meaning children tend to choose a smaller immediate reward over a larger delayed reward (Christakou et al., 2011; de Water et al., 2014; Green et al., 1994; Olson et al., 2007; Scheres et al., 2006; Steinberg et al., 2009).”
From Does puberty mark a transition in sensitive periods for plasticity in the associative neocortex? (2017) · cites this paper as Christakou et al., 2011
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- Authors
- Christakou, A., Brammer, M., & Rubia, K.
- Affiliations
- King's College London (GB)
- Corresponding author
- Christakou, Anastasia
- Venue
- NeuroImage
- Publisher
- Elsevier BV
- Published
- 2011-01
- Volume
- 54
- Issue
- 2
- Pages
- 1344-1354
- ISSN
- 1053-8119 (ISSN-L)
- OpenAlex
- W1982834603
- Cited by
- 266
- References
- 139
- Citations by year
- 2026: 4 · 2025: 10 · 2024: 11 · 2023: 13 · 2022: 9 · 2021: 12 · 2020: 15 · 2019: 14 · 2018: 28 · 2017: 23 · 2016: 16 · 2015: 19 · 2014: 31 · 2013: 22 · 2012: 29
- FWCI
- 11.60
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- NeuroImage (publishedVersion)
- PubMed (publishedVersion)
- CentAUR (University of Reading) (submittedVersion)
- Research Portal (King's College London) (submittedVersion)
- Funders
- Medical Research Council (GO300155)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Social Sciences › Decision Sciences › General Decision Sciences › Decision-Making and Behavioral Economics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- delay discounting, neuronal maturation, impulsivity, impulsive choice, ventromedial prefrontal cortex, anterior cingulate cortex, ventral striatum, insula, frontostriatal circuits, functional connectivity, intertemporal choice, adolescence, brain aging
- MeSH terms
- Adolescent, Adult, Aging, Brain, Brain Mapping, Child, Choice Behavior, Humans, Image Processing, Computer-Assisted, Impulsive Behavior, Magnetic Resonance Imaging, Male, Neural Pathways, Reward, Young Adult
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.
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.
What counts as a claim ›How we measure confidence ›How we check this ›
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