Abstract
Objective
The term delay aversion has been used both to describe a behavioural tendency of greater preference for smaller-immediate over larger-delayed rewards (choice impulsivity), and to refer to a secondary explanatory construct put forward by delay aversion theory. In this study we examined the association of ADHD symptoms with choice impulsivity and tested the specific hypothesis derived from delay aversion theory.
Method
1062 children aged 7.90-10.90 years (49% female) made a fixed number of repeated choices between a smaller reward delivered immediately and a larger reward delivered after a delay (choice-delay task), under two conditions (including and excluding a post-reward delay). We assessed the unique contribution of each ADHD symptom dimension to the prediction of choice impulsivity and delay aversion, controlling for age (or age and IQ). Gender effects were examined.
Results
Inattention ratings uniquely predicted preference for smaller-immediate rewards under both task conditions for both genders. An index of delay aversion was associated with inattention only in boys; the effect size was small yet significant. Hyperactivity-impulsivity ratings were negatively associated with choice impulsivity in girls in the post-reward delay condition, whereas no significant association with hyperactivity-impulsivity ratings was observed in boys. Categorical analyses using groups with high ADHD symptoms yielded similar results.
Conclusions
This is the first study to report a unique association between inattention symptoms and behavioural measures of choice impulsivity and delay aversion. The findings indicate the importance of the primary constitutional processes that underlie choice impulsivity and their potential role in behavioural inattention. Understanding the behavioural and brain processes underlying choice impulsivity may lead to the improved targeting of behavioural and pharmacological interventions.
Keywords: ADHD, inattention, hyperactivity-impulsivity, delay aversion, choice impulsivity
Delay aversion theory1,2 has been influential in ADHD research, rekindling interest in motivational processes as explanatory factors for symptoms of inattention and hyperactivity-impulsivity. Defined as a motivational style characterised by a “negative emotional reaction to the imposition of delay”,3 the concept of delay aversion is used to denote an independent, complementary developmental route that may contribute to the emergence of ADHD behaviours, alongside a more cognitive/executive dysfunction pathway, as proposed in a dual pathway model.1,3
The choice-delay paradigm has provided an experimental platform for the development of delay aversion theory. Participants are offered a fixed number of repeated choices between a smaller-immediate or a larger-delayed reward (a secondary reinforcer). Preference for smaller-immediate rewards (henceforth called choice impulsivity) denotes lack of self-control, assuming that maximisation of rewards is of greater importance for the organism.4,5
The initial formulation of delay aversion theory2 proposed an alternative to the traditional inability-for-self-control interpretation of choice impulsivity in children with “pervasive hyperactivity”. A stronger preference for smaller-immediate rewards was observed when this response style also shortened task length, but not when choice did not impact on task duration. An impulsive behavioural style, rather than reflecting an inhibitory deficit, was seen as a functional, adaptive strategy to reduce overall delay by people who are averse to it. Two direct predictions were derived. First, hyperactive children should be sensitive to overall task length, irrespective of whether the delay precedes or follows the delivery of rewards. Secondly, children with ADHD will be able to restrain “impulsive” behaviour when it does not reduce overall task length but will prefer not to do so when it shortens task length, despite the economic cost of this behaviour. A study using 3 year old preschoolers with ADHD-typical behaviour provided support for the initial delay aversion theory6 (although caution is required in extrapolating to school-aged children given the potential role of verbal ability in self control7), but other studies challenged it. Controlling for level of reward, Tripp and Alsop8 showed that children with ADHD are unusually sensitive to pre-reward (rather than post-reward) delays, suggesting that they have a stronger need to seek immediate rewards rather than be delay-averse. Schweitzer and Sulzer-Azaroff9 found that children with ADHD had a higher preference for smaller-immediate rewards compared to controls even though task length was kept constant.
Later formulations of delay aversion theory3,10 embrace impulsivity-as-lack-of-self-control as the necessary substrate for the development of an acquired motivational tendency to avoid/escape delays, i.e. delay aversion. It is postulated that the interaction between a primary constitutional dysfunction of the mesolimbic dopaminergic system (presenting as behavioural impulsivity) and specific familial-societal demands, which clash with an impulsive behavioural style, lead to failure and consequently the development of negative affect for periods of delay.10 The developmental aspect to this model is yet to be tested empirically.
Children with a clinical or research diagnosis of ADHD have demonstrated increased choice impulsivity both when this reduces overall task length11-15 and when it does not.9 Choice impulsivity has also been associated with ADHD symptoms in studies using community samples16,17 and in a study with young adults.18 Other studies, using the same19,20 or a different paradigm,21 have failed to replicate this finding. Studies using hypothetical rewards suggest that the nature and magnitude of rewards may be important factors.18,22
The prediction that children with ADHD prefer smaller-immediate over larger-delayed rewards is not specific to delay aversion theory, but shared with other theories too.23,24 What sets delay aversion theory apart is the prediction that children with ADHD should show a differential increase in choice impulsivity under conditions where delay can be escaped compared to conditions where delay cannot be avoided. So far, apart from the original study,2 three studies have obtained data that enable a direct test of the hypothesis specific to delay aversion theory. These studies compared the two conditions: choice of the smaller-immediate reward followed by no post-reward delay, with a post-reward delay condition such that task length remains constant irrespective of one’s pattern of responses. The association between delay aversion and ADHD has been tested in two ways: as the statistical interaction between diagnostic group and delay condition,25 or as the differential increase in choice impulsivity for children with ADHD in the no post-reward delay condition.6,25
The first study was reviewed above.6 The second study,25 on a large European sample of 360 combined type ADHD probands and 112 controls found, first, that probands with ADHD selected the larger-delayed reward less often than healthy controls in both the post- and no post-reward delay conditions (effect sizes partial η2=0.029 and 0.056 respectively). Second, the interaction between group and condition was significant, corresponding to an effect size of partial η2=0.027 (all effects uncorrected for age or IQ).25 Partial η2 does not express the total amount of explained variance, but the maximum possible amount of variance the corresponding term can explain.26,27 We therefore conclude from this study that a maximum of 2.7% of the variance in the change in choice impulsivity between the two test conditions (reflecting delay aversion) is accounted for by ADHD group status. Finally, a third study21 failed to support the delay aversion theory as children with ADHD were indistinguishable from typically developing children under both conditions. This study showed that, across diagnostic status, children (6-11 years old) had a steeper discounting of delayed rewards compared to adolescents (12-17 years old) under both conditions, suggesting that choice is influenced by reward immediacy rather than delay aversion in the younger group.
Evidence from quantitative genetic and epidemiological studies supports the idea that individuals with ADHD represent the extreme of continuously distributed ADHD symptoms in the general population and the validity of making inferences from population data to clinical cases (see28 for a summary). Given the selection biases that may be associated with clinic-referred samples, it is important to complement studies that have focused on clinical samples with studies that focus on unselected, population-based samples. Population samples also enable an investigation of the two ADHD symptom dimensions separately, as well as an investigation of gender effects. Some previous studies have showed an association between choice impulsivity and both inattention and hyperactivity-impulsivity,17 while others only with hyperactivity-impulsivity.12,18 In general population samples, boys have higher inattention and hyperactivity/impulsivity scores than girls,16,29 while no gender differences in choice impulsivity16,25 or discounting rate30 have been reported.
The present study focuses on a large, general population sample of children, using a task identical to that used by Marco et al.25 We predicted that the behavioural symptoms of inattention and hyperactivity-impulsivity would be positively associated with choice impulsivity under both the post-reward delay and no post-reward delay conditions. The original delay aversion formulation predicted an association with ADHD only in the no post-reward delay condition, yet more recent theoretical arguments and empirical data lead to the prediction of an association with ADHD symptoms under both conditions. According to recent formulations of the delay aversion hypothesis, we further predicted that ADHD symptom scores would be positively correlated with an index of delay aversion, expressing the relative increase in preference for smaller-immediate rewards in the no post-reward compared to the post-reward delay condition.
Second, we adopted a categorical approach to defining extreme groups based on the inattention, hyperactivity-impulsivity or combined symptom dimensions, and used the 95th percentile on each scale, based on the whole sample, as a cut-off point. The comparison of a quantitative and a categorical approach in the same general population sample allows us to examine whether ADHD symptoms are associated with choice impulsivity and/or delay aversion below the clinical threshold levels and not only in clinical cases of ADHD. Assuming that ADHD is the extreme of a quantitative trait normally distributed in the population, we predicted that the association between extreme group membership, choice impulsivity and delay aversion would be comparable to that observed using the quantitative symptom scores. The categorical analyses were restricted to boys due to the very small number of girls with high symptom ratings.
METHOD
Sample and procedure
Participants are members of the Study of Activity and Impulsivity Levels (SAIL) in children,31 a general population sample of twins aged 7.9 to 10.9 years, recruited from the Twins’ Early Development Study (TEDS),32 a birth cohort study which had invited parents of all twins born in England and Wales during 1994-1996 to enrol.
Of the 1,230 suitable families contacted, 672 families (55%) agreed to participate. Children with an IQ below 70, on neuropsychiatric medication or with specific medical, neurological or psychiatric conditions were excluded (for details on inclusion and exclusion criteria, see31). For the current analyses, we only included participants with ADHD ratings from both parents and teachers, who completed both conditions of the Maudsley Index of Childhood Delay Aversion task, reflecting 79% of the total available SAIL sample, or 1,062 children. The mean age was 8.80 (SD=0.66) and children’s IQs ranged from 70 to 158 (M=109.74, SD=14.95). Parents of all participants gave informed consent following procedures approved by the Institute of Psychiatry Ethical Committee.
Two testers assessed the twins simultaneously in separate testing rooms at the Research Centre. The tasks were administered in a fixed order as part of a more extensive test session, which in total lasted approximately 2.5 hours.
Measures
Wechsler Intelligence Scales for Children, Third Edition (WISC-III)33
The vocabulary, similarities, picture completion and block design subtests from the WISC were used to obtain an estimate of the child’s IQ.
The Maudsley Index of Childhood Delay Aversion14 (MIDA; see31 for a description of task presentation)
Two conditions, each with 20 trials, were administered. In each trial the child had a choice between a smaller-immediate reward (one point involving a 2 second pre-reward delay) and a larger-delayed reward (two points involving a 30 second pre-reward delay). In the no post-reward delay condition, choosing the small reward led immediately to the next trial, reducing the overall length of the condition. In the post-reward delay condition, choosing the small reward led to a delay period of 30 seconds and choosing the large reward to a delay period of 2 seconds before the next trial; therefore the overall delay was constant and independent of choice made. The order of the two conditions was randomly chosen for each twin.
Two measures were extracted from this task: (a) number of times the smaller-immediate reward was selected in each condition, controlling for total number of trials attempted (see Data analyses); (b) a quantitative index of delay aversion (IDA), calculated as the difference in the percentage of times the smaller-immediate reward was selected between the two conditions. A higher score reflected increased preference for smaller-immediate rewards in the no post-reward delay condition and thus a greater degree of delay aversion.
Ratings of inattention and hyperactivity-impulsivity
Parents and teachers were asked to complete the Long Versions of the Conners’ Parent and Teacher Rating Scales.34,35 From both scales, we used the 9-item hyperactive-impulsive and 9-item inattentive DSM-IV symptoms sub-scales. A total DSM-IV ADHD symptoms subscale was formed by adding up items from the two subscales. In a few cases, missing data in Conners’ scales were pro-rated: a summary score based on the mean of individual questions on the rest of the subscale was used if there was more than 75% completion for each subscale. Of those with MIDA data (N=1210), 1208 had Conners’ Parent Rating Scale data available, and 1064 had Conners’ Teacher Rating Scale data. Parent and teacher ratings on each subscale were combined by summating scores.
Data analyses
Details regarding data analysis can be found in the supplementary digital content (online only) materials at http://links.lww.com/admin/xxx. Negative binomial regression (NBREG) models were used to assess the unique contribution of each ADHD symptom dimension (including the other dimension as a covariate) or extreme group membership in predicting the number of times participants selected smaller-immediate rewards, after controlling for age (model I) or age and IQ (model II). To facilitate comparisons between predictors we used standardised scores for ADHD symptoms. The incident rate ratio (IRR) expresses the factor by which the expected number of smaller-immediate reward choices changes for a change of 1 SD in the predictor (dimensional analyses), or with membership in one of the extreme groups.36 To facilitate interpretation, we calculated the discrete change in the percentage of times the smaller-immediate reward was selected per 1 SD change in symptom scores (or with extreme group membership), holding all other variables at their means. As a further aid, discrete change is also expressed as the raw number by which the smaller-immediate reward choices were expected to change for a typical participant who completed 20 trials. To test the delay aversion specific hypothesis, we used IDA scores, which were normally distributed, in linear regression models. All analyses were conducted using STATA (release 9.2, STATA Corporation, College Station, TX, USA), and corrections were applied for the cluster-correlated nature of our data (twin pairs).
For the categorical analyses (male participants), we used the 95th percentile on each symptom dimension as our threshold (it is close to the estimated prevalence rates of ADHD in the UK37, 38) to define three extreme groups: (i) ADHD-IN (N=32), including participants who scored in the top 5% on inattention ratings, but below the top 5% on hyperactivity-impulsivity ratings; (ii) ADHD-H/I (N=25), consisting of participants who scored in the top 5% on hyperactivity-impulsivity ratings but below the top 5% on inattention ratings; (iii) ADHD-CO (N=19), comprising participants who scored in the top 5% on both inattention and hyperactivity-impulsivity ratings. These groups resemble the DSM-IV inattentive, hyperactive/impulsive and combined ADHD subtypes respectively, but only in terms of presence of symptoms, as information regarding the age of onset, pervasiveness, duration and impact of ADHD symptoms needs additionally to be taken into account for a clinical diagnosis.
RESULTS
Subgroup characteristics
Boys and girls did not differ in age or IQ, but girls had lower ratings on both ADHD symptom dimensions. Additional information can be found in the supplementary digital content (online only) materials at http://links.lww.com/admin/xxx. There were no significant differences in age or IQ between the extreme groups and the rest of the sample in the categorical analyses. Table A can be found in the supplementary digital content (online only) materials at http://links.lww.com/admin/xxx.
Gender differences in choice impulsivity and delay aversion
Girls showed a higher percentage of smaller-immediate reward choices both in the post-reward delay (boys: M=13.25, SD=18.28; girls: M=17.3, SD=18.89; F(1, 568)=10.49, p=.001, R2=.01) and the no post-reward delay (boys: M=27.94, SD=29.71; girls: M=32.65, SD=26.21; F(1, 568)=7.24, p=.007, R2=.01) conditions, but did not differ from boys on the IDA (F(1, 568)=0.21, p=.65).
Dimensional analyses
Choice impulsivity
Inattention significantly predicted preference for smaller-immediate rewards after controlling for hyperactivity-impulsivity and age in both task conditions and for both gender groups (Table 1, model I). An increase of one SD in inattention increased the expected percentage of times a smaller-immediate reward was selected by 2.41-5.46 points in boys and 4.35-7.01 points in girls, in the post- and no post-reward delay conditions respectively. This translated to an expected increase of 0.48-1.40 in the number of times a typical participant selected the smaller-immediate reward per one SD increase in inattention scores. Controlling for IQ attenuated this effect but it remained significant, except for boys in the post-reward delay condition (Table 1, model II).
Table 1.
Model I Controlling for other symptom dimension and age |
Model II Controlling for other symptom dimension, age & IQ |
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---|---|---|---|---|---|---|---|---|---|---|
|
|
|||||||||
IRR1 | SE2 | p | IRR 95% CI3 | Discrete change %points (rewards) 4 |
IRR1 | SE2 | p | IRR 95% CI3 | Discrete change %points (rewards) 4 |
|
Post-Reward Delay condition | ||||||||||
Males | ||||||||||
Inattention 5 | 1.21 | 0.086 | .008 | (1.05, 1.39) |
2.41 (0.48) | 1.11 | 0.080 | .16 | (0.96, 1.28) | 1.19 (0.24) |
Hyperactivity/impulsivi
ty 5 |
0.99 | 0.067 | .83 | (0.86, 1.13) |
−0.18 (−0.04) | 1.03 | 0.071 | .70 | (0.90, 1.18) | 0.31 (0.06) |
| ||||||||||
Total ADHD
symptoms 5 |
1.16 | 0.067 | .006 | (1.05, 1.31) |
2.00 (0.40) | 1.12 | 0.064 | 0.44 | (1.00, 1.26) | 1.34 (0.27) |
Females | ||||||||||
Inattention 5 | 1.25 | 0.104 | .007 | (1.06, 1.47) |
4.35 (0.87) | 1.18 | 0.093 | .036 | (1.01, 1.38) | 2.99 (0.60) |
Hyperactivity/impulsivi
ty 5 |
0.79 | 0.075 | .013 | (0.66, 0.95) |
−3.23 (−0.65) | 0.77 | 0.069 | .004 | (0.65, 0.92) | −3.37 (−0.67) |
| ||||||||||
Total ADHD
symptoms 5 |
1.01 | 0.070 | .84 | (0.89, 1.16) |
0.00 (0.00) | 0.94 | 0.065 | .37 | (0.82, 1.08) | −0.94 (−0.19) |
No post-Reward Delay condition | ||||||||||
Males | ||||||||||
Inattention 5 | 1.22 | 0.063 | < .001 | (1.10, 1.35) |
5.46 (1.09) | 1.18 | 0.061 | .002 | (1.06, 1.30) | 4.27 (0.85) |
Hyperactivity/impulsivi
ty 5 |
0.97 | 0.052 | .57 | (0.87, 1.08) |
−0.80 (−0.16) | 0.97 | 0.053 | .63 | (0.88, 1.08) | −0.67 (−0.13) |
| ||||||||||
Total ADHD
symptoms 5 |
1.17 | 0.050 | <.001 | (1.08, 1.27) |
4.28 (0.86) | 1.13 | 0.049 | .003 | (1.04, 1.23) | 3.31 (0.66) |
Females | ||||||||||
Inattention 5 | 1.21 | 0.075 | .002 | (1.07, 1.36) |
7.01 (1.40) | 1.16 | 0.070 | .011 | (1.04, 1.31) | 5.43 (1.09) |
Hyperactivity/impulsivi
ty 5 |
0.91 | 0.060 | .16 | (0.80, 1.04) |
−2.81 (−0.56) | 0.90 | 0.058 | .10 | (0.79, 1.02) | −3.08 (−0.62) |
| ||||||||||
Total ADHD
symptoms 5 |
1.10 | 0.055 | .059 | (1.00, 1.21) |
3.31 (0.66) | 1.05 | 0.053 | .32 | (0.95, 1.16) | 1.68 (0.34) |
Note: Negative binomial regression models have been used to examine the unique contribution of each symptom dimension or total ADHD scores to choice impulsivity under each task condition, controlling for age (model I) or age and IQ (model II).
Incidence rate ratio.
Robust standard error.
Confidence intervals.
Expected change in preference for smaller-immediate rewards per 1 SD change in symptom scores, holding all other variables at their means, in terms of either percentage points or raw rewards for a typical participant.
Standardised scores. MIDA: Maudsley Index of Childhood Delay Aversion.
Hyperactivity-impulsivity did not significantly predict choice impulsivity after controlling for inattention symptoms and age, except for girls in the post-reward delay condition (Table 1). This effect was similar in size, but opposite in direction, to that of inattention, and was maintained after controlling for IQ.
Total ADHD symptom scores showed a significant but attenuated association with choice impulsivity relative to inattention scores in boys, but no association in girls (Table 1). This reflects the opposite in direction association of inattention and hyperactivity-impulsivity symptoms with choice impulsivity.
Index of delay aversion
Inattention (but not hyperactivity-impulsivity) ratings uniquely predicted IDA scores in boys, after controlling for age and hyperactivity-impulsivity symptoms, increasing R2 by 0.013, a small yet significant effect (Table 2, top). The association was attenuated but still significant after controlling for IQ. Neither symptom dimension significantly predicted IDA scores in girls.
Table 2.
Model I. Predictors: Age, Inattention, Hyperactivity/impulsivity |
Model II. Predictors: IQ, Age, Inattention, Hyperactivity/impulsivity |
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---|---|---|---|---|---|---|---|---|---|---|
|
|
|||||||||
b | SE1 | p | 95% CI2 | ΔR2 3 | b | SE1 | p | 95% CI2 | ΔR2 3 | |
Males | ||||||||||
Inattention 4 | 3.30 | 1.23 | .008 | (0.87, 5.73) | .013 | 2.93 | 1.23 | .018 | (0.51, 5.35) | .009 |
Hyperactivity/impulsiv ity 4 |
−1.10 | 1.06 | .30 | (−3.18, 0.98) | .001 | −0.99 | 1.05 | .35 | (−3.05, 1.07) | .001 |
Model I R2=.029, F(3,371)=5.47, p=.001 | Model II R2=.037, F(4,371)=5.44, p<.001 | |||||||||
Females | ||||||||||
Inattention 4 | 1.86 | 1.49 | .21 | (−1.07, 4.79) | .003 | 1.71 | 1.52 | .26 | (−1.27, 4.69) | .003 |
Hyperactivity/impulsiv
ity 4 |
1.23 | 1.44 | .39 | (−1.59, 4.05) | .001 | 1.23 | 1.44 | .39 | (−1.60, 4.05) | .001 |
Model I R2=.010, F(3,364)=1.65, p=.18 | Model II R2=.011, F(4,364)=1.28, p=.28 |
Model I. Predictors: Age, total ADHD symptoms | Model II. Predictors: IQ, Age, total ADHD symptoms | |||||||||
---|---|---|---|---|---|---|---|---|---|---|
b | SE 1 | p | 95% CI 2 | ΔR2 3 | b | SE 1 | p | 95% CI 2 | ΔR2 3 | |
Males | ||||||||||
Total ADHD
symptoms 4 |
2.01 | 0.90 | .025 | (0.25, 3.78) | .008 | 1.77 | 0.88 | .046 | (0.03, 3.50) | .006 |
Model I R2=.029, F(2,371)=6.90, p=.001 | Model I R2=.032, F(3,371)=6.45, p<.001 | |||||||||
| ||||||||||
Females | ||||||||||
Total ADHD
symptoms 4 |
2.80 | 1.33 | .036 | (0.18, 5.42) | .009 | 2.66 | 1.32 | .046 | (0.06, 5.27) | .008 |
Model I R2=.010, F(2,364)=2.49, p=.084 | Model I R2=.011, F(3,364)=1.71, p=.17 |
Note: Linear regression has been used to examine the unique contributions of each symptom dimension or total ADHD scores to the prediction of index of delay aversion (IDA) scores, controlling for age (Model I) or age and IQ (Model II).
Robust standard error.
Confidence intervals
R2 change after adding the specific predictor in a model containing the remaining predictors.
Standardised scores.
Total ADHD symptom scores showed a significant but attenuated association with IDA relative to inattention scores in boys (Table 2, bottom). A similar association was observed in girls, although the model was not significant. This reflects the fact that both inattention and hyperactivity-impulsivity scores showed a non-significant but positive association with IDA in girls.
Categorical analyses (male participants)
Choice impulsivity
Membership in the group defined in terms of extreme inattention ratings (ADHD-IN) predicted a significant increase in choice impulsivity in the no post-reward delay condition. Membership in any of the other groups did not predict choice impulsivity in either condition (Table 3).
Table 3.
Extreme group (top 5%) |
n (total) | IRR1 | SE2 | p | IRR 95% CI3 | Discrete change %points (rewards)4 |
---|---|---|---|---|---|---|
Post-reward delay condition | ||||||
ADHD-IN 5 | 32(542) | 1.15 | 0.28 | .57 | (0.71, 1.84) | 1.94 (0.39) |
ADHD-H/I 6 | 25(542) | 1.05 | 0.30 | .87 | (0.60, 1.84) | 0.64 (0.13) |
ADHD-CO 7 | 19(542) | 1.37 | 0.35 | .21 | (0.83, 2.26) | 4.88 (0.98) |
No post-reward delay condition | ||||||
ADHD-IN 5 | 32(542) | 1.45 | 0.22 | .015 | (1.07, 1.97) | 12.33 (2.47) |
ADHD-H/I 6 | 25(542) | 0.99 | 0.21 | .98 | (0.66, 1.51) | −0.14 (−0.03) |
ADHD-CO 7 | 19(542) | 1.32 | 0.24 | .12 | (0.93, 1.88) | 8.95 (1.79) |
Note: Negative binomial regression models have been used to examine whether extreme group membership can predict choice impulsivity under each task condition.
Incidence rate ratio.
Robust standard error.
Confidence intervals.
Expected change in preference for smaller-immediate rewards with extreme group membership expressed in percentage points or raw rewards for a typical participant.
ADHD-Inattentive extreme group.
ADHD-Hyperactive/impulsive extreme group.
ADHD-Combined subtype extreme group. MIDA: Maudsley Index of Childhood Delay Aversion.
Index of delay aversion
Only membership in the ADHD-IN group was positively associated with IDA scores, accounting for 0.9% of the variance (Table 4).
Table 4.
Extreme group (top 5%) |
n (total) | b | SE1 | p | 95% CI2 | R2 |
---|---|---|---|---|---|---|
ADHD-IN 3 | 32(542) | 10.39 | 4.94 | .036 | (0.68, 20.10) | 0.009 |
ADHD-H/I 4 | 25(542) | −0.81 | 3.76 | .83 | (−8.20, 6.58) | 0.000 |
ADHD-CO 5 | 19(542) | 4.08 | 5.46 | .46 | (−6.65, 14.81) | 0.001 |
Note: Linear regression has been used to examine whether extreme group membership can predict index of delay aversion (IDA) scores.
Robust standard error.
Confidence intervals.
ADHD-Inattentive extreme group.
ADHD-Hyperactive/impulsive extreme group.
ADHD-Combined subtype extreme group.
DISCUSSION
Currently, some ambiguity surrounds the term “delay aversion”. It has been used both in a descriptive capacity, to denote the preference for smaller-immediate over larger-delayed rewards (or the steeper discounting of rewards as a function of time to delivery), which we named choice impulsivity to avoid confusion, and to refer to an acquired motivational tendency postulated by delay aversion theory as an explanatory construct contributing to choice impulsivity.
This is the first study to examine choice impulsivity and the delay aversion construct in relation to ADHD symptoms using a large population sample. Choice impulsivity showed a small yet significant association with inattention (controlling for hyperactivity-impulsivity and age). This association was observed in both task conditions, was similar across genders, and remained significant but was attenuated after controlling for IQ (except for boys in the post-reward delay condition). In the categorical analyses, boys with high inattention ratings chose more smaller-immediate rewards when this reduced overall task length.
Unexpectedly, the association between hyperactivity-impulsivity and choice impulsivity was context- and gender-specific. For girls in the post-reward delay condition, higher levels of hyperactivity-impulsivity were associated with reduced smaller-immediate reward choices. This association was similar in size but opposite in direction compared to inattention ratings. In boys there was no association between hyperactivity-impulsivity and choice impulsivity.
Turning to the predictions stemming from the revised delay aversion theory,10,25 we observed a small yet significant association between inattention ratings and the index of delay aversion in boys only (controlling for hyperactivity-impulsivity and age). Adding inattention ratings in the model increased the explained variance by 1.3% (0.9% after controlling for IQ). The categorical analyses yielded similar results; boys in the inattentive subgroup showed an increase in IDA scores, accounting for 0.9% of the explained variance.
This is the first study to show that, in a large general population sample of school-aged children, choice impulsivity and a derivative measure reflecting the motivational construct of “delay aversion” (IDA) may be associated with inattention rather than hyperactivity-impulsivity ratings. This is not entirely unexpected since delay aversion theory makes no prediction for a preferential association with either symptom dimension3 and existing research, while scant, does not point to a clear direction. A previous study with similarly aged children with combined subtype ADHD found a moderate correlation between choice impulsivity and teacher hyperactivity-impulsivity ratings,12 while a study with pre-school children reported similar correlations between both inattentive and hyperactive-impulsive symptom dimensions and choice impulsivity.17 Another study using a young adult population sample has reported an association between a measure of temporal discounting and hyperactivity-impulsivity only.18 At the behavioural level, choice impulsivity has been positively associated with gross motor behaviour in children with ADHD,12,13 but dissociated from hyperactivity in rodents.39
Future research needs to clarify the extent to which the stronger association of behavioural measures of choice impulsivity and delay aversion with inattention rather than hyperactivity-impulsivity ratings reflects true relations between underlying processes, or an artefact resulting from different levels, or inadequate methods, of measurement. The DSM-IV diagnostic criteria are not operational definitions of precise cognitive processes such as inattention and impulsivity. For instance, DSM-IV “inattention” symptoms may also capture aspects of impulsivity40 and data-driven approaches to subtype definition have identified an inattentive-impulsive class.41 Moreover, questionnaire- and laboratory-based measures of impulsivity do not necessarily associate well, reflecting different levels of analysis.42,43
The observed association between inattention symptoms and a measure of delay aversion (IDA) in the current general population study is consistent with recent evidence from a large sample of clinically ascertained probands with DSM-IV combined subtype ADHD and controls which used the same task.25 The current study further suggests that the association between ADHD and delay aversion may be stronger in boys, and driven by a stronger association with inattention symptoms; a finding that is yet to be confirmed with a clinically ascertained sample. The differential association of inattention and hyperactivity-impulsivity ratings with choice impulsivity/delay aversion in the current study is consistent with research in other areas44 which suggests a possible separation of underlying processes. Our results encourage the separate examination of the two ADHD symptom dimensions, for which purpose general population samples are ideal. The lack of a threshold effect demarcating the top 5% groups is consistent with the idea that ADHD symptoms are quantitative traits distributed continuously in the population and that ADHD represents the tail of this distribution.
The use of secondary reinforcers may be a limitation of the choice-delay paradigm as it has been used to date, reducing its sensitivity to capture the full range of individual differences in choice impulsivity. This may particularly apply in the post-reward delay condition: the lack of a truly immediate effect for the smaller-immediate reward might deprive it from its single advantage in this condition, namely, the gratification of the impulsive drive for an immediate effect. This could also affect the measurement of delay aversion, as the IDA is a relative measure based on the score difference between the two conditions. Given the inherent difficulties in the use of primary reinforcers, these issues could be addressed in future research through the direct assessment of delay aversion independently from choice impulsivity, by obtaining some physiological index of emotional reactivity to delays (e.g. reactivity of the amygdala, see45).This would allow the independent assessment of primary (choice impulsivity) and secondary (delay aversion) manifestations of the underlying aetiology, as well as of their association to ADHD symptoms and to each other. Delay aversion is a developmental concept; it has been thought to emerge over time, progressively leading to “an elaboration of symptoms from impulsiveness to inattentiveness and overactivity”.3 Choice impulsivity and delay aversion are interrelated, as the latter is proposed to be the product of the interaction of environmental factors with the former.3 Their relation will likely be a complex one, with reciprocal, feed-forward and feedback pathways, and to be assessed it will require independent measures of each variable and longitudinal data.
Based on existing data, the acquired motivational tendency to avoid delays (delay aversion) contributes only minimally to ADHD, perhaps in a gender specific-manner; it explains no more than 0.9-2.7% of the variance, depending on the nature of the sample. Therefore, a reappraisal of ADHD symptoms and choice impulsivity as instances of adaptive behaviour, or preferences, which aim to reduce delays or their psychological impact2, might be necessary.
Choice impulsivity is a commonly observed behavioural phenomenon5,46 which is neurobiologically and behaviourally dissociable from other impulsivity facets (e.g. impulsive disinhibition, measured with the stop signal paradigm) in both animals and humans.39,43,47-50 The association of choice impulsivity with ADHD is more consistent and robust, reflecting moderate effect sizes reported to range from d=0.57 to d=0.7110; a formal meta-analysis with explicit criteria is yet to be published. These estimates are comparable to those reported for executive function measures, ranging from Cohen’s d=0.46 to d=1.16.51,52 These findings warrant focusing research interest on the primary, constitutional processes which manifest as choice impulsivity (and eventually may lead to the secondary acquisition of aversion to delays), as a possible aetiological factor contributing to ADHD. Existing theoretical models link the development of ADHD symptoms to a constitutional dysfunction in the dopamine-based brain circuitry which underpins reinforcement learning and reward processing.23,24,53 Choice impulsivity has been directly linked to dopamine function54, and associated with activation in the mesolimbic reward processing circuitry (e.g.55,56) which is dysfunctional in ADHD (e.g.57). The constitutional nature of this dysfunction is consistent with the high heritability of ADHD,58 but lends itself to early behavioural interventions (e.g.53) and pharmacological treatment which may positively influence an organism’s developmental pathway and hinder or subdue the development of ADHD symptoms and associated behaviours.
Supplementary Material
Acknowledgments
The Study of Activity and Impulsivity Levels in children (SAIL) is funded by a project grant from the Wellcome Trust (GR070345MF).
Thank you to all who make this research possible: the TEDS-SAIL families, who give their time and support so unstintingly; Rebecca Gibbs, Hannah Rogers, Eda Salih, Greer Swinard, Kate Lievesley, Kayley O’Flynn, Suzi Marquis and Rebecca Whittemore; and everyone on the TEDS team.
Footnotes
Supplemental digital content for this article can be found online only. See text for specific link.
Disclosure: Mr. Paloyelis is supported by a Ph.D. Studentship from the Medical Research Council, UK. Dr. Asherson is on the speakers’ bureau of and is a consultant to Janssen-Cilag, Eli Lilly & Company, Shire, and Flynn Pharma. He is further supported by the Medical Research Council, the Wellcome Trust, and the National Institute of Health Research. Dr. Kuntsi receives additional support from the Medical Research Council.
REFERENCES
- 1.Sonuga-Barke EJS. Psychological heterogeneity in AD/HD - A dual pathway model of behaviour and cognition. Behav. Brain Res. 2002;130(1-2):29–36. doi: 10.1016/s0166-4328(01)00432-6. [DOI] [PubMed] [Google Scholar]
- 2.Sonuga-Barke EJS, Taylor E, Sembi S, Smith J. Hyperactivity and delay aversion-I. The effect of delay on choice. J. Child Psychol. Psychiatry. 1992;33(2):387–398. doi: 10.1111/j.1469-7610.1992.tb00874.x. [DOI] [PubMed] [Google Scholar]
- 3.Sonuga-Barke EJS. Causal models of attention-deficit/hyperactivity disorder: From common simple deficits to multiple developmental pathways. Biol. Psychiatry. 2005;57(11):1231–1238. doi: 10.1016/j.biopsych.2004.09.008. [DOI] [PubMed] [Google Scholar]
- 4.Rachlin H, Green L. Commitment, choice and self-control. J. Exp. Anal. Behav. 1972;17(1):15–22. doi: 10.1901/jeab.1972.17-15. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Logue AW. Research on self-control: An integrating framework. Behav. Brain Sci. 1988;11(4):665–709. [Google Scholar]
- 6.Dalen L, Sonuga-Barke EJS, Hall M, Remington B. Inhibitory deficits, delay aversion and preschool AD/HD: Implications for the dual pathway model. Neural Plas. 2004;11(1-2):1–11. doi: 10.1155/NP.2004.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Barkley RA. Behavioral inhibition, sustained attention, and executive functions: constructing a unifying theory of ADHD. Psychol. Bull. 1997;121(1):65–94. doi: 10.1037/0033-2909.121.1.65. [DOI] [PubMed] [Google Scholar]
- 8.Tripp G, Alsop B. Sensitivity to reward delay in children with attention deficit hyperactivity disorder (ADHD) J. Child Psychol. Psychiatry. 2001;42(5):691–698. [PubMed] [Google Scholar]
- 9.Schweitzer JB, Sulzer-Azaroff B. Self-control in boys with attention deficit hyperactivity disorder: effects of added stimulation and time. J. Child Psychol. Psychiatry. 1995;36(4):671–686. doi: 10.1111/j.1469-7610.1995.tb02321.x. [DOI] [PubMed] [Google Scholar]
- 10.Sonuga-Barke EJS, Sergeant JA, Nigg J, Willcutt E. Executive Dysfunction and Delay Aversion in Attention Deficit Hyperactivity Disorder: Nosologic and Diagnostic Implications. Child Adolesc. Psychiatr. Clin. N. Am. 2008;17(2):367–384. doi: 10.1016/j.chc.2007.11.008. [DOI] [PubMed] [Google Scholar]
- 11.Antrop I, Stock P, Verte S, Wiersema JR, Baeyens D, Roeyers H. ADHD and delay aversion: The influence of non-temporal stimulation on choice for delayed rewards. J. Child Psychol. Psychiatry. 2006;47(11):1152–1158. doi: 10.1111/j.1469-7610.2006.01619.x. [DOI] [PubMed] [Google Scholar]
- 12.Solanto MV, Abikoff H, Sonuga-Barke E, et al. The ecological validity of delay aversion and response inhibition as measures of impulsivity in AD/HD: A supplement to the NIMH multimodal treatment study of AD/HD. J. Abnorm. Child Psychol. 2001;29(3):215–228. doi: 10.1023/a:1010329714819. [DOI] [PubMed] [Google Scholar]
- 13.Hoerger ML, Mace FC. A computerized test of self-control predicts classroom behavior. J. Appl. Behav. Anal. 2006;39(2):147–159. doi: 10.1901/jaba.2006.171-04. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14.Kuntsi J, Oosterlaan J, Stevenson J. Psychological mechanisms in hyperactivity: I Response inhibition deficit, working memory impairment, delay aversion, or something else? J. Child Psychol. Psychiatry. 2001;42(2):199–210. [PubMed] [Google Scholar]
- 15.Neef NA, Marckel J, Ferreri SJ, et al. Behavioral assessment of impulsivity: a comparison of children with and without attention deficit hyperactivity disorder. J. Appl. Behav. Anal. 2005;38(1):23–37. doi: 10.1901/jaba.2005.146-02. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.Sonuga-Barke EJS, Dalen L, Remington B. Do executive deficits and delay aversion make independent contributions to preschool attention-deficit/hyperactivity disorder symptoms? J. Am. Acad. Child Adolesc. Psychiatry. 2003;42(11):1335–1342. doi: 10.1097/01.chi.0000087564.34977.21. [DOI] [PubMed] [Google Scholar]
- 17.Thorell LB. Do delay aversion and executive function deficits make distinct contributions to the functional impact of ADHD symptoms? A study of early academic skill deficits. J. Child Psychol. Psychiatry. 2007;48(11):1061–1070. doi: 10.1111/j.1469-7610.2007.01777.x. [DOI] [PubMed] [Google Scholar]
- 18.Scheres A, Lee A, Sumiya M. Temporal reward discounting and ADHD: Task and symptom specific effects. J. Neural Transm. 2008;115(2):221–226. doi: 10.1007/s00702-007-0813-6. [DOI] [PubMed] [Google Scholar]
- 19.Bidwell LC, Willcutt EG, DeFries JC, Pennington BF. Testing for Neuropsychological Endophenotypes in Siblings Discordant for Attention-Deficit/Hyperactivity Disorder. Biol. Psychiatry. 2007;62(9):991–998. doi: 10.1016/j.biopsych.2007.04.003. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.Solanto MV, Gilbert SN, Raj A, et al. Neurocognitive functioning in AD/HD, predominantly inattentive and combined subtypes. J. Abnorm. Child Psychol. 2007;35(5):729–744. doi: 10.1007/s10802-007-9123-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Scheres A, Dijkstra M, Ainslie E, et al. Temporal and probabilistic discounting of rewards in children and adolescents: effects of age and ADHD symptoms. Neuropsychologia. 2006;44(11):2092–2103. doi: 10.1016/j.neuropsychologia.2005.10.012. [DOI] [PubMed] [Google Scholar]
- 22.Barkley RA, Edwards G, Laneri M, Fletcher K, Metevia L. Executive functioning, temporal discounting, and sense of time in adolescents with attention deficit hyperactivity disorder (ADHD) and oppositional defiant disorder (ODD) J. Abnorm. Child Psychol. 2001;29(6):541–556. doi: 10.1023/a:1012233310098. [DOI] [PubMed] [Google Scholar]
- 23.Sagvolden T, Johansen EB, Aase H, Russell VA. A dynamic developmental theory of attention-deficit/hyperactivity disorder (ADHD) predominantly hyperactive/impulsive and combined subtypes. Behav. Brain Sci. 2005;28(3):397–419. doi: 10.1017/S0140525X05000075. [DOI] [PubMed] [Google Scholar]
- 24.Tripp G, Wickens JR. Research review: dopamine transfer deficit: a neurobiological theory of altered reinforcement mechanisms in ADHD. J. Child Psychol. Psychiatry. 2008;49(7):691–704. doi: 10.1111/j.1469-7610.2007.01851.x. [DOI] [PubMed] [Google Scholar]
- 25.Marco R, Miranda A, Schlotz W, et al. Delay and reward choice in ADHD: an experimental test of the role of delay aversion. Neuropsychology. 2009;23:367–380. doi: 10.1037/a0014914. [DOI] [PubMed] [Google Scholar]
- 26.Levine TR, Hullett CR. Eta squared, Partial Eta squared, and Misreporting of Effect Size in Communication Research. Human Communication Research. 2002;28(4):612–625. [Google Scholar]
- 27.Tabachnick BG, Fidell LS. Using Multivariate Statistics. 5th ed Pearson; New York: 2007. [Google Scholar]
- 28.Chen W, Zhou K, Sham P, et al. DSM-IV combined type ADHD shows familial association with sibling trait scores: A sampling strategy for QTL linkage. Am J Med Genet B Neuropsychiatr Genet. 2008 doi: 10.1002/ajmg.b.30672. [DOI] [PubMed] [Google Scholar]
- 29.McLoughlin G, Ronald A, Kuntsi J, Asherson P, Plomin R. Genetic support for the dual nature of attention deficit hyperactivity disorder: substantial genetic overlap between the inattentive and hyperactive-impulsive components. J. Abnorm. Child Psychol. 2007;35(6):999–1008. doi: 10.1007/s10802-007-9149-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 30.Steinberg L, Graham S, O’Brien L, Woolard J, Cauffman E, Banich M. Age differences in future orientation and delay discounting. Child Dev. 2009;80(1):28–44. doi: 10.1111/j.1467-8624.2008.01244.x. [DOI] [PubMed] [Google Scholar]
- 31.Kuntsi J, Rogers H, Swinard G, et al. Reaction time, inhibition, working memory and ’delay aversion’ performance: genetic influences and their interpretation. Psychol. Med. 2006;36(11):1613–1624. doi: 10.1017/S0033291706008580. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 32.Trouton A, Spinath FM, Plomin R. Twins early development study (TEDS): a multivariate, longitudinal genetic investigation of language, cognition and behavior problems in childhood. Twin Res. 2002;5(5):444–448. doi: 10.1375/136905202320906255. [DOI] [PubMed] [Google Scholar]
- 33.Wechsler D. Wechsler Intelligence Scale for Children. 3rd ed The Psychological Corporation; London: 1991. [Google Scholar]
- 34.Conners CK, Sitarenios G, Parker JD, Epstein JN. The revised Conners’ Parent Rating Scale (CPRS-R): factor structure, reliability, and criterion validity. J. Abnorm. Child Psychol. 1998;26(4):257–268. doi: 10.1023/a:1022602400621. [DOI] [PubMed] [Google Scholar]
- 35.Conners CK, Sitarenios G, Parker JD, Epstein JN. Revision and restandardization of the Conners Teacher Rating Scale (CTRS-R): factor structure, reliability, and criterion validity. J. Abnorm. Child Psychol. 1998;26(4):279–291. doi: 10.1023/a:1022606501530. [DOI] [PubMed] [Google Scholar]
- 36.Long JS, Freese J. Regression Models for Categorical Dependent variables Using Stata. 2nd ed STATA Press; College Station, Texas: 2006. [Google Scholar]
- 37.Ford T, Goodman R, Meltzer H. The British Child and Adolescent Mental Health Survey 1999: the prevalence of DSM-IV disorders. J. Am. Acad. Child Adolesc. Psychiatry. 2003;42(10):1203–1211. doi: 10.1097/00004583-200310000-00011. [DOI] [PubMed] [Google Scholar]
- 38.Polanczyk G, de Lima MS, Horta BL, Biederman J, Rohde LA. The worldwide prevalence of ADHD: a systematic review and metaregression analysis. Am. J. Psychiatry. 2007;164(6):942–948. doi: 10.1176/ajp.2007.164.6.942. [DOI] [PubMed] [Google Scholar]
- 39.Dalley JW, Fryer TD, Brichard L, et al. Nucleus accumbens D2/3 receptors predict trait impulsivity and cocaine reinforcement. Science. 2007;315(5816):1267–1270. doi: 10.1126/science.1137073. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 40.Evenden JL. Varieties of impulsivity. Psychopharmacology (Berl) 1999;146(4):348–361. doi: 10.1007/pl00005481. [DOI] [PubMed] [Google Scholar]
- 41.Rasmussen ER, Neuman RJ, Heath AC, Levy F, Hay DA, Todd RD. Replication of the latent class structure of Attention-Deficit/Hyperactivity Disorder (ADHD) subtypes in a sample of Australian twins. J. Child Psychol. Psychiatry. 2002;43(8):1018–1028. doi: 10.1111/1469-7610.00229. [DOI] [PubMed] [Google Scholar]
- 42.Krishnan-Sarin S, Reynolds B, Duhig AM, et al. Behavioral impulsivity predicts treatment outcome in a smoking cessation program for adolescent smokers. Drug Alcohol Depend. 2007;88(1):79–82. doi: 10.1016/j.drugalcdep.2006.09.006. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 43.Reynolds B, Penfold RB, Patak M. Dimensions of impulsive behavior in adolescents: laboratory behavioral assessments. Exp Clin Psychopharmacol. 2008;16(2):124–131. doi: 10.1037/1064-1297.16.2.124. [DOI] [PubMed] [Google Scholar]
- 44.Willcutt EG, Pennington BF, Olson RK, DeFries JC. Understanding comorbidity: a twin study of reading disability and attention-deficit/hyperactivity disorder. Am J Med Genet B Neuropsychiatr Genet. 2007;144B(6):709–714. doi: 10.1002/ajmg.b.30310. [DOI] [PubMed] [Google Scholar]
- 45.Plichta MM, Vasic N, Wolf RC, et al. Neural hyporesponsiveness and hyperresponsiveness during immediate and delayed reward processing in adult attention-deficit/hyperactivity disorder. Biol. Psychiatry. 2009;65(1):7–14. doi: 10.1016/j.biopsych.2008.07.008. [DOI] [PubMed] [Google Scholar]
- 46.Green L, Myerson J. A discounting framework for choice with delayed and probabilistic rewards. Psychol. Bull. 2004;130(5):769–792. doi: 10.1037/0033-2909.130.5.769. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 47.Cardinal RN, Pennicott DR, Sugathapala CL, Robbins TW, Everitt BJ. Impulsive choice induced in rats by lesions of the nucleus accumbens core. Science. 2001;292(5526):2499–2501. doi: 10.1126/science.1060818. [DOI] [PubMed] [Google Scholar]
- 48.Eagle DM, Robbins TW. Lesions of the medial prefrontal cortex or nucleus accumbens core do not impair inhibitory control in rats performing a stop-signal reaction time task. Behav. Brain Res. 2003;146(1-2):131–144. doi: 10.1016/j.bbr.2003.09.022. [DOI] [PubMed] [Google Scholar]
- 49.Reynolds B, Ortengren A, Richards JB, de Wit H. Dimensions of impulsive behavior: Personality and behavioral measures. Personality and Individual Differences. 2006;40(2):305–315. [Google Scholar]
- 50.Robinson ES, Eagle DM, Economidou D, et al. Behavioural characterisation of high impulsivity on the 5-choice serial reaction time task: Specific deficits in ‘waiting’ versus ‘stopping’. Behav. Brain Res. 2009;196(2):310–316. doi: 10.1016/j.bbr.2008.09.021. [DOI] [PubMed] [Google Scholar]
- 51.Martinussen R, Hayden J, Hogg-Johnson S, Tannock R. A meta-analysis of working memory impairments in children with attention-deficit/hyperactivity disorder. J. Am. Acad. Child Adolesc. Psychiatry. 2005;44(4):377–384. doi: 10.1097/01.chi.0000153228.72591.73. [DOI] [PubMed] [Google Scholar]
- 52.Willcutt EG, Doyle AE, Nigg JT, Faraone SV, Pennington BF. Validity of the executive function theory of attention-deficit/hyperactivity disorder: a meta-analytic review. Biol. Psychiatry. 2005;57(11):1336–1346. doi: 10.1016/j.biopsych.2005.02.006. [DOI] [PubMed] [Google Scholar]
- 53.Johansen EB, Killeen PR, Russell VA, et al. Origins of altered reinforcement effects in ADHD. Behav Brain Funct. 2009;5:7. doi: 10.1186/1744-9081-5-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 54.Kobayashi S, Schultz W. Influence of reward delays on responses of dopamine neurons. J. Neurosci. 2008;28(31):7837–7846. doi: 10.1523/JNEUROSCI.1600-08.2008. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 55.Ballard K, Knutson B. Dissociable neural representations of future reward magnitude and delay during temporal discounting. Neuroimage. 2009;45(1):143–150. doi: 10.1016/j.neuroimage.2008.11.004. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 56.Hariri AR, Brown SM, Williamson DE, Flory JD, de Wit H, Manuck SB. Preference for immediate over delayed rewards is associated with magnitude of ventral striatal activity. J. Neurosci. 2006;26(51):13213–13217. doi: 10.1523/JNEUROSCI.3446-06.2006. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 57.Scheres A, Milham MP, Knutson B, Castellanos FX. Ventral striatal hyporesponsiveness during reward anticipation in attention-deficit/hyperactivity disorder. Biol. Psychiatry. 2007;61(5):720–724. doi: 10.1016/j.biopsych.2006.04.042. [DOI] [PubMed] [Google Scholar]
- 58.Faraone SV, Perlis RH, Doyle AE, et al. Molecular genetics of attention-deficit/hyperactivity disorder. Biol. Psychiatry. 2005;57(11):1313–1323. doi: 10.1016/j.biopsych.2004.11.024. [DOI] [PubMed] [Google Scholar]
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