Elsevier

Cortex

Volume 106, September 2018, Pages 164-173
Cortex

Research Report
Waiting and working for rewards: Attention-Deficit/Hyperactivity Disorder is associated with steeper delay discounting linked to amygdala activation, but not with steeper effort discounting

https://doi.org/10.1016/j.cortex.2018.05.018Get rights and content

Abstract

Objective

Children and adolescents with ADHD have a relatively strong preference for smaller immediate rewards over larger delayed rewards (steep delay discounting). It is unknown whether such steep discounting of rewards is specific for delayed rewards, i.e., supporting the delay aversion account of ADHD, or whether it is also present for effortful rewards, i.e., representing general reward insensitivity. Therefore, this study examined behavioral and BOLD responses during delay discounting (DD) and effort discounting (ED) in ADHD.

Method

Thirty adolescents with ADHD and 28 controls (12–17 years) were scanned while performing a DD-ED task (fMRI findings were based on 21 and 25 participants, respectively). During DD, participants were presented with a series of choices between a small reward delivered immediately and a larger reward delivered after 5–25s. During ED, participants were presented with choices between a small reward that was delivered after exerting 15% of their maximal hand grip strength and a larger reward delivered after exerting 30–90% of their strength.

Results

Analyses on the subjective values of delayed and effortful rewards and on the Area Under the discounting Curves (AUCs) indicated that adolescents with ADHD showed steeper discounting than controls for DD, but not for ED. This was accompanied by a slightly stronger delay dose–response relationship in the amygdala for adolescents with ADHD who reported to be more delay averse in daily life.

Conclusion

Together, these results–steeper DD in the ADHD group and a stronger delay dose–response relationship in the amygdala, while no evidence for group differences in ED was found–support the delay aversion account of ADHD.

Introduction

Relatively strong preferences for small immediate rewards over larger delayed rewards (Jackson and MacKillop, 2016, Patros et al., 2016) are thought to be an important correlate of symptoms of Attention-Deficit/Hyperactivity Disorder (ADHD) (Sonuga-Barke, 2005). These preferences are frequently examined by delay discounting (DD) tasks in which people choose between large delayed rewards, and smaller immediate rewards. Preferences for the larger delayed reward typically decrease as the delay preceding this reward increases. This decrease of subjective value of the large reward as a function of increasing delay is referred to as DD (Critchfield & Kollins, 2001). Understanding the mechanism(s) of this impulsive behavior may contribute to development of interventions to reduce this behavior and associated unhealthy outcomes.

One theoretical model proposes that the main mechanism involved in steep DD in ADHD is delay aversion (Sonuga-Barke, Dalen, & Remington, 2003). Individuals with ADHD are thought to experience relatively strong negative emotions during waiting times, resulting in a preference to escape delay. Evidence for this theory, however, is still limited. There are only a few studies that have examined whether subjective experiences during waiting contribute to an immediate reward preference in ADHD. Scheres, Tontsch, and Thoeny (2013b), for example, showed that impulsive choices were more strongly correlated with difficulty waiting in youth with ADHD than in controls. In another study, self-reported delay aversion was associated with preferences for smaller sooner rewards in undergraduates (Mies, De Water, & Scheres, 2016). In addition, the neural correlates of delay aversion have not been clearly established yet. Some studies showed increased amygdala and insula activation in individuals with ADHD compared to controls in response to cues predicting delay (Lemiere et al., 2012, Van Dessel et al., 2018), and with increasing length of anticipated delays (Wilbertz et al., 2013). Increased amygdala activation was also found in adults with ADHD in response to anticipated delayed rewards (Plichta et al., 2009). Activation in these brain regions is thought to reflect emotional value and salience of delay-related stimuli, indirectly suggesting that steep DD in ADHD is associated with delay aversion. Competing alternative explanations for steep DD in ADHD have not yet been tested. Aberrant reward sensitivity (Luman, Tripp, & Scheres, 2010) could, for example, play a role. Therefore, we investigated the extent to which steep DD in ADHD was associated with delay aversion versus a relative insensitivity to reward magnitude.

One of the ways to examine this is by comparing behavioral and neural responses of adolescents with ADHD and controls during a delay discounting (DD) and an effort discounting (ED) task. In this latter task, participants chose between exerting more physical effort by squeezing a handgrip in order to gain a larger reward, or less effort to gain a smaller reward. Differences in the duration needed to exert more versus. less physical effort is negligible, making it an ideal ‘control’ condition to compare DD against. A recent study in young healthy men showed that rewards associated with physical effort were devalued in the same way as rewards associated with delays (Prevost, Pessiglione, Metereau, Clery-Melin, & Dreher, 2010). Clearly, both waiting and working for rewards are costly. Here, our aim was to examine whether altered discounting behavior in adolescents with ADHD is limited to delayed rewards, or whether it represents insensitivity to reward magnitude. If delay aversion is the primary factor involved in steep DD in ADHD, then group differences are expected for DD but not ED. If, however, reward insensitivity is an important factor, or if ADHD is associated with effort aversion, then we would expect to see steep discounting in ADHD also for ED.

Importantly, we chose to use real monetary rewards and real delays and efforts, as opposed to hypothetical designs used in previous fMRI studies on DD in ADHD (Carlisi et al., 2016, Chantiluke et al., 2014, Ortiz et al., 2015, Plichta et al., 2009, Rubia et al., 2009). Real delays and rewards require less episodic prospection, which may not be fully developed in children and adolescents yet, and real delays are, intuitively, more likely to capture delay aversion. Examining ED will advance our understanding of discounting of different types of cost, and increase our knowledge of motivational mechanisms in ADHD. Additionally, subjective experiences during the task, and daily-life delay aversion and reward sensitivity were assessed to gain a better understanding of the mechanisms involved in DD and ED.

Prevost et al. (2010) showed that the neural systems tracking rewards associated with delay and effort are different. They found, largely consistent with other imaging studies on DD (Scheres, de Water, & Mies, 2013a), involvement of the ventral striatum (VS), ventromedial prefrontal cortex (vmPFC) and lateral prefrontal cortex (LPFC) in DD. These brain regions were found to value larger delayed rewards. In the ED condition, however, the anterior cingulate cortex (ACC) and anterior insula appeared to track the devaluation of rewards that require more effort.

In the present study, we expected, in accordance with the delay aversion model 1) that adolescents with ADHD would show steeper DD than controls, but similar ED, and 2) to find group differences in the neural system underlying DD, but not underlying ED. Specifically, we expected aberrant activation of the VS, vmPFC, LPFC, posterior cingulate cortex (PCC) and posterior parietal cortex (PPC) in response to delay-related reward cues (decision-making) in the ADHD group compared to controls (Prevost et al., 2010, Scheres et al., 2013a). In response to effort-related reward cues, we expected activation of the ACC and anterior insula (Prevost et al., 2010), and no group differences, in line with our behavioral hypothesis. Additionally, we expected that adolescents with ADHD would show increased amygdala and insula activation during the experience of delay. During effort exertion, no group differences were expected.

Section snippets

Participants

Thirty-four adolescents (12–17 years) with ADHD (combined subtype) and 32 controls matched on age and gender were enrolled. Participants and parents both gave written informed consent, and the study was approved by the local medical ethics committee.

ADHD participants had an ADHD-combined type diagnosis by a child psychiatrist/psychologist. We assessed current validity of the diagnosis, and screened for other disorders, with the Diagnostic Interview Schedule for Children (DISC-IV) (Shaffer,

Behavior

DD was reflected by a large main (linear) effect of delay on SV [F (4,53) = 24.0, p < .001, η2p = .30]. The ADHD group discounted delayed rewards more than controls [main effect of group: F (1,56) = 5.3, p = .025, η2p = .087; Fig. 2A]. The interaction between group and delay did not reach statistical significance [F (4,53) = 2.6, p = .09, η2p = .045], suggesting that the group effect did not depend on delay level. Physical effort was also discounted [F (4,53) = 14.9, p < .001, η2p = .21],5

Discussion

This study aimed to dissociate the contribution of delay aversion and altered reward sensitivity to steep DD often found in ADHD. ED was included to examine whether steep discounting in adolescents with ADHD is limited to DD, or also occurs during ED, which would suggest that not only delay aversion, but also altered sensitivity to reward magnitude might play a role in DD. We replicated earlier findings by showing steeper DD in ADHD than control participants, using a task with real delays and

Conclusion

In sum, this study shows that adolescents with ADHD discount rewards associated with delay–but not with effort–more than controls. This effect was accompanied by a stronger delay dose–response relationship in the amygdala during waiting for those who reported to be more delay averse in daily life. This study therefore provides evidence for delay aversion in adolescents with ADHD.

Conflict of interest

Jan K Buitelaar has been in the past 3 years a consultant to / member of advisory board of / and/or speaker for Janssen Cilag BV, Eli Lilly, Lundbeck, Shire, Roche, Medice, Novartis, and Servier. He has received research support from Roche and Vifor. He is not an employee of any of these companies, and not a stock shareholder of any of these companies. He has no other financial or material support, including expert testimony, patents, royalties. Gabry W Mies, Ili Ma, Erik de Water and Anouk

Acknowledgments

This study was supported by a VIDI-grant (016.105.363) from the Netherlands Organisation for Scientific Research (NWO) awarded to Dr. Scheres. We thank all participants and their parents, Maria Lojowska for designing and programming the task, Pascal de Water for programming and technical support together with Mark van de Hei. We thank Marjolein van Donkelaar, Jana Kruppa and Jennifer Dicker for their help in data collection/entry, Paul Gaalman for his help in fMRI-data acquisition, Raimon Pruim

References (42)

  • A. Scheres et al.

    Steep temporal reward discounting in ADHD-combined type: Acting upon feelings

    Psychiatry Research

    (2013)
  • D. Shaffer et al.

    NIMH diagnostic Interview Schedule for children version IV (NIMH DISC-IV): Description, differences from previous versions, and reliability of some common diagnoses

    Journal of the American Academy of Child and Adolescent Psychiatry

    (2000)
  • E.J. Sonuga-Barke

    Causal models of attention-deficit/hyperactivity disorder: From common simple deficits to multiple developmental pathways

    Biological Psychiatry

    (2005)
  • E.J. Sonuga-Barke et al.

    Do executive deficits and delay aversion make independent contributions to preschool attention-deficit/hyperactivity disorder symptoms?

    Journal of the American Academy of Child and Adolescent Psychiatry

    (2003)
  • N. Tzourio-Mazoyer et al.

    Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain

    Neuroimage

    (2002)
  • T.M. Achenbach et al.

    Manual for the ASEBA school-age forms & profiles

    (2001)
  • Y. Benjamini et al.

    Controlling the false discovery rate - a practical and powerful approach to multiple testing

    Journal of the Royal Statistical Society Series B (Methodological)

    (1995)
  • M. Brett et al.

    Region of interest analysis using an SPM toolbox. 8th International Conference on Functional Mapping of the Human Brain

    (2002)
  • C.O. Carlisi et al.

    The effects of acute fluoxetine administration on temporal discounting in youth with ADHD

    Psychological Medicine

    (2016)
  • C.S. Carver et al.

    Behavioral inhibition, behavioral activation, and affective responses to impending reward and punishment: The BIS/BAS scales

    Journal of Personality and Social Psychology

    (1994)
  • S. Clare et al.

    The quick delay questionnaire: A measure of delay aversion and discounting in adults

    Attention Deficit and Hyperactivity Disorders

    (2010)
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