New perspectives on self-control development: Highlighting the roleof intentional inhibition

Margot A. Schel a,b,n, Anouk Scheres c, Eveline A. Crone a,b

a Institute of Psychology, Leiden University, Leiden, The Netherlandsb Leiden Institute for Brain and Cognition (LIBC), Leiden, The Netherlandsc Developmental Psychology, Behavioural Science Institute, Radboud University, Nijmegen, The Netherlands

a r t i c l e i n f o

Keywords:Self-controlIntentional inhibitionDelay discountingDevelopment

a b s t r a c t

The ability to exert self-control over one's thoughts and actions is crucial for successful functioning indaily life. To date, self-control development has been primarily studied from the perspective ofexternally driven inhibition. In this review, we introduce a new perspective on the development ofself-control by highlighting the importance of intentional inhibition. First, we will review the existingbehavioral and neuroscientific literature on the development of self-control from the perspective ofexternally driven inhibition. Next, we will introduce a new framework for studying the development ofself-control from the perspective of intentional inhibition. We will discuss several recent studies in thisdomain, showing that intentional inhibition within cold contexts has an early development, butcontinues to develop through adolescence in motivational contexts. We conclude that understandingthe developmental trajectory of intentional inhibition in cold and motivationally relevant contexts andits underlying mechanisms is an important direction for future research, which has importantimplications for our understanding of developmental disorders associated with problems in self-control,such as Attention Deficit Hyperactivity Disorder.

& 2014 Elsevier Ltd. All rights reserved.

1. Introduction

Self-control can be defined as the ability to exercise controlover one’s action, thoughts and emotions (Casey & Caudle, 2013).Self-control abilities are crucial for successful functioning in allaspects of human life (e.g. social situations, educational and workenvironments). The development of self-control is an importantaspect of cognitive development through childhood and adoles-cence (Diamond, 2013), and has far-reaching implications duringthis important developmental period. That is, self-control isimportant for learning (e.g. concentrating on the task at handand not getting distracted by the environment), for makingoptimal decisions (e.g. healthy food-related or financial decisions),for keeping friendships (e.g. not reacting impulsively and hittingsomeone, when being teased), and for social skill development(e.g. inhibit the impulse to cut in line) (Diamond, 2013).

At the core of self-control lies the ability to intentionally inhibitone’s actions. Intentional inhibition has been defined as a late‘veto’ mechanism (Filevich, Kühn, & Haggard, 2012; Haggard,

2008). By means of this late ‘veto’ mechanism, one can cancelaction execution of an already initiated action at the last possiblemoment, as given in by an internal thought process (Filevich et al.,2012; Haggard, 2008). Thus, intentional inhibition differs fromstimulus- or externally driven inhibition in that it is driven by aninternally generated process, rather than an external stimuluswhich tells you to stop your behavior. To date self-control devel-opment has been primarily studied from the perspective ofexternally driven inhibition (for a review, see Diamond (2013)),yet, intentional inhibition is clearly present in many aspects ofchildren’s life, such as when inhibiting the tendency to get up oftheir chair and walk around in the classroom based on internallyset goals, or when trying to finish a tedious task without super-vision. In addition, given that intentional inhibition lies at the coreof self-control, that is to say, most of our action control is driven byinternal motives, problems in intentional inhibition have wide-ranging implications, such as for childhood psychological and psy-chiatric disorders, such as Attention Deficit Hyperactivity Disorder(ADHD) (Moffitt et al., 2011) or conduct disorder (Fergusson, Boden, &Horwood, 2013).

Therefore, the goal of this review is to describe a new perspec-tive on the development of self-control by highlighting the impor-tance of intentional inhibition and the new advances in studyingthis domain. As such, we will first review the existing behavioral

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Neuropsychologia

http://dx.doi.org/10.1016/j.neuropsychologia.2014.08.0220028-3932/& 2014 Elsevier Ltd. All rights reserved.

n Corresponding author at: Institute of Psychology, Leiden University, Wasse-naarseweg 52, 2333 AK Leiden, The Netherlands. Tel.: þ31 71 5276692.

E-mail address: mschel@fsw.leidenuniv.nl (M.A. Schel).

Please cite this article as: Schel, M. A., et al. New perspectives on self-control development: Highlighting the role ofintentional inhibition. Neuropsychologia (2014), http://dx.doi.org/10.1016/j.neuropsychologia.2014.08.022i

Neuropsychologia ∎ (∎∎∎∎) ∎∎∎–∎∎∎

and neuroscientific literature on the development of self-control,with a focus on what is currently known about externally guidedinhibition. Next, we will describe the distinction between externallyand internally guided self-control and introduce a new frameworkfor studying the development of internally guided self-control,drawing on behavioral, psychophysiological and neuroscientificfindings. Several recent studies in this domain will be presented.Finally, we will discuss the implications of this new framework fordevelopmental disorders.

2. The development of self-control: externally guidedinhibition

The ability to control one’s actions and stop actions when theenvironment requires one to do so, also referred to as inhibition, isone of the most studied components of self-control development(Diamond, 2013; Zelazo et al., 2003). There are marked improve-ments in inhibition in infancy (Diamond, 2013), early childhood(Zelazo et al., 2003) and school-aged children (van der Molen,2000), which has been interpreted as reflecting the protracteddevelopment of executive control functions. Executive control isoften used as an umbrella term to refer to our ability to control ourthoughts and actions in order to attain future goals, and inhibitionis a key component of executive control (Diamond, 2013). As such,inhibition is thought to lie at the core of cognitive development(Diamond, 2013).

Most research on the development of inhibition has focused onthe development of stimulus-driven inhibition. In these experi-ments, inhibition is typically preceded by an external stimulus orcue, which signals that one has to stop an already initiated orprepotent action. Research with two experimental paradigms hascontributed significantly to our knowledge of the mechanismsunderlying stimulus-driven inhibition, namely the stop-signalparadigm and the go/no go paradigm. In the stop-signal paradigmparticipants are presented with a simple stimulus (e.g. a left orright pointing arrow) to which they have to respond as quickly aspossible. On a limited number of trials (i.e. about 25% of all trials) astop signal (e.g. a loud noise or a color-change of the stimulus) ispresented after the stimulus has come online. By varying the delaybetween presentation of the stimulus and presentation of thestop-signal, it is possible to calculate the Stop Signal Reaction Time(SSRT), that is the time one needs to inhibit an already initiatedresponse (Band, van der Molen, & Logan, 2003; Logan & Cowan,1984). The go/no go paradigm also examines the inhibition ofprepotent responses (Casey et al., 1997). In this paradigm, partici-pants are presented with a stream of stimuli (e.g. different letters)to which they have to respond by pressing a button. However, onestimulus (e.g. the X) is instructed to be a no go-stimulus, signalingthat participants have to withhold responding. This no go-stimulusis presented on a limited numbers of trials (i.e. around 20% of alltrials), and when this no go-stimulus is presented participantshave to inhibit a prepotent response to the presentation of a newstimulus (Casey et al., 1997). In contrast to the stop-signal para-digm, the go/no go paradigm does not allow for a calculation of theSSRT. Instead, the dependent variable in the go/no go paradigm isthe number of false alarms (i.e. the number of times a participantdoes not inhibit when a no go-stimulus is presented).

Cross-sectional developmental comparison studies using theseparadigms have shown that stimulus-driven inhibition has aprotracted development (Casey et al., 1997; Cohen et al., 2010;Durston et al., 2002; Rubia, Smith, Taylor, & Brammer, 2007).Studies using the stop-signal paradigm have found that eventhough children are already able to inhibit, the SSRT continues tobecome faster across development (between 6 and 30 years ofage) (Cohen et al., 2010; Ridderinkhof, Band, & Logan, 1999;

Williams, Ponesse, Schachar, Logan, & Tannock, 1999). Further-more, studies using the go/no go paradigm have shown that eventhough 6–10 year-old children are already able to inhibit, they aremore susceptible to the effects of prepotency of responding(Durston et al., 2002). That is to say, when a no go-trial waspreceded by a larger number of go-trials, thereby increasing theprepotency of responding, children experienced more difficultyinhibiting responding to that no go-stimulus (Durston et al., 2002).Taken together, young children are already able to inhibit, but notto the same level as adults and not in a stable level across the fullduration of a paradigm (Diamond, 2013; Luna, Padmanabhan, &O’Hearn, 2010). This ability continues to improve across childhoodand adolescence, with mature performance levels being reached inearly (11 years of age) (Huizinga, Dolan, & van der Molen, 2006) tolate adolescence (18 years of age), depending on task-difficulty(Luna et al., 2010).

Neuroscientific studies in adults have shown that a specificnetwork of brain regions is active when participants perform astop-signal task. This network involves the dorsal and ventralprefrontal cortex (specifically right inferior frontal gyrus (IFG)), theanterior cingulate cortex (ACC)/pre-supplementary motor area(SMA) and parts of the basal ganglia, including the subthalamicnucleus (STN) (see Fig. 1) (Aron & Poldrack, 2006; Ridderinkhof,Forstmann, Wylie, Burle, & van den Wildenberg, 2011; Verbruggen& Logan, 2008). Individual differences analyses have shown thatactivity in rIFG and STN correlates with SSRT, suggesting that theseare core regions for successful response inhibition (Aron, Behrens,Smith, Frank, & Poldrack, 2007; Aron & Poldrack, 2006). In addition,functional and structural network analyses have found that increasedconnectivity between rIFG and STN is related to successful responseinhibition performance (Aron et al., 2007; Forstmann et al., 2012;Jahfari et al., 2011; King et al., 2012).

Compared to adults, children show different activity duringexternally driven response inhibition. Specifically, some studieshave shown that 8–12 year-old children use left lateralized PFCregions whereas adults use right lateralized regions (Bunge,Dudukovic, Thomason, Vaidya, & Gabrieli, 2002), some studiesreported more activity in dorsolateral prefrontal cortex in 8–12year-old children compared to adults (Velanova, Wheeler, & Luna,2008), and others reported more activity in ventrolateral PFC inadults than in 6–10 year-old children (Durston et al., 2002).Together, these changes can be characterized as a shift fromdiffuse to focal activity (Durston et al., 2002). In other words, inchildhood, widespread inhibition related activation was observedacross lateral prefrontal cortex (Durston et al., 2002; Luna et al.,2010), whereas with increasing age this activation became morefocalized to the rIFG (Durston et al., 2002; Luna et al., 2010). Thesefindings are consistent with structural neuroimaging studiesshowing that regions in the lateral prefrontal cortex are the lastto mature in terms of loss of gray matter volume, which is an indexof neuronal maturation (Giedd, 2004; Shaw et al., 2008; Sowell etal., 2004), as well as in terms of slowly developing white mattermaturation in the prefrontal cortex and its connections (Paus,2010; Paus et al., 2001).

These findings fit well with studies focusing on other compo-nents of executive control which also rely on lateral prefrontalcortex, such as working memory (e.g. Crone, Wendelken,Donohue, van Leijenhorst, & Bunge, 2006; Finn, Sheridan, Kam,Hinshaw, & D’Esposito, 2010; Jolles, Kleibeuker, Rombouts, &Crone, 2011), task switching (e.g. Christakou et al., 2009; Crone,Donohue, Honomichl, Wendelken, & Bunge, 2006), and attention(Smith, Halari, Giampetro, Brammer, & Rubia, 2011). These studiesalso reported that prefrontal cortex activity is developing protractedlyin childhood and adolescence, which has been interpreted in terms ofincreased interactive specialization (i.e., an interactive experience-related process where some regions become less and other regions

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Please cite this article as: Schel, M. A., et al. New perspectives on self-control development: Highlighting the role ofintentional inhibition. Neuropsychologia (2014), http://dx.doi.org/10.1016/j.neuropsychologia.2014.08.022i

more involved in the task over time) of brain regions important forhigher order cognitive processes (Johnson, 2011). In sum, there issubstantial evidence that response inhibition, measured by theinhibition of behavior based on external signals, lies at the core ofcognitive development (Diamond, 2013), matures slowly acrossdevelopment (Diamond, 2013; Luna et al., 2010), and is associatedwith immature activity in the prefrontal cortex (Luna et al., 2010).

3. The development of self-control: intentionally guidedinhibition

Many of our daily activities involve stopping actions based oninternally generated (i.e., intentional) stop signals, rather thanexplicit external stimuli telling us to stop our actions. Despite theclear importance of the intentional component of inhibition,intentional inhibition has not been often addressed in develop-mental psychology and developmental cognitive neuroscience.Since intentional inhibition is not preceded by an external stimu-lus or cue, and does not result in any behavioral output, there areobvious difficulties in studying intentional inhibition. However,the need to inhibit is not constantly signaled by external cues, andtherefore, understanding the mechanisms of intentional inhibitionis of clear importance.

3.1. How to examine intentional inhibition

A useful framework for studying intentional inhibition is thefactorial organization of action control (Filevich et al., 2012).According to this framework both the motivation for action andthe motivation for inhibition can be externally or internally guided(see Table 1). Importantly, in daily life, action and inhibitiondecisions are often based on a combination of external andinternal motivations. For instance in our previous example ofchildren having to intentionally inhibit the tendency to get up oftheir chair and walk around in the classroom, external factors suchas teacher expectations also play a role. Within experimentalresearch, internal and external motivations for action and inhibi-tion are separated by the presence or absence of an external cuesignaling action or inhibition (Filevich et al., 2012).

Stimulus-driven inhibition involves the externally guided inhibi-tion of both externally and internally guided action. However, asoutlined above, traditionally most research has focused on externallyguided inhibition of externally guided action. Intentional inhibitionon the other hand involves the internally guided inhibition of bothexternally and internally guided action. When studying intentionalinhibition there are three main difficulties (Filevich et al., 2012). First,intentional inhibition does not result in any behavioral output. Thus,on the behavioral level one can only examine whether someone hasintentionally inhibited or not. However, concluding that intentionalinhibition has happened on the basis of no behavioral output is

Table 1Factorial organization of action control.

Action

Externally guided Internally guided

Inhibition Externally guided Stop walking when a green traffic light suddenly turns red. Stop teasing a classmate when a teacher suddenly appears.

Internally guided Resisting the impulse to take another biscuit from thebiscuit box standing in front of you.

Resisting the impulse to cut in line.

Fig. 1. (A) Brain regions associated with externally guided inhibition (in blue) and internally guided inhibition (in purple). (B) Brain regions associated with hypotheticaltemporal discounting (in green). Note: rIFG¼right inferior frontal gyrus, ACC/preSMA¼anterior cingulate cortex/presupplementary motor area, dFMC¼dorsal fronto-median cortex, STN¼subthalamic nucleus, dlPFC¼dorsolateral prefrontal cortex, mPFC¼medial prefrontal cortex, PCC¼posterior cingulate cortex, PPC¼posterior parietalcortex, vlPFC¼ventrolateral prefrontal cortex, and VS¼ventral striatum.

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Please cite this article as: Schel, M. A., et al. New perspectives on self-control development: Highlighting the role ofintentional inhibition. Neuropsychologia (2014), http://dx.doi.org/10.1016/j.neuropsychologia.2014.08.022i

problematic (see the third point). Therefore, psychophysiological andneuroimaging measures are particularly useful in the study ofintentional inhibition, since they can help identify the covertprocesses associated with inhibition. A second difficulty in the studyof intentional inhibition is that, intentional inhibition because it is aninternal process, which is not triggered by an external stimulus orcue, it cannot be easily manipulated in an experimental task. Third,according to our definition of intentional inhibition, intentionalinhibition involves the inhibition of an action. However, at thebehavioral level we cannot distinguish between an action that wasinhibited and an action that was never prepared. In the latter case,we would speak of early decision not to prepare an action. Thisprocess is linked more to action selection than to inhibition (Haggard,2008). Early decisions not to prepare an action are more likely inparadigms where there is no strong motivation for acting (Filevichet al., 2012). Therefore, paradigms designed to measure intentionalinhibition should include a strong motivation or prepotency foracting.

The marble paradigm (see Fig. 2A) is a valuable paradigm to studyintentional inhibition, which was first developed by Kühn, Haggard,and Brass (2009). In this paradigm, a white marble is rolling down aramp. As soon as the marble starts rolling, the marble changes colorto green. Participants are instructed to respond to the rolling marbleas quickly as possible, in order to prevent the marble from droppingfrom the ramp and crashing. On a number of trials (around 35%, thisdiffers slightly between experiments), the rolling marble does notchange color and remains white. In this case, participants are free tochoose to either respond or inhibit. The large proportion of greentrials serves two functions. First, the green trials lead to a prepotenttendency for action. Since the green marble trials are rather difficult,participants have to remain focused on the goal of respondingquickly to the rolling marble, thus increasing the prepotency ofresponding. Also, due to the intermixed presentation of green andwhite trials participants cannot predict when a white trial will bepresented. Therefore participants have to be prepared to quickly

respond to a green marble during the whole duration of theexperiment, leaving the prepotency intact. This is desirable, so thatintentional inhibition of action will involve a late brake on analready-prepared action, rather than a decision not to initiate actionpreparation. As will be shown in the subsequent sections, combiningthe marble task with heart rate and neuroimaging techniques canprovide valuable insights in the processes involved in intentionalinhibition.

3.2. Psychophysiological and neural concomitants of intentionalinhibition

A useful measure for studying the covert processes underlyingintentional inhibition is the study of phasic heart rate changes.Phasic heart rate changes are shown to be a sensitive index ofcognitive control processes in general (Crone, Somsen, Van Beek, &Van Der Molen, 2004; Crone et al., 2003; Jennings, Van der Molen,& Debski, 2003), and response activation and inhibition processesin particular (Jennings & van der Molen, 2002; van der Molen,2000; Van der Veen, Van der Molen, & Jennings, 2000). Duringpreparation and/or anticipation of a speeded response (a go-stimulus in a go/no go or stop-signal paradigm), a pattern of heartrate deceleration is typically observed (Jennings & van der Molen,2002, 2005; Jennings, van der Molen, Somsen, & Terezis, 1990).This pattern of anticipatory heart rate deceleration is interpretedas indicative of the central inhibition of action representations(Jennings & van der Molen, 2002, 2005). This anticipatory heartrate deceleration is followed by acceleratory recovery when aresponse is made (Jennings & van der Molen, 2005; Jennings et al.,1990). However, during inhibition, the shift from anticipatoryheart rate deceleration to acceleratory recovery is delayed, andheart rate continues to decelerate (Börger & van der Meere, 2000;Jennings & van der Molen, 2005; Jennings, van der Molen, Pelham,Debski, & Hoza, 1997; van der Molen, 2000; Van der Veen et al., 2000).This continued deceleration is implicated to be indicative of midbrain

Fig. 2. (A) Schematic representation of the marble paradigm. See text for details about the paradigm. (B) Percentage of internally guided inhibition choice for children (8–10-year olds), early adolescents (11–12-year olds), and adults (18–26-year olds). (C) Stimulus-locked heart rate changes associated with externally guided action, omission,internally guided action, and internally guided inhibition. IBI 0 refers to the IBI during which the marble started rolling. An increase in IBI difference scores indicates heartrate deceleration, and a decrease in IBI difference scores indicated heart rate acceleration. Note: IBI¼ Interbeat Interval, the time between two consecutive heart beats inmilliseconds.

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Please cite this article as: Schel, M. A., et al. New perspectives on self-control development: Highlighting the role ofintentional inhibition. Neuropsychologia (2014), http://dx.doi.org/10.1016/j.neuropsychologia.2014.08.022i

inhibition of action (Jennings, van der Molen, & Stenger, 2008; Van derVeen et al., 2000).

This measure was applied to study the covert componentsof intentional inhibition using the marble paradigm (Schel,Windhorst, van der Molen, & Crone, 2013). In this study thefollowing conditions were dissociated; actions on the externallydriven green action trials, omissions on the externally drivengreen action trials, decision to act on the intentional white trials,and decisions to inhibit on the intentional white trials. In line withthe literature on externally driven inhibition (Jennings & van derMolen, 2005; Van der Veen et al., 2000), anticipatory heart ratedeceleration was observed for all conditions. However, heart ratecontinued to decelerate in both the intentional action and theintentional inhibition condition, indicative of involvement of asupervisory attentional system in intentional action and inhibitiondecisions. Importantly, heart rate deceleration was most pro-nounced during intentional inhibition, indicating that an activeinhibitory process was in place. Taken together, in this study it wasfound that heart rate was sensitive to intentional decisions to actor inhibit (see Fig. 2C) (Schel et al., 2013).

A second method, which is useful for unraveling the covertprocesses involved in intentional inhibition, is neuroimaging. fMRIstudies can generate more specific hypotheses about the under-lying mechanisms involved in externally driven and intentionalinhibition. The first fMRI study specifically designed to measureintentional inhibition made use of a free choice paradigm invol-ving the internally generated inhibition of internally generatedaction (Brass & Haggard, 2007). In this paradigm, participants wereasked to always prepare and perform a simple action (i.e. a keypress) at the time of their choice. Importantly, participants wereinstructed to withhold this action at the last possible moment onsome freely chosen trials. On every trial, including those whentheir action was inhibited, participants reported the time at whichthey felt they were about to perform their action. This reportedtime, also in the absence of action, formed the event modeled inthe fMRI analysis. This analysis showed specific activation duringintentional inhibition in the dorsal fronto-median cortex (dFMC), abrain region not implicated in stimulus-driven inhibition (seeFig. 1) (Brass & Haggard, 2007). However, the free choice paradigmdiffers in two aspects from traditional stimulus-driven inhibitionexperiments, which focus on externally guided inhibition ofexternally guided action. That is to say, in this free choiceparadigm both the decision to act and the decision to inhibit wereinternally guided, making the interpretation of these resultsdifficult.

In an fMRI study in adults, Kühn et al. (2009) introduced themarble paradigm, which only differs in the internal initiation ofinhibition from the traditional stimulus-driven inhibition para-digms. The critical contrast focused on brain regions that weremore active during intentional decisions to inhibit compared tointentional decisions to act. This study also showed specificactivation in the dFMC during intentional inhibition (Kühn et al.,2009), comparable in location to the study by Brass and Haggard(2007). One question that remained unanswered was the extent towhich this activation was dependent on prepotency of responding.To address this question, Schel et al. (2014) used the same task butmade a distinction between intentional action and inhibitiondecisions that were preceded by different numbers of externallydriven green action trials, thereby varying the prepotency ofresponding. Here, it was found that dFMC activation is contextspecific (Schel et al., 2014). That is, as shown by a parametricanalysis, participants showed less dFMC activation during inten-tional inhibition when there was a strong prepotency for acting(i.e. when the intentional inhibition trial was preceded by a largernumber of green action trials). Also the behavioral results showedthat participants were less likely to inhibit when there was a

strong action prepotency (Schel et al., 2014). A second issue thatwas addressed in this study was the extent to which there wasoverlap in activation for externally and internally guided inhibi-tion. Schel et al. (2014) showed that there is considerable overlapin the neural networks involved in intentional and stimulus-driven inhibition. Thus, although intentional inhibition is concep-tually different from stimulus-driven inhibition, similar inhibitorynetworks were involved when inhibition was applied, irrespectiveof how (intentional or stimulus-driven) inhibition was initiated(Schel et al., 2014).

These results show that, in adults, intentional and externallyguided inhibition activate a similar network of regions in lateralprefrontal regions (including rIFG) and ACC/preSMA. However,intentional inhibition also appears to be associated with distinctactivation in dFMC, a region that is not involved in stimulus-driveninhibition (Brass & Haggard, 2007; Kühn et al., 2009; Schel et al.,2014). This dFMC region extending to the dorsal ACC is also foundto be the main region important for intentional inhibition in ameta-analysis of fMRI studies looking at intentional inhibition(Filevich et al., 2012). Interestingly, although intentional inhibitioncannot be easily manipulated because it is not triggered by anexternal signal or cue, it has been shown that varying thepreceding context can influence both the likelihood of intentionalinhibition and the level of activation of the dFMC during inten-tional inhibition (Schel et al., 2014). Thus, the underlying neuralmechanisms of intentional inhibition appear to be at least partlydistinct from the neural mechanisms underlying externally guidedinhibition.

3.3. Development of intentional inhibition

As outlined above, stimulus-driven inhibition appears to have aprotracted developmental trajectory (Diamond, 2013; Luna et al.,2010), with mature performance levels being reached in lateadolescence (Luna et al., 2010). This protracted developmentco-occurs with developmental changes in the underlying neuralcorrelates; that is, children show compensatory activation in thelateral prefrontal cortex during inhibition (Durston et al., 2002;Luna et al., 2010) and with increasing age this activation becomesmore focalized to the rIFG (Durston et al., 2002). However, muchless is known about the development of intentional inhibition.

One way in which the development of intentional inhibitionhas been studied, is with a heart rate study using the marbleparadigm (Schel et al., 2013). Three age-groups (8–10, 11–12, and18–26 year olds) performed the marble task, while their heart ratewas measured continuously. As with the analysis of heart rateresponses in adults, the following conditions were dissociated:actions on the externally driven green action trials, omissions onthe externally driven green action trials, decision to act on theintentional white trials, and decisions to inhibit on the intentionalwhite trials. The results showed that 8–10 year-old and 11–12year-old children did not differ in intentional inhibition decisionsfrom adults; all participants decided to inhibit on approximately50% of the trials (see Fig. 2B). All age groups showed anticipatoryheart rate deceleration for all conditions. Also, all age groupsshowed continued heart rate deceleration in both the intentionalaction and the intentional inhibition conditions (see Fig. 2C). Thus,in this study we have shown that 8–10 year-old children arealready able to intentionally inhibit response to a similar extent asadults. Also, heart rate was most sensitive to intentional inhibitionacross age groups. For all age groups, a pronounced heart ratedeceleration during intentional inhibition was found, indicative ofinvolvement of a supervisory attentional system (Schel et al.,2013).

The marble paradigm has also been applied in a cross-sectional developmental fMRI study to examine the development

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of the neural bases underlying intentional inhibition (Schel,Ridderinkhof, & Crone, 2014). In this study two age-groups (10–12 and 18–26) performed the marble task while fMRI data wereacquired. The results of this study showed a replication of the earlydevelopment of intentional inhibition, by showing that bothchildren and adults decided to inhibit on approximately 50% ofthe trials. However, although performance was similar, the under-lying neural mechanisms were different in children (Schel,Ridderinkhof et al., 2014). That is, compared to adults, childrenshowed increased activation during intentional inhibition relativeto intentional action in rIFG and right putamen, key regions of thefronto-basal ganglia network for inhibition (Aron & Poldrack,2006; Ridderinkhof et al., 2011). However, no developmentaldifferences in dFMC activation during intentional inhibition wereobserved (Schel, Ridderinkhof et al., 2014).

Thus, in contrast to stimulus-driven inhibition, intentionalinhibition as measured with the marble paradigm appears to havea relatively early developmental trajectory (Schel, Ridderinkhof etal., 2014; Schel et al., 2013). This idea was reinforced by theabsence of covert heart rate differences in response to intentionalinhibition demands. However, the underlying neural correlatesdiffered between children and adults (Schel, Ridderinkhof et al.,2014), yet, these differences emerged in the brain network whichis typically associated with externally guided inhibition, not in thedFMC. Thus, it remains a question for future research whetherintentional action control is a process which develops beforeexternally guided action control.

An additional question, which was previously addressed in abehavioral study, was whether intentional inhibition was influ-enced by motivational or affective context. In daily life, we oftenexperience strong motivations for action and inhibition, and inhibi-tion rarely happens in an affectively neutral context. A previousstudy showed that stimulus-driven inhibition appears to be influ-enced by affective context (Tottenham, Hare, & Casey, 2011). In thisstudy, participants were instructed to respond to face stimuliexpressing a certain emotion and inhibit responding to facesexpressing a different emotion. Four different emotional expres-sions were included, three negative emotions (fear, anger andsadness), and one positive emotion (happiness), and in each blocka different emotional face was coupled with neutral faces, toexamine whether response inhibition was differently influencedby neutral versus emotional faces. In a developmental sample (5–28year olds) it was found that response inhibition performance wasmost negatively influenced by emotions for which emotion recog-nition was worst, namely for anger and sadness (Tottenham et al.,2011). Also, irrelevant emotional background stimuli appearedto influence response inhibition performance (Cohen-Gilbert &Thomas, 2013; Krypotos, Jahfari, van Ast, Kindt, & Forstmann,2011; Verbruggen & De Houwer, 2007). Importantly, these effectsappear to be dependent on arousal, such that highly arousingpictures have a stronger influence on response inhibition(Verbruggen & De Houwer, 2007). Also, it was found that thisinfluence of irrelevant emotional stimuli on response inhibition waslarger for individuals who showed more heart rate variability(a proxy of emotion regulation) (Krypotos et al., 2011). Thesefindings made us hypothesize that possibly also intentional inhibi-tion would be affected by motivational context and possibly moreso in children and adolescents than in adults.

In order to examine whether intentional inhibition was influ-enced by affective context, Schel and Crone (2013) performed anintentional inhibition experiment in which colors were the rele-vant dimension (i.e. the colors indicated whether participants hadto act, inhibit, or choose between acting and inhibiting) andemotion was an irrelevant dimension. In this study it was foundthat across development, irrelevant emotions had no influence onintentional inhibition decisions (Schel & Crone, 2013). However,

it remains an important question for future research whether thesame is true when emotion is relevant for the task at hand. Forexample, one study found that emotional faces in a go/no go taskwere associated with more activation in ventral striatum (a regionimportant for reward processing) in adolescents compared tochildren and adults when this cue was relevant to the task(Somerville, Hare, & Casey, 2011).

These differences when emotional stimuli are behaviorally rele-vant or incidental may also be important when studying the neuralcorrelates of intentional inhibition. Kühn and colleagues used thisapproach in an fMRI study comparing the intentional and stimulus-driven inhibition of experiencing emotion (Kühn, Haggard, & Brass,2013). In this study they showed that intentional and stimulus-driven inhibition of experiencing emotions could be dissociated onthe basis of underlying neural mechanisms. Intentional inhibition ofexperiencing emotions was associated with activation of the dFMC,the same brain region implicated in intentional inhibition of action(Brass & Haggard, 2007; Kühn et al., 2009; Schel et al., 2014),whereas stimulus-driven inhibition of experiencing emotions wasassociated with activation in the dorsolateral prefrontal cortex (Kühnet al., 2013). Thus, there is a promising potential of studying thedevelopment of intentional inhibition using affective stimuli as thefocus of action or inhibition.

4. The development of self-control: inhibition in order tomaximize future rewards

As outlined above, exerting self-control, and especially inten-tional inhibition, rarely happens in affectively neutral contexts indaily life. It has been shown that both relevant and irrelevantaffective contexts influence stimulus-driven inhibition (Cohen-Gilbert & Thomas, 2013; Somerville et al., 2011; Tottenham et al.,2011), but an irrelevant affective context does not appear toinfluence intentional inhibition decisions (Schel & Crone, 2013).However, the mere presence of an affective context does notnecessarily impose motivational forces, which can influence inten-tional decisions; therefore looking at the influence of rewardsmight be a fruitful research direction.

An important motivator for self-control concerns determiningthe balance between preferring small immediate rewards overlarger delayed rewards, a process also referred to as delay ofgratification (Mischel, Shoda, & Rodriguez, 1989), or delay discount-ing (Ainslie, 2005; Green, Fry, & Myerson, 1994). Paradigms tappinginto these processes are highly applicable to understanding inten-tional components of self-control, because in such paradigms,participants have control over whether to act and receive theimmediate reward, or to control the tendency to act by inhibitingand waiting for the delayed reward. A classic developmentalparadigm in which these motivational forces are clearly present isthe delay of gratification paradigm, also referred to as the marsh-mallow test. This delay of gratification paradigm for preschoolerspresents children with one pair of two options: one marshmallownow, or two marshmallows after an unspecified delay (later, whenthe experimenter returns (Mischel et al., 1989)). Studies using thisparadigm have shown that there are individual differences in theability to inhibit the impulse to choose the immediately gratifyingoption of one marshmallow during the preschool ages (Mischelet al., 1989), which appear to be predictive for self-control abilitieslater in life (Casey et al., 2011; Eigsti et al., 2006). In addition, Caseyand colleagues found that individuals who were less able to delaygratification when they were preschoolers, showed poorer self-control and differential recruitment of the fronto-basal ganglianetwork during an emotional go/no go paradigm 40 years later(Casey et al., 2011), suggesting that these early individual differ-ences reflect temperament characteristics with long term effects.

M.A. Schel et al. / Neuropsychologia ∎ (∎∎∎∎) ∎∎∎–∎∎∎6

Please cite this article as: Schel, M. A., et al. New perspectives on self-control development: Highlighting the role ofintentional inhibition. Neuropsychologia (2014), http://dx.doi.org/10.1016/j.neuropsychologia.2014.08.022i

In addition to these individual differences, several studies havereported that preferences for small immediate rewards tend todecrease as a function of age, suggesting that self-control increaseswith age (Christakou, Brammer, & Rubia, 2011; de Water, Cillessen,& Scheres, 2014; Lee et al., 2013; Olson, Hooper, Collins, & Luciana,2007; Prencipe et al., 2011; Scheres et al., 2006; Steinberg et al.,2009). Unlike individual differences during the preschool years,these age effects have been examined with delay discounting (DD)tasks, consisting of a series of, often hypothetical, choice pairs(rather than only one in the marshmallow test) between monetaryrewards (rather than marshmallows). A further distinctionbetween the tasks is that the constant temptation to takethe immediate reward (1 marshmallow in front of the child) inthe delay of gratification paradigm while the child is waiting forthe experimenter, is not present in delay discounting tasks. , thedelay is not experienced, and in real DD tasks, participants cannotchange their mind once they have decided to choose the largedelayed reward. Therefore, it is likely that self-control, while alsoinvolved in DD tasks, plays a more prominent role in delay ofgratification paradigms. Keeping this in mind, we will brieflysummarize the age effects on self-control as measured with DDtasks. The task that is most comparable to the marshmallow task isthe airplane task, developed by Scheres et al. (2006). In this task,participants choose between a variable small reward that wouldbe immediately delivered and a large constant reward that wouldbe delivered after a variable delay. Importantly, participants reallyhad to wait during the delay period, when choosing for thedelayed reward (see Fig. 3A), and money was actually paid toparticipants. Age comparisons between children aged 6–11 andadolescents aged 12–17 showed that adolescents were more likelyto prefer the delayed reward compared to children (see Fig. 3B).These findings fit well with hypothetical delay tasks, in whichthere were only hypothetical delay periods and monetary rewards,but in which participants could choose between a small immedi-ate and a larger delayed reward (Christakou et al., 2011; de Wateret al., 2014; Lee et al., 2013; Steinberg et al., 2009), and withpotentially real tasks, in which participants are informed that onechoice will be randomly selected and paid to them (Olson et al.,2007; Prencipe et al., 2011). These studies also reported anincreasing preference for delayed rewards during adolescence.Note, however, that the only longitudinal study on delay discount-ing reported preferences in a potentially real task to be stableduring adolescence (Audrain-McGovern et al., 2009). Similarly,Lamm, Zelazo, and Lewis (2006) reported no significant changes inpotentially real delay discounting from 9 to 17 years of age.In addition, two studies, one with a hypothetical task and onewith a real task (the airplane game) reported non-linear effects of

age: 11–13 year olds showed maximal ability to wait relative to 8–10 and 14–16 year olds in a hypothetical tasks (Demurie, Roeyers,Baeyens, & Sonuga-Barke, 2012a), while in the airplane game,adolescents showed maximal ability to wait (peaking at age 14) ascompared to children and emerging adults (Scheres, Tontsch,Thoeny, & Sumiya, 2014).

In adults a network of brain regions, including medial prefrontalcortex (mPFC), ventral striatum, and posterior cingulate cortex(PCC) regions involved in the valuation of immediate rewards,and posterior parietal cortex (PPC), dorsolateral prefrontal cortex(dlPFC), and ventrolateral prefrontal cortex (vlPFC) regions involvedin the valuation of immediate and delayed rewards, is associatedwith hypothetical delay discounting (for a review, see Scheres, deWater, and Mies (2013)). In a study comparing adolescents andadults it was found that adults made more consistent decisions.Compared to adolescents, adults showed more parietal cortexactivation during decision making on a hypothetical delay discount-ing task, which was associated with more consistent decisionmaking (Ripke et al., 2012). Another developmental study showedthat older participants showed stronger functional connectivitybetween ventromedial prefrontal cortex (vmPFC) and striatal areasduring selection of immediate options (Christakou et al., 2011).Peper et al. (2013) also showed that in adults increased structuralconnectivity between frontal and striatal regions was associatedwith better impulse control on a temporal discounting paradigm.

To our knowledge, no study has yet examined the neuralcorrelates of actual waiting for delayed rewards during real delaydiscounting tasks across development, which entails the inten-tional inhibition of an (tempting) action. Our prediction would bethat waiting for the delayed reward will be associated withincreased activity in the dFMC, a region which partly overlapswith the mPFC region associated with hypothetical discounting.Currently, only a few studies have focused on the inhibition oftempting actions and these studies were all based on adults. Thesestudies have shown that in adults, inhibiting the temptation tocontinue gambling (Campbell-Meiklejohn, Woolrich, Passingham,& Rogers, 2008), and inhibiting a craving for cigarettes (Brodyet al., 2007) both activate the dFMC, the same region implicated inintentional inhibition of motoric actions (Brass & Haggard, 2007;Kühn et al., 2009; Schel et al., 2014). Given that developmentaldifferences seem present mostly when there is a strong motivationto act, an important model for future research will be to test theinterplay between activity in brain regions which drive emotionsand brain regions which ‘veto’ our motives to act, which will allowus to understand self-control from a broader perspective, integratingknowledge from externally-guided response control, motivation, andinternal self-control.

Fig. 3. (A) Schematic representation of the airplane paradigm. See text for details about the paradigm. (B) Delay discounting curves of children (6–11-year olds) andadolescents (12–17-year olds).

M.A. Schel et al. / Neuropsychologia ∎ (∎∎∎∎) ∎∎∎–∎∎∎ 7

Please cite this article as: Schel, M. A., et al. New perspectives on self-control development: Highlighting the role ofintentional inhibition. Neuropsychologia (2014), http://dx.doi.org/10.1016/j.neuropsychologia.2014.08.022i

5. Implications for developmental disorders

There are several childhood/adolescence disorders, which areassociated with difficulties with self-control, such as AttentionDeficit Hyperactivity Disorder (ADHD) (Willcutt, Doyle, Nigg,Faraone, & Pennington, 2005), oppositional defiant disorder/con-duct disorder (ODD/CD) (Nigg, 2003), and substance abuse (Wills& Stoolmiller, 2002). Traditionally, these disorders have beenexamined from a self-control perspective using externally driveninhibition tasks, with mixed results. For example, meta-analyses ofstudies using externally driven inhibition tasks have shown thatthere are clear inhibition problems in children and adults withADHD (Lijffijt, Kenemans, Verbaten, & van Engeland, 2005;Oosterlaan, Logan, & Sergeant, 1998; Willcutt et al., 2005). How-ever, effect sizes are small to moderate, and not all children withADHD have problems with externally driven inhibition (Nigg,Willcutt, Doyle, & Sonuga-Barke, 2005). In terms of neurobiologi-cal correlates, the results of prior studies have shown that childrenand adults with ADHD show decreased recruitment of the fronto-basal ganglia network (including rIFG) during externally drivenresponse inhibition compared to healthy controls (for meta-analyses, see Cortese et al. (2012) and Hart, Radua, Nakao,Mataix-Cols, and Rubia (2013)).

One interesting direction for future research on self-control inADHD, will be to examine the role of intentional inhibition, giventhat in many daily life situations, children need to control impulsessuch as wanting to get up of their chair and walk around in theclassroom. These types of behavior, which are typical of childrenwith ADHD or conduct disorder, often require an internal decisionto inhibit, or veto, actions. The behavioral paradigms and neuro-biological model proposed here provide a promising starting pointfor examining intentional inhibition in these disorders. Addition-ally, as children grow up, adults expect an increasing ability tointentionally inhibit actions. Specifically, when still in their child-hood, individuals with ADHD will more often than not have adultsin their proximity who serve as external drivers of self-controlledbehaviors. However, as individuals with ADHD get older, thedemands on internally driven inhibition will only increase. Forexample, in high school and beyond, it is expected that studentsdemonstrate self-controlled behaviors with less and less assis-tance from others. Therefore, an intriguing hypothesis, whichcould be addressed in future research, is that the developmentof intentional inhibition may play a role in the remission versuspersistence of ADHD symptoms over time.

A promising start for studying intentional inhibition in moti-vationally relevant contexts in individuals with ADHD has beenmade in research employing delay discounting tasks (Barkley,Edwards, Laneri, Fletcher, & Metevia, 2001; Demurie, Roeyers,Baeyens, & Sonuga-Barke, 2012b; Hurst, Kepley, McCalla, &Livermore, 2011; Paloyelis, Asherson, Mehta, Faraone, & Kuntsi,2010; Plichta et al., 2009; Scheres et al., 2006; Scheres, Tontsch,Thoeny, & Kaczkurkin, 2010; Wilson, Mitchell, Musser, Schmitt, &Nigg, 2011) or choice delay tasks (Solanto et al., 2001; Sonuga-Barke, Taylor, Sembi, & Smith, 1992; for a review, see Luman,Oosterlaan, and Sergeant (2005)). These tasks are relevant here,because participants have control over whether or not to controlthe tendency to act by inhibiting and waiting for the delayedreward. If these tasks are viewed as measures of intentionalinhibition, a preliminary conclusion would be that those withADHD have relatively weak intentional inhibition, since themajority of studies have demonstrated that individuals with ADHDchose not to control the tendency to act and prefer the immediatereward. However, we note here that additional processes areinvolved in delay discounting tasks such as delay aversion, sub-jectively experienced difficulty waiting, and sensitivity to rewardmagnitude and reward immediacy (Marco et al., 2009; Scheres,

Tontsch, & Thoeny, 2013; Scheres et al., 2010). Additionally, asubstantial portion of these studies made use of hypotheticaltasks, reducing the demand on intentional inhibition to resist atemptation. Therefore, other paradigms may be more suitable formeasuring intentional inhibition in individuals with ADHD, bothin cool contexts, such as the marble paradigm (Kühn et al., 2009),and in hot contexts, such as the marshmallow paradigm (Mischelet al., 1989) or an emotion regulation paradigm (Kühn et al., 2013).

A better understanding of the typical development of theunderlying mechanisms of the ability to intentionally inhibittempting actions will help to better understand developmentaldisorders of impulsivity such as ADHD. Currently, many childrenwith ADHD receive cognitive behavioral therapy focused on theuse of external reinforcers in order to stimulate positive behavior(Serrano-Troncoso, Guidi, & Alda-Diez, 2013). However, an impor-tant direction for future research will be to examine whethershifting the focus to motivations and drives from within (internalprocesses) may help children, adolescents, and adults with ADHDto better regulate their own behavior (see also Solanto et al.(2010)).

6. Conclusion

To conclude, intentional inhibition is an important componentof self-control, which should be examined from a developmentalperspective. Within a cold context, intentional inhibition appearsto mature early (in childhood), even though underlying neuralcorrelates hint towards activation differences in the inhibitionnetwork between children and adults (Schel, Ridderinkhof et al.,2014; Schel et al., 2013). However, when stimuli are motivationallyrelevant, developmental differences become more prevalent, suchas in the airplane task (Scheres et al., 2006). These newlydeveloped paradigms provide an important starting point forexamining this salient, but understudied process in child andadolescent development.

Neurobiological models suggest an important role for themedial prefrontal cortex, and especially the dFMC, in intentionalinhibition in both cold and motivationally relevant contexts.Studying the neurobiological development of intentional inhibi-tion from a motivational perspective provides a promising routefor future research. fMRI studies of the development of intention-ally inhibiting emotions and waiting for rewards might add to ourunderstanding of developmental disorders such as ADHD andODD/CD and help provide new treatments tailored to the needsof children with ADHD and ODD/CD.

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