PSYCHIATRY AND PRECLINICAL PSYCHIATRIC STUDIES - ORIGINAL ARTICLE

CID: a valid incentive delay paradigm for children

Viola Kappel • Anne Koch • Robert C. Lorenz •

Rudiger Bruhl • Babette Renneberg • Ulrike Lehmkuhl •

Harriet Salbach-Andrae • Anne Beck

Received: 30 August 2012 / Accepted: 14 December 2012

� Springer-Verlag Wien 2013

Abstract Despite several modifications and the wide use

of the monetary incentive delay paradigm (MID; Knutson

et al. in J Neurosci 21(16):RC159, 2001a) for assessing

reward processing, evidence concerning its application in

children is scarce. A first child-friendly MID modification

has been introduced by Gotlib et al. (Arch Gen Psychiatry

67(4): 380–387, 2010); however, comparability in the

results of different tasks and validity across different age

groups remains unclear. We investigated the validity of a

newly modified MID task for children (CID) using func-

tional magnetic resonance imaging. The CID comprises the

integration of a more age appropriate feedback phase. We

focused on reward anticipation and their neural correlates.

Twenty healthy young adults completed the MID and the

CID. Additionally, 10 healthy children completed the CID.

As expected, both paradigms elicited significant ventral

and dorsal striatal activity in young adults during reward

anticipation. No differential effects of the tasks on reaction

times, accuracy rates or on the total amount of gain were

observed. Furthermore, the CID elicited significant ventral

striatal activity in healthy children. In conclusion, these

findings demonstrate evidence for the validity of the CID

paradigm. The CID can be recommended for the applica-

tion in future studies on reward processing in children,

adolescents, and in adults.

Keywords Children � Monetary incentive delay paradigm �Reward anticipation � Validity � Ventral striatum

Introduction

Reward processing is a key component for effective

learning and the development of goal-directed behavior

(DeRusso et al. 2010; Staddon and Cerutti 2003). Reward-

related brain responses represent valuable biomarkers for

an individuals’ preferences, personality traits, and psy-

chopathology (Dillon et al. 2011). At the neural level, the

mesolimbic dopaminergic system has been recognized for

its central role in reward processing (Alcaro et al. 2007;

Daw and Shohamy 2008; Haber and Knutson 2010;

McClure et al. 2004; O’Doherty 2004; Schultz 2010;

Schultz et al. 1997). Key structures of this network are the

ventral striatum (VS), the ventral pallidum, the anterior

cingulate cortex, the orbitofrontal cortex (OFC), and the

dopaminergic midbrain.

A standard paradigm to explore reward-related brain

responses is the monetary incentive delay (MID) task,

introduced by Knutson et al. (2001a). The MID task allows

the explicit distinction between an anticipation phase

V. Kappel (&) � A. Koch � U. Lehmkuhl � H. Salbach-Andrae

Department of Child and Adolescent Psychiatry, Psychosomatics

and Psychotherapy, Charite-Universitatsmedizin Berlin,

Augustenburger Platz 1, 13353 Berlin, Germany

e-mail: viola.kappel@charite.de

V. Kappel � B. Renneberg

Clinical Psychology and Psychotherapy,

Freie Universitat Berlin, Habelschwerdter Allee 45,

14195 Berlin, Germany

R. C. Lorenz � A. Beck

Department of Psychiatry and Psychotherapy,

Charite-Universitatsmedizin Berlin, Chariteplatz 1,

10117 Berlin, Germany

R. C. Lorenz

Department of Psychology, Humboldt Universitat zu Berlin,

Unter den Linden 6, 10099 Berlin, Germany

R. Bruhl

Physikalisch Technische Bundesanstalt Berlin,

Abbestraße 2-12, 10587 Berlin, Germany

123

J Neural Transm

DOI 10.1007/s00702-012-0962-0

(introduction of a cue signaling the upcoming potential

reward) and an outcome phase (reward is delivered or

omitted). Functional magnetic resonance imaging (fMRI)

studies using the MID task, consistently ascertained spe-

cific brain responses [blood oxygenation level dependent

(BOLD) responses] in healthy adults. Anticipation of

monetary reward increases ventral striatal (nucleus ac-

cumbens, NAcc) and dorsal striatal (putamen and caudate

nucleus) BOLD responses (Knutson et al. 2001a, b, 2003;

Spreckelmeyer et al. 2009). Specifically, ventral striatal

activity increases with the amount of monetary gain

(Knutson et al. 2001a).

The MID task has been used in a broad variety of

studies. Several task modifications exist, which mainly

vary in anticipation and feedback conditions or in the type

of incentives used. Despite the variety of conditions and

incentives, the same proportional increase of striatal

activity during adult reward anticipation has been reported

in response to social feedback (Spreckelmeyer et al. 2009),

primary taste reward (O’Doherty et al. 2002), food

(McClure et al. 2007), and verbal reward (Kirsch et al.

2003). Moreover, there is evidence that the striatum’s role

in reward processing depends on the salience associated

with the anticipated reward, rather than value or hedonic

feelings (Cooper et al. 2009; Cooper and Knutson 2008;

Zink et al. 2004). Thus, the incentive delay task and its

induced neural response seem to comprise both valence as

well as salience of an anticipated reward, and are not

limited to monetary cues.

With a developmental focus, the MID paradigm has

been used in children and adolescents (Bjork et al. 2004,

2008, 2010; Demurie et al. 2011; Guyer et al. 2006;

Scheres et al. 2007). Compared to studies on adults, most

studies of reward processing in youth have found enhanced

activity in mesolimbic circuitry during reward anticipation

compared to neutral anticipation (Delgado et al. 2000;

Ernst et al. 2005; Galvan et al. 2006). In contrast, studies

by Bjork et al. (2004, 2008, 2010) using the MID task in

youth consistently reported decreased activation in these

structures during reward anticipation compared to neutral

anticipation. However, the MID task may have yielded

these distinct results in youth compared to adults because

the MID was originally designed for adults and is therefore

suboptimal for younger populations. In order to collect

adequate fMRI data and to keep younger participants

engaged, it is essential to use age appropriate tasks that

allow children to achieve reasonable levels of performance

(Davidson et al. 2003). The MID task requires advanced

working memory and sustained task engagement, both of

which are challenging for children and adolescents (for

review see Taylor et al. 2012). For this reason, the MID

paradigm was modified for younger participants (Gotlib

et al. 2010; Helfinstein et al. 2012). Recently, a cartoon

style, child-friendly version of the MID task, the so-called

‘‘pinata task’’ was presented. It elicits neural activation

patterns consistent with those seen in adults via the MID

paradigm (Helfinstein et al. 2012). Although its colorful

stimuli are likely to be more engaging for younger children

than the rather unamusing white stimuli of the original

MID task, the context of the game represents a rather

emotionally engaging set of stimuli that may distract par-

ticipants and attenuate neural activation (Vuilleumier

2005). Furthermore, the pinata task does not include ‘‘loss’’

trials, which may change the way participants respond to

the reward trials due to the effects of framing (Reyna and

Brainerd 2011). Reward trials may be processed differently

if they are ‘‘framed’’ by the presence of loss trials. While

the pinata task investigates ‘‘pure’’ reward processing, the

original MID investigates neural correlates of reward pro-

cessing intermixed with neutral and loss conditions. Thus,

direct comparisons with the original MID cannot be made.

In contrast, Gotlib et al. (2010) presented the ‘‘kids mon-

etary incentive delay (KIDMID) task’’ for children. In

order to use an age appropriate incentive, the feedback

condition was modified for children older than 10 years.

The modification consisted of the replacement of the

rewarding monetary stimulus by points that could be con-

verted into prizes. More precisely, during the feedback

condition, the participants saw the word ‘‘points’’ behind

the numeric display of gained and received prizes, instead

of money, according to the total amount gained. So far, the

KIDMID task by Gotlib et al. (2010) is the modification

most similar to the original MID task and may therefore, in

theory, allow comparisons of results across different stud-

ies using either the MID or the KIDMID task. However, the

abstract numeric presentation of reward may still be too

difficult to understand for children younger than 10 years

of age, especially for young inpatients with severe psy-

chiatric disorders such as attention deficit hyperactivity

disorder (ADHD) or autism spectrum disorders (Helfinstein

et al. 2012). Moreover, points may represent a weaker

reward stimulus than money, which may be closer to social

feedback; therefore, direct comparisons toward the classic

MID task should not be made. In sum, the comparability of

results obtained by modified MID tasks and the original

MID task remains vague. Thus, the validity of result

comparisons, e.g. across different studies and age groups,

remains unclear. It is conceivable that different effects

could emerge with different task modifications. Unfortu-

nately, in spite of modifications of the MID task and

its use in different age groups, little methodological

approval exists on its validity and on the validity of fMRI

tasks in general (Desmond and Annabel Chen 2002;

Fliessbach et al. 2010). Therefore, it is essential to verify

V. Kappel et al.

123

methodological validity of future MID modifications and

the comparability of their results by directly comparing

results assessed via the original MID task and the modified

version.

The aim of the present study is to validate a modified

MID paradigm for later application in psychiatrically

impaired children and adolescents suffering from severe

neurodevelopmental disorders. The validation was achieved

by comparing the modified version, the so-called child-

friendly incentive delay task (CID), with the original ver-

sion (MID) in young adults. Drawing on findings obtained

by previous neuroimaging studies, we predict that MID and

CID both trigger ventral striatum activity during reward

anticipation. Additionally, the CID was piloted in a sample

of healthy children to validate the striatal response toward

reward anticipation for this young age group.

Materials and methods

Participants

A total of 23 healthy young male adults and 10 healthy

children (2 female) participated in the study. All participants

were recruited through advertisements in the local commu-

nity. Participants had (1) no psychiatric diagnosis according

to the International Classification of Diseases, 10th revision

(ICD-10) or Axis I and II of the Diagnostic and Statistical

Manual of mental disorders, 4th edition, text revision (DSM-

IV-TR), (2) no history of dependence on illicit drugs and

alcohol, (3) no first-degree relatives with a neurological or

psychiatric disorder, (4) no sensory-motor deficits or other

neurological disorders, and (5) were currently not taking any

psychotropic medication. All participants were right-handed,

except for one left-handed boy. Due to technical problems or

excessive head movement (translation larger than 2 mm

and/or rotation larger than 1� in any direction), three adults

had to be excluded from further analyses. Thus, data of 20

males between 19 and 31 years of age (M = 24.7,

SD = 3.4), and 10 healthy children between 8 and 12 years

of age (M = 11.0, SD = 0.4) were analyzed. Written

informed consent was obtained from each participant and/or

their legal guardians prior to participation and after a full

explanation of the purpose and procedures of the study was

given. Adults were reimbursed for participating in the study

and children received a gift certificate for a toy store for their

participation. Approval for the study was obtained from the

local Ethics Committee.

Diagnostic procedures

To ensure that participants were free of any physical or

mental illness, and/or behavior problems, an individual

diagnostic assessment consisting of standardized self-

report inventories and interviews was conducted on all

participants by a professional examiner prior to the MRI

data acquisition (for sample characteristics see Table 1).

Socioeconomic status was measured with the Hollingshead

Index of Social Status in adults and in children according to

parental occupation (Hollingshead 1975). IQ was assessed

using the Culture Fair Intelligence Test (CFT-20-R, Weiß

2006). Handedness was examined via the Edinburgh

Handedness Inventory (Oldfield 1971). The assessment in

adults also included the German version of the Structured

Clinical Interview for DSM–IV Diagnoses (SCID I & II,

Wittchen et al. 1997). Due to their association with reward

processing (Beck et al. 2009; Ross and Peselow 2009),

substance use was assessed in adults via the Composite

International Diagnostic Interview, module addiction

(CIDI/DIA-X, Wittchen et al. 1996), which is a computer-

based interview for the examination of substance-use dis-

orders on the basis of ICD-10 and DSM-IV criteria. Five

adults were smokers and 19 adults had regular alcohol

intake. Psychiatric examination in children included the

semi-structured diagnostic interview Schedule for Affec-

tive Disorders and Schizophrenia for School-Age Children-

Present and Lifetime Version (Kiddie-SADS-PL, Kaufman

et al. 1997; German translation: Delmo et al. 2001).

Because patients with ADHD show altered reward pro-

cessing (Wilbertz et al. 2012), ADHD symptoms in adults

were assessed via the German version of the self-report form

of the Conner’s adult ADHD rating scale (CAARS, Conners

et al. 1999), and in children via the Attention-Deficit/

Hyperactivity Disorder Rating Scale-IV-Parent Version:

Investigator-administered and Scored (ADHD-RS-IV-Par-

ent; DuPaul et al. 1998). Participants’ mean scores for the

CAARS’ scales and for the ADHD-RS-IV-Parent did not

reveal any clinically significant values.

Functional magnetic resonance imaging

Adults completed both versions of the MID paradigm,

while children completed only the child version CID. In

order to control for possible sequence effects in the

examination of adults, we used a pseudorandomized design

in which 50 % of the adult participants first performed the

original MID task by Knutson et al. (2001a) and 50 % of

the adult participants first performed the CID. Adults had a

short break between the two tasks in which they could

leave the scanner. Both tasks are event-related fMRI

designs that consist of two sessions of 72 trials, yielding a

total of 144 trials per task. Each run lasted about 11 min.

Before entering the scanner, all participants completed a

short practice version of the task to minimize learning

effects and to ensure that participants had completely

understood the task.

Child-friendly incentive delay task

123

Original MID

The original MID task as described by Knutson et al.

(2001a) examines neural responses during anticipation and

consumption of monetary gain, loss, and no consequences.

During the anticipation phase (250 ms), participants saw

one of three geometric figures that signaled the opportunity

to either gain money (circle), to avoid losing money

(square), or to react for no consequences (triangle = neu-

tral condition) by responding as fast as possible with a

button press during subsequent target presentation (white

square presented for 200 ms up to maximum 1,000 ms).

A variable delay of 2,250–2,750 ms was inserted between

cues and targets. After responding, participants received

feedback for 1,650 ms indicating a gain, a loss, or neutral

outcome according to their performance and the total

cumulative amount of gain was updated. Due to the

application of an adaptive algorithm for target duration,

task difficulty was standardized to a hit rate of 67 % for all

participants. The first trial started with a given account of

eight points (numeric). Within one trial, subjects could

constantly gain or lose one point, or receive a neutral

outcome. Before entering the scanner, adult participants

were informed that they would receive 5 € in additional to

a basic reimbursement if they had reached a total of 20

points by the end of the second session. This outcome was

the same for adults in both tasks. In total, the two sessions

consisted of 54 gain, 54 loss, and 36 neutral trials, that

were presented in a pseudorandomized sequence.

Child-friendly incentive delay task (CID)

In order to provide a less abstract feedback and to assure a

clear and prompt comprehension even for younger chil-

dren, the original MID task was modified by inserting a

feedback phase that is appropriate for children. We fol-

lowed the idea of Gotlib et al. (2010) who used points as

the rewarding stimulus; however, instead of presenting a

plus or minus followed by the numeric amount of points

that had been gained or lost, participants were informed

about their performance by dots and an arrow. Depending

on the preceding cue, the arrow could either point upward

(response was fast enough and gain of one point), down-

ward (no response or not in the given time window and loss

of one point), or to the right (no response or response in the

given time window and no consequence). Furthermore,

instead of the updated cumulative amount of points pre-

sented as a numeric figure, subjects saw white dots. Chil-

dren were informed that they can exchange their points for

candy and that they will receive a toy store coupon after the

test session. Apart from the modified feedback condition,

the MID and the CID task did not differ and were con-

ducted in the exact same way as described in ‘‘Original

MID’’ (Fig. 1), including the constant win or loss of one

point (or nothing in the neutral condition) within a trial.

Table 1 Sample characteristics

Adults n = 20 Children n = 10

M SD M SD

Age (years) 27.4 3.4 11.0 0.4

SES (Hollingshead Index of Social Status) 5.93 1.23 5.85 0.84

Education (years) 12.4 1.23 5.05 1.32

CFT-IQ (Part 1, minimum time) 107.4 11.37 111.9 5.1

Edinburgh Handedness Inventory 92.78 9.21 83.33 14.43

Cigarettes per day (n = 5) 5.8 5.36 0 0

Alcohol per month (g) 212.5 208.3 0 0

CFT culture fair intelligence test, M mean, n sample size, SD standard deviation, SES socioeconomic status

Fig. 1 Task structure for a representative successful gain trial in the

original monetary incentive delay task (MID, top) and for the child-

friendly incentive delay task (CID, bottom)

V. Kappel et al.

123

FMRI data acquisition and analysis

Scanning was conducted on a 3T GE Signa Scanner with an

8-channel head coil. Functional images were acquired using

a T2*-weighted in-/out-spiral pulse sequence using the fol-

lowing parameters: repetition time [TR] = 2,300 ms, echo

time [TE] = 27 ms, flip = 90�, matrix = 128 9 96, field

of view (FOV) = 256 9 192 mm, voxel size = 2 9 2 9

4 mm3. Twenty-nine slices were collected approximately

parallel to the bicommissural plane (AC-PC-line), covering

the mesolimbic and prefrontal regions of interest, as delin-

eated by prior research (Knutson et al. 2001a). A total of 295

fMRI volumes were acquired per session. For anatomical

reference, a three-dimensional (3D) magnetization prepared

rapid gradient echo (MPRAGE) image was acquired

(TR = 7.9 ms; TE = 3.2 ms; flip = 20�; matrix = 256 9

192; FOV = 240, voxel size = 1 9 1.25 9 1 mm3). FMRI

data were analyzed using SPM8b (Wellcome Department of

Neuroscience, London, UK, http://www.fil.ion.ucl.ac.uk/spm).

After temporal (correction for slice acquisition delay) and

spatial preprocessing (movement correction, spatial normali-

zation interpolating to a final voxel size of 3.3 9 3.3 9

3.3 mm3 using a 4th degree b-spline interpolation and

smoothing with 7 mm full-width at half maximum [FWHM]),

fMRI data were analyzed as an event-related design in the

context of the general linear model (GLM) approach in a two-

level procedure.

Prior to preprocessing, data of all participants were

manually inspected and it was ensured that images were

aligned correctly. The first three volumes of each time

series were excluded to avoid non steady-state effects

caused by T1 saturation. The mean image was used to

estimate the transformation parameters for the stereotaxic

normalization to a standard echo-planar imaging template

as facilitated by the Montreal Neurological Institute (MNI-

template). Normalization of children’s brain data was

conducted via a customized pediatric template created with

the Template-O-Matic toolbox by Wilke et al. (2008). To

account for variance caused by head movement, corre-

sponding parameters were included in the single subject

models. Participants with translation of more than 2 mm in

any direction and rotation of 1� during the whole experi-

ment were excluded (3 participants).

On the first level, the three different cue conditions

(anticipation of gain, anticipation of loss, and anticipation

of neutral outcome), the target, and five feedback condi-

tions (successful gain, non-successful gain, successful loss

avoidance, non-successful loss avoidance, and neutral

outcome) were modeled as events and convolved with the

canonical hemodynamic response function. For each sub-

ject and each task (MID, CID), the baseline contrast images

for ‘‘gain anticipation cues’’, ‘‘loss anticipation cues’’, and

‘‘neutral anticipation cues’’ were computed and taken to the

second level. To detect group differences in the adult

sample, a second level random effects analysis using a

2 9 3 ANCOVA with the factors condition (gain, loss,

neutral) and task (CID, MID), as well as the covariates

(alcohol and cigarette consumption, and impulsivity) was

conducted. These covariates were included due to their

significant association with reward processing (Ripke et al.

2012; Beck et al. 2009; Rose et al. 2012). For the children

sample, a 1 9 3 ANCOVA with the factor condition

and the covariates (age, gender, and impulsivity) was

conducted. Age and sex were included as covariates

because the children sample consisted of four girls and six

boys, and because of pervasive morphological changes that

occur during normal development in this age range. Due to

apriori hypotheses, we only report anticipation contrasts.

Activations are reported at a significance threshold of

p \ 0.05 (FDR-corrected for multiple comparisons, whole

brain) and a minimum cluster size of 10 voxels. Due to the

small sample size of the children sample, additional

AlphaSim correction (as provided in REST toolbox, Song

et al. 2011) was conducted with a p \ 0.005 threshold and

within voxels that were taken into account of the whole

brain analysis. 1000 Monte Carlo simulations revealed a

multiple comparison corrected minimum clustersize of 26

voxels with a significance level of p \ 0.05.

Corresponding brain regions were identified with reference

to the Anatomy Toolbox for SPM (version 1.7, http://www.

fz-juelich.de/inm/inm-1/DE/Forschung/_docs/SPMAnantomy

Toolbox/SPMAnantomyToolbox_node.html) as developed

by Eickhoff et al. (2005).

Results

Behavioral data

1. Adult sample: a repeated measures ANOVA with the

factors ‘‘task’’ (MID, CID) and ‘‘condition’’ (gain,

neutral, loss) was performed for reaction times. Mean

reaction times revealed a significant main effect of

condition [F (2,38) = 6.554, p \ 0.001), indicating

faster responses during both gain (186.67 ms

(SE = 3.82)] and loss trials [188.27 ms (SE = 2.92)]

compared to the neutral trials [260.93 ms (SE =

21.66)]. Neither a main effect of task [F (1,19)

= 0.39, p = 0.539] nor a task-by-condition interac-

tion [F (2,38) = 1.3, p = 0.283] appeared. There was

also no significant difference in the total amount of

gains [Mgain = 21.1 points, t = -0.135, p = 0.894)

and in accuracy rates of cues indicating gain, loss or

neutral outcome (p \ 0.05) all together, indicating

that the two tasks did not differ in their behavioral

results.

Child-friendly incentive delay task

123

2. Children sample: due to small sample size, a Kruskal–

Wallis Test was conducted for reaction times to

compare the three ‘‘conditions’’ (gain, neutral, loss).

Although there was no significant effect of condition

on reaction times (H (2) = 2.738, p = 0.254), the

same trend as in the adult sample, indicating faster

responses during gain and loss trials, was observable.

It has to be noted that this result may represent a bias

due to the small sample size and the large variance in

the neutral condition (for behavioral data see Table 2).

Neuroimaging results

Neural activity within tasks during reward anticipation

1. Adult sample: For the MID task during the anticipation

of gain in comparison to the neutral condition, the

2 9 3 ANCOVA with the factors condition (gain, loss,

neutral) and task (CID, MID) revealed a significant

activation in the bilateral ventral striatum, the bilateral

putamen, and the left supplementary motor area

(SMA) with the left precentral gyrus. For the CID task

during the anticipation of gain in comparison to the

neutral condition, the 2 9 3 ANCOVA with the fac-

tors condition (gain, loss, neutral) and task (CID, MID)

revealed a significant activation in the left ventral

striatum, the bilateral putamen, the left middle cingu-

late cortex with the SMA, the right precuneus and the

left inferior frontal gyrus (p \ 0.05 whole brain FDR-

corrected for multiple comparisons, minimum cluster

size: 10 voxel; see Table 3).

2. Children sample: for the CID task during the antici-

pation of gain, the 1 9 3 ANCOVA with the factor

condition (gain, loss, neutral) revealed a significant

activation for gain [ neutral in the bilateral ventral

striatum, the left precentral gyrus, the right thalamus,

the right cerebellum, the left SMA, and the bilateral

lingual gyrus (Table 3). Exploratory analyzes for the

CID task revealed no significant differences between

children and adults during the anticipation of gain

(covariates: age, sex, impulsivity; cluster size of [26

voxels and therefore correctable for multiple compar-

isons regarding AlphaSim correction p \ 0.05).

Task comparison of MID versus CID in adults

during reward anticipation

The 2 9 3 ANCOVA with the factors condition (gain, loss,

neutral) and task (CID, MID) did not reveal a main effect

of task for gain anticipation. Specifically, an overlap of

striatal activation in both tasks (contrast: gain [ neutral

cues) was displayed in the bilateral putamen and the left

ventral striatum (Fig. 2).

Task order effects have been ruled out by comparing the

group that started with MID (n = 11) to the group that

started with CID (n = 9) during reward anticipation

(gain [ neutral). The 2 9 3 ANCOVA with the factors

condition (gain, loss, neutral) and group (first CID, first

MID) revealed no significant differences between both

groups (p [ 0.05, FDR-corrected).

Discussion

Our results show that the CID task is a valid fMRI para-

digm to study reward processing in children and adults and

therefore enables distinct and consistent developmental

fMRI research on reward processing across the life span.

This is the first validation study comparing neural activa-

tion during a modified MID paradigm for children (CID)

with the original MID paradigm (Knutson et al. 2001a, b).

To achieve this, neural activation during the CID task was

Table 2 Behavioral data

Adults Children

MID CID p CID

M SD M SD M SD

Total gain 21.15 2.6 21.05 2.37 0.894 17.3 4.88

Reaction time gain (ms) 187.98 17.1 185.36 22.18 0.518 245.07 41.23

Reaction time loss (ms) 190.58 18.97 185.97 18.13 0.175 259.24 55.18

Reaction time neutral (ms) 251.65 157.76 270.2 116.01 0.324 323.18 129.78

Hitrate gain (%) 64.64 5.01 62.88 4.39 0.138 57.79 5.01

Hitrate loss (%) 59.56 6.08 61.22 4.27 0.186 59.47 6.39

Hitrate neutral ( %) 48.61 16.08 45.14 9.9 0.245 52.49 14.85

CID child-friendly incentive delay task, MID monetary incentive delay task, M mean, SD standard deviation

No significant differences in Student’s t test: all p [ 0.05

V. Kappel et al.

123

Table 3 Brain regions activated during the anticipation of gain in comparison to the neutral condition (ANCOVA, covariates for adults: alcohol

and cigarette consumption, and impulsivity; covariates for children: age, sex, and impulsivity)

Brain structure (CP %) H Cluster size (voxel) Z (peak) p (FDR) MNI coord. (mm)

x y z

MID (n = 20 adults)

SMA L 823 5.28 0.001* -5 -3 49

Area 6 (70 %)

Precentral gyrus L 4.88 0.001* -38 -13 49

Area 6 (40 %)

Putamen L 109 4.42 0.001* -19 10 -1

Ventral striatum L 4.15 0.003* -9 10 -4

Putamen R 102 5.06 0.001* 18 10 -7

Ventral striatum R 3.16 0.028* 11 3 3

CID (n = 20 adults)

Middle cingulate cortex L 2426 6.78 0.000* -5 -3 46

Area 6 (60 %)

SMA L 6.24 0.000* -5 -13 62

Area 6 (100 %)

Putamen R 1679 6.61 0.000* 14 13 -7

Putamen L 6.16 0.000* -15 13 -7

Ventral striatum L 5.11 0.000* -12 7 6

Precuneus R 24 3.27 0.008* 14 -66 46

SPL (7P) (10 %)

Inferior frontal gyrus (pars Triangularis) L 13 2.87 0.019* -38 36 26

CID (n = 10 children)

Precentral gyrus L 414 5.06 0.029** -32 -23 69

Area 6 (100 %)

Angular gyrus L 4.25 0.232** -42 -69 46

IPC (PGp) (60 %)

Inferior parietal lobule L 4.24 0.232** -42 -49 62

SPL (7PC) (20 %)

Thalamus (pulvinar) R 107 3.68 0.577** 1 -30 -10

Brainstem (red nucleus) L 3.61 0.577** -2 -23 -7

Brainstem (substantia nigra) L 3.59 0.577** -12 -26 -14

Cerebellum vermis R 104 3.10 0.917** 4 -66 -27

Lobule VI (Vermis) (43 %)

Cerebellum R 2.98 0.994** 18 -66 -30

Lobule VI (Hem) (86 %)

SMA L 66 3.71 0.577** -2 -13 52

Area 6 (90 %)

Ventral striatum R 35 3.25 0.868** 11 7 -4

Ventral striatum L 27 2.87 0.994** -15 7 -1

Lingual gyrus L 26 3.26 0.868** -2 -86 -14

Area 18 (10 %)

Lingual gyrus R 2.75 0.994** 14 -89 -7

Area 18 (70 %)

CID child-friendly incentive delay task, CP cytoarchitectonic probability (if available), FDR false-discovery rate, H hemisphere, IPC inferior

parietal cortex, L left, MID monetary incentive delay task, MNI Montreal Neurological Institute, R right, SMA supplementary motor area, SPLsuperior parietal lobe

* Whole brain FDR-corrected for multiple comparisons, p \ 0.05, cluster size [ 10 voxels

** Cluster size of [26 voxels and therefore correctable for multiple comparisons regarding AlphaSim correction p \ 0.05

Child-friendly incentive delay task

123

directly compared with activation during the original MID

task in the same sample of healthy young adults. In order to

provide a less abstract feedback and to assure a clear and

prompt comprehension in children, the original MID task

was simplified based on a first modification by Gotlib et al.

(2010) by inserting an outcome phase that is appropriate

for children. As predicted, both tasks (MID, CID) elicited

consistent brain activity in healthy young adults during

reward anticipation in the dorsal striatum (putamen) and

ventral striatum and there were no differential effects of the

task on this activation. Behavioral data support the con-

current validity of the CID task, since there were no sig-

nificant differences between the two tasks regarding

reaction times and the total amount of gain. Additionally, a

pilot sample of healthy children completed the CID task.

Findings revealed the predicted striatal activation and

behavioral results and therefore underline the validity of

the CID task in children. Our results replicate previous

findings based on monetary reward anticipation during the

MID task (Knutson et al. 2001a, b, 2003). Nevertheless,

this is the first study to show that the modified feedback

condition did not alter task performance on a behavioral or

neurofunctional level. In sum, the presented CID task is a

valid paradigm to study reward-related brain response in

children, adolescents, and adults and therefore enables

direct comparisons across different age groups.

Because the CID task was especially modified for future

investigations of neural reward processing in children, a

few considerations have to be noted: first, to ensure validity

of the CID in children, a direct comparison of the MID and

the CID task in a sample of children would be optimal.

However, it has to be noted that children of this young age

group do not properly understand the original MID task,

which was the reason for the task modification in the first

place; therefore, direct comparisons of CID and MID task

are not feasible in children.

Secondly, to confirm validity of fMRI results across

different age groups, simple and adequately rewarding

paradigms, which also enable younger participants to

understand the task, are needed. At the same time, suffi-

ciently high valence and salience of the anticipated reward

is essential for task engagement of older participants.

Because the CID task uses points (in terms of graphical

dots) instead of numeric stimuli, this may attenuate neural

activations. However, results confirm that the CID task

adhered to both requirements and that even such dots can

trigger reward-related brain response in healthy young

adults if they receive a rather small monetary reward after

Fig. 2 Increase in ventral striatal activation during gain anticipation

in both, the original monetary incentive delay task (MID) and the

child-friendly version (CID). MID (left panels) and CID (middlepanels) brain activation results for the contrast ‘‘gain cues [ neutral

cues’’ for the MID task; displayed at MNI coordinate y = 12. Bottom:

Box plots with the parameter estimates for the BOLD response in the

ventral striatum during anticipation of gain (red) and neutral (blue)

for left and right VS. MID\ [CID (upper right panel) Brain

activation results for the contrast ‘‘gain cues [ neutral cues’’ for MID

task versus CID task; displayed at MNI coordinate y = 12. Overlap(lower right panel) brain activation results for the overlap for the

contrast ‘‘gain cues [ neutral cues’’ for the two tasks (dark blue CID

activation difference; cyan: overlap between MID and CID);

displayed at MNI coordinate y = 12. CID in children (upper rightpanel): Brain activation results for the contrast ‘‘gain cues [ neutral

cues’’ for the CID task; displayed at MNI coordinate y = 7. BottomBox plots with the parameter estimates for the BOLD response in the

ventral striatum during anticipation of gain (red) and neutral (blue)

for left and right VS. For illustrative purposes, all results are shown at

p \ 0.05 (FDR corrected, whole brain), cluster size [ 10 voxels. a.u.arbitrary units, BOLD blood oxygenation level-dependent, MNIMontreal Neurological Institute

V. Kappel et al.

123

the session. A high consistency in neural activation was

demonstrated during reward anticipation in both versions

of the MID task, as well as the findings in healthy children;

this leads to the assumption that valence and salience in the

CID task are comparable with the original MID task.

Thirdly, recent studies linked altered reward processing

to adolescent onset behavior problems, i.e., substance

abuse (Schneider et al. 2012), smoking (Peters et al. 2011),

and alcohol consumption (Nees et al. 2012). Yet, cross-

sectional studies examining adolescent reward processing

relative to adults revealed conflicting results, especially

concerning the VS. During reward anticipation, there is

evidence for both, striatal hypo- (Bjork et al. 2004, 2010)

and hyper-responsiveness (Ernst et al. 2005; Galvan et al.

2006; Jarcho et al. 2012; Van Leijenhorst et al. 2010b).

Whereas striatal hyperactivity could reflect an increased

salience of rewards during adolescence and therefore pro-

voke greater reward-seeking behavior (Ernst et al. 2005;

Galvan et al. 2006; Van Leijenhorst et al. 2010a, b),

decreased striatal activity could reflect a blunted response

to typical rewards and enhance motivation to seek high-

intensity rewards (Bjork et al. 2004; Schneider et al. 2012).

These conflictive results may be partly due to methodo-

logical differences caused by the paradigms used in those

studies. While studies reporting decreased striatal activa-

tion used the original MID paradigm (Bjork et al. 2004,

2010), striatal hyperactivity has been shown in different

incentive tasks, such as the wheel of fortune task (Ernst

et al. 2005), a delayed response two-choice task (Galvan

et al. 2006), a decision-making task (Jarcho et al. 2012), a

gambling task (Van Leijenhorst et al. 2010a), or a slot

machine task (Van Leijenhorst et al. 2010b). Task-specific

features may have led to conflicting results. While some of

these tasks discriminate between reward anticipation and

reward consumption, others may have confounded these

two components (Van Leijenhorst et al. 2010b). Discrim-

inating these processes, adolescents showed increased ven-

tral striatal responses during reward consumption compared

to adults and children, but no such group differences

emerged during reward anticipation (Van Leijenhorst et al.

2010a). A more differentiated picture evolves concerning

other task-specific features, such as the need for decision-

making (Jarcho et al. 2012). Tasks that do not require

decision-making often result in developmental differences

in striatal activity during reward anticipation, but not dur-

ing reward receipt (Bjork et al. 2004, 2010), whereas tasks

that engage the participants in decision making often reveal

opposite findings (Ernst et al. 2005; van Leijenhorst et al.

2010a). To conclude, variability in task-design may have

contributed to the discrepancies in these findings; therefore,

task consistency should be closely monitored to allow more

distinct conclusions on reward processing across the life

span. Other possible explanations that may account for

these inconsistencies include differences in the definition

of adolescence (e.g. age-related vs. Tanner stages-related)

and further methodological differences in terms of image

analysis (Desmond and Annabel Chen 2002). However, to

compare and interpret fMRI study results, the use of con-

sistent paradigms is essential (Bandettini 2012; Callicott

et al. 1998; Poldrack 2000).

Lastly, only a few studies explored reward processing in

children and adolescents at risk for mental disorders, e.g.,

adolescent children of alcohol-dependent parents (Bjork

et al. 2008), and children at risk for depression (Gotlib

et al. 2010) or substance abuse (Schneider et al. 2012). The

CID paradigm presented here provides a valid opportunity

to conduct further studies in this vital field.

In sum, these inconsistent results drawn by inconsistent

fMRI paradigms demonstrate the need for studies with

consistent task procedures addressing maturational changes

in reward processing. Untangling these neural processing

differences in children, adolescents, and adults can stimu-

late further considerations for the early detection of chil-

dren at risk for reward-related health problems. The

presented validation of the CID paradigm for children

enables more distinct and consistent developmental fMRI

research on reward processing across the life span because

it can be used in youth as well as in adults. The CID task

may also be appropriate for elderly patients with mild

cognitive impairment, since this group shows deficits in

calculation and therefore most likely also in the represen-

tation of quantitative stimuli (Ribeiro et al. 2006). Fur-

thermore, CID could also be helpful in the identification of

neurobiological factors of early and late psychopathology

related to reward processing by exploring healthy partici-

pants parallel to different clinical populations, such as

ADHD (Scheres et al. 2007), depression (Shad et al. 2011),

or conduct disorder (Finger et al. 2010).

The present study addresses the major lack of method-

ological studies concentrating on the validity and reliability

of new or modified fMRI paradigms (Desmond and Ann-

abel Chen 2002; Fliessbach et al. 2010). To ensure

adequate conclusions, results of fMRI studies need to

reflect brain activity exclusive of methodological arti-

facts. A major strength of this study is the exclusion of

several methodological sources of potential error variance.

Experimental conditions during both task versions were

kept as constant as possible. Data acquisition was con-

ducted following a standardized protocol and identical

scanner hardware and software were used. Compared to

previous studies, we included a large homogeneous sam-

ple of healthy male adults, similar in age and education,

as well as a pilot-sample of healthy children. We strictly

excluded participants with any physical or psychiatric

diagnosis according to standardized semi-structured

interviews.

Child-friendly incentive delay task

123

The current study is not without limitations. First, we

did not control for the intake of potentially psychoactive

substances (nicotine, alcohol, or caffeine) prior to the

study, but strictly excluded subjects with substance use

disorders. Second, we did not completely randomize but

pseudo-randomized the order of task presentation, which

could have led to effects on participant–task interactions.

Third, in order to keep the CID task as simple as possible,

we used only one single reward possibility. In contrast,

Gotlib et al. (2010) used five different incentive levels in

their KIDMID, in line with the original MID paradigm by

Knutson et al. (2001a). Unfortunately, younger children

aged 8–12 years did not properly understand these

different incentive levels, which is why this approach was

not feasable in our study. Hence, due to the lack of

different reward levels it is not possible to consider cue

incentive size activation modulations in regions consis-

tently reported in MID task studies that are associated

with gambling effects [i.e., VS, insula, medial prefrontal

cortex, and thalamus (Helfinstein et al. 2012; Knutson and

Greer 2008)]. Because rates of gambling, problem gam-

bling, and pathological gambling are especially high in

adolescents (for a review see Chambers and Potenza

2003), future studies should investigate possible different

activation patterns during the CID task with and without

gambling aspects. Fourth, although both MID and CID

tasks elicit activation of the brain reward system, the two

tasks may trigger different cognitive processes. While the

MID task offers a tangible reinforcer (money), the CID

offers non-financial performance feedback (points in the

form of dots) that may be more closely related to socially

relevant feedback in terms of token economy. However,

this study focuses on neural activation patterns and more

specific experiments are needed to consolidate these

assumptions.

In conclusion, our findings demonstrate the CID para-

digm to be a valid method to examine reward processing in

children and adults. By employing healthy young adults to

the original MID task by Knutson et al. (2001a), as well as

our modified CID task, a consistent neural activation

pattern was shown during the anticipation of reward. Pilot

findings also demonstrate validity of the CID task in

healthy children. Thus, the presented CID task can be

recommended for future studies on reward processing,

especially to assess possible vulnerability or developmental

factors during critical developmental periods in the onset of

psychiatric disorders. Our results enable the investigation

of neurobiological processes linked to reward-related brain

response in healthy children, as well as in children with

psychiatric disorders.

Acknowledgments We thank all participants and collaborators for

supporting this study.

Conflict of interest The authors declare that they have no conflict

of interest.

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