The neuropsychology of the human reward system : impaired gambling
performance in ADHD children and adults with psychopathic tendencies
Habib M.*, Boulanger C.**, Lançon C.**,
Soubias M.*, Delarbre C.*, Joly-Pottuz B*.
*Pediatric Neurology, University Hospital of Marseille & I.N.C.M., CNRS, Marseille, France
** Department of Psychiatry, Sainte-Marguerite Hospital, Marseille, France
INTRODUCTION / RATIONALE
SUMMARY
Since the seminal work of the Damasio's group, reward processing has been explored
using gambling tasks in which people have to make their decision by choosing between
four card decks providing either small but durable rewards or immediate larger rewards
but leading to more risky and finally less advantageous outcomes. Here we present
evidence of impaired decision-making measured with the gambling task in two
neurobehavioral conditions previously suspected of entailing a reward system
dysfunction: children with Attention deficit with Hyperactivity (ADHD: N=22), and young
adults with psychopathic tendency (N=20), both populations being compared to carefully
selected normal controls. In both cases, performance on the gambling task was clearly
impaired, with a tendency for both children and adults to prefer less advantageous
decks and to fail to improve their behavior throughout the task duration. For ADHD
children, failure to perform the task was unrelated to any of two versions of the Stroop
test. For psychopaths, gambling performance was marginally correlated to Stroop
performance, but was very significantly correlated to the degree of psychopathy
(assessed by the Hare's psychopathy check list). Interestingly, these correlations were
found in the control group as well. Taken together, these results suggest that ADHD
children as well as adults with psychopathy tendencies have a dysfunction in brain
reward mechanisms.
While ADHD and conduct disorders in children are classically viewed as two
frequently comorbid conditions, the relationship between children
behavioural disorders and adult psychopathy is unclear [1]. Psychopathy
itself remains a loose and debated concept, where, in addition to aggressive
and deceitful behaviours, persons are reported as showing shallow affect,
manipulativeness, selfishness, and lack of empathy, guilt or remorse [2].
Some of these personality traits are also found in children with conduct
disorders, in particular tendencies to deceit and manipulate, and more
generally to break rules, but also cruel behaviours, emotional dysregulation
and lack of empathy [3]. Finally, all these conditions share common
neuropsychological features, especially impulsivity, defective selection and
inhibition strategies [4], and finally defective decision making [5-7].
A neural circuitry, centred on the nucleus accumbens and related parts of
the striato-pallidum, is thought to entail the function of processing the reward
value of current or expected situations [8], in association with medial frontal
cortex, which is involved in reward-based action selection and evaluation of
action-outcome contingencies [9]. Such circuitry is believed to subserve the
process of decision making in tasks such as the Iowa gambling task.
The Iowa gambling task [10; 11]]
The task requires participants to select from one of four decks of cards that
are identical in physical appearance for 100 trials. Each card choice leads to
either a variable financial reward or a combination of a variable financial
reward and penalty. Unknown to participants, the rewards and punishments
on the decks have been fixed by the experimenter. For each selection from
decks A and B participants win $100 and from each selection from decks C
and D participants win $50. Every so often variable punishment is also given.
Overall, the high reward decks (A and B) give higher levels of punishment
whereas the low reward decks (C and D) give lower levels of punishment.
Thus, successful task performance relies on sampling more from decks C
and D than from decks A and B. It is
argued that the reward/punishment
schedule is opaque, such that
participants are unlikely to be able to
perform an exact calculation of net
gains and losses. To do well, it is
therefore claimed that participants
must rely on more ‘intuitive’
decision-making processes, in
particular the activation of somatic
marker biasing signals.
STUDY 1 : ADHD PATIENTS
IOWA GAMBLING TASK
POPULATION AND METHOD
•22 successive children with a diagnosis of ADHD
• (19 M, 7;9 to 14;4 y-o; µ=11)
•15 normal controls, matched on age, sex and
socio-economic status.
•All normal IQ
•17/22: hyperactive-impulsive type (Conners);
•5/22 : inattentive type, unmedicated
Cognitive assessment of inhibition:
2 forms of the Stroop Test
y = -,5x + ,9, r2 = 1,2E-2
40
0,5
0
bloc1-1
bloc1-2
bloc 1-3
bloc 1-4
bloc 1-5
-0,5
-1
-2
1-5+2-5
ADHD children show
persistent
disadvantageous
behaviour, while controls
increase their
advantageous drawings
1
1-5+2-5: exp
1-5+2-5: tém
30
y = -,3x + ,4, r2 = 6,6E-3
40
1-5+2-5: exp
1-5+2-5: tém
30
20
20
10
10
1-5+2-5
gambling session 1
-1,5
0
0
-10
-10
-20
-20
-30
-30
-40
-2
0
2
4
6
stroopA
8
10
12
-40
-2
14
0
2
4
6
stroopC
8
10
12
-2,5
-4
2
2
No correlation with either form of the Stroop task
ADHD
controls
-3,5
2
2
0
2
bloc5 2 -4
bloc 2 -5
0
0
4
2
4
6
4
-6
-4
-4
-4
-12
-10
10
12
10
-2
0
-2
3
4
4
6
4
12
18
-2
-4
-4
2
0
0
4
18
10
10
4
0
2
1
18
20
20
2
2
0
2
8
10
0
3 ,3 3 3 3 3 3 3 3 3 ,4 6 6 6 6 6 6 7 4 ,6 6 6 6 6 6 6 7
bloc 2 -1
bloc 2 - 2
bloc 2 -3
Dependant variable : nb drawing from
advantageous minus disadvantageous decks
gambling session 2
ADHD
controls
4
3
bloc 2 -3
bloc 2 -4
bloc 2 -5
1-5+2-5: exp
1-5+2-5: tém
30
20
20
10
10
0
-10
0
-10
-20
-20
-30
-30
-40
-5
0
5
10
15
20
Conners TDAH
25
-40
-2
30
0
2
4
6
8 10
conduites
12
14
16
18
2
moyenne 1
moyenne 2
-1
No correlation with either ADHD or conduct disorder rating
1
3 ,6 6 6 6 6 6 6 7 3 ,6 7 6 1 9 0 4 8 4 ,6 1 9 0 4 7 6 2
-2
y = -,8x + 2,7, r2 = ,1
40
1-5+2-5: exp
1-5+2-5: tém
30
Repeated measure ANOVA
1st session:
• group p=0.066
•Group x block p =0.083
2d session:
• group p=0.0508
•Group x block p =0.0011
5
y = -,4x + 4,3, r2 = ,1
40
1-5+2-5
-3
1-5+2-5
Diagnosing conduct disorder :
- qualitative : DSM-IV criteria : 12/22
TDAH, 0/15 controls
- quantitative: extended Conners’
questionnaire : answers to 6 specific
questions
CORRELATIONS
0
-1
STUDY 2 : PSYCHOPATHY
-2
bloc 1
bloc 3
bloc 4
bloc 5
IOWA GAMBLING TASK
CORRELATIONS
•Twenty young adults (18-40y) with DSM-IV axis II
diagnosis of antisocial personality disorder (SCID II)
r = ,431;p=0.0138
•20 age- and sex-matched controls
y = ,381x - 33,232, r
0
8
2 = ,333
list (PCLR)
Hare's psychopathy
Score check
total
POPULATION AND METHOD
bloc 2
-10
6
-20
4
Clinical assessment: PCL-R, Stroop
interference index, TMT, WCST
Emotional assessment: Alexithymia
(TAS-20)
Level of Empathy: cognitive (LEAS),
emotional (RME)
PCL-R: Psychopathy Checklist-Revised; TAS-20: Toronto Alexithymia Scale
TMT : trail-making test, WCST : Wisconsin card sorting test LEAS: Level of
emotional Awareness Scale; RME: Reading the Mind in the Eyes
2
0
psychopaths
controls
-2
indi cestrooptps
-30
-40
-50
-60
-70
-4
-80
-6
indi cestrooptps: Psychop
-90
indi cestrooptps: témoin
-100
-80
-8
-60
-40
-10
-20
0
20
40
60
40
Psychop
35
controls
30
25
20
15
10
-80
-60
-40
21-40
41-60
61-80
81-100
BLOC
Correlation between the rate of disadvantageous
choice on gambling task and an index of sensitivity
to interference on Stroop Test.
Disadvantageous gambling
behaviour in psychopaths
compared to controls
F(1,38)=35,521, p<0,0001
40
60
r=0.713, p=0.0001
22,5
30
20
27,5
Psychop
Contr ols
17,5
25
Psychop
controls
22,5
empathie emot
15
TAS F3
20
Correlation with severity of
psychopathy (PCR-L)
r = ,492; p=0.0042
12,5
10
7,5
20
17,5
15
12,5
5
10
2,5
0
-80
0
(C+D)- (A+B)
(C+D)- (A+B)
1-20
-20
7,5
-60
-40
-20
0
20
40
(C+D)- (A+B)
Notwithstanding uncertainty about its ecological validity, the tendency to make risky choices observed in both ADHD
children and psychopath young adults on the Iowa Gambling task can be taken as a marker of impairment of the brain
mechanisms of reward in these two populations. More specifically, both populations perform on the Iowa gambling task in a
way very similar to that of neurological patients with orbital frontal lesions [12; 13]. Whereas the degree of such impairment
seems independent from cognitive (Stroop test) and behavioural (Conners rating scales) data in ADHD children, in adults with
psychopathic tendencies, disadvantageous gambling strategy seems to relate to the severity of psychopathy (as assessed on
the Hare’s psychopathy Check List), and to a lesser extent to the degree of dysexecutive functioning [14].
Moreover, impaired reward mechanisms seem to correlate with scores of emotional control, especially alexithymic traits
and deficient empathy, suggesting some common underlying mechanisms.
Interestingly, many of these correlations were also found among the control group, suggesting a continuum between
normality and pathology.
Finally, further exploring the relationship between pleasure seeking behaviours and awareness of emotional status and/or
experience, for oneself and for other persons, may prove an important objective for future research [15].
5
-80
-60
-40
-20
0
20
40
60
(C+D)- (A+B)
Correlation with alexithymia score
(Toronto Alexithymia Score)
DISCUSSION - CONCLUSIONS
60
Correlation with empathy
questionnaire
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