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Psychopharmacology (2010) 210:377–392

DOI 10.1007/s00213-010-1833-8

ORIGINAL INVESTIGATION

Impulsivity and executive functions


in polysubstance-using rave attenders
Antonio Verdejo-García & María del Mar Sánchez-Fernández &
Luisa María Alonso-Maroto & Fermín Fernández-Calderón & Jose C. Perales &
Óscar Lozano & Miguel Pérez-García

Received: 1 December 2009 / Accepted: 10 March 2010 / Published online: 13 April 2010
# Springer-Verlag 2010

Abstract Impulsive Behavior Scale, the delay-discounting question-


Objectives Rave parties are characterized by high levels of naire and a set of neuropsychological tests taxing different
drug use and polysubstance-using patterns that may be aspects of executive functions: response speed, working
especially harmful for psychological and neuropsychological memory, reasoning, response inhibition and switching,
functioning. The aim of this study was to conduct a self-regulation, decision making, and emotion perception.
comprehensive assessment of different aspects of impulsivity Results For impulsivity measures, RvA had significantly
and executive functions in a sample of polysubstance-using elevated scores on lack of perseverance and positive and
rave attenders. negative urgency, but did not differ from controls on lack of
Methods We collected data from two groups: rave attenders premeditation or sensation seeking. For neuropsychological
(RvA, n=25) and drug-free healthy comparison individuals functioning, RvA had significantly poorer performance on
(HCI, n=27). RvA were regular users of cannabis, cocaine, indices of analogical reasoning, processing speed, working
methampethamine, hallucinogens, and alcohol. The assess- memory, inhibition/switching errors, and decision making,
ment protocol included a drug-taking interview, the UPPS-P but performed similar to controls on indices of self-

María del Mar Sánchez-Fernández and Luisa María Alonso-Maroto


contributed equally to the development of this manuscript.
Electronic supplementary material The online version of this article
(doi:10.1007/s00213-010-1833-8) contains supplementary material,
which is available to authorized users.
A. Verdejo-García : M. Pérez-García F. Fernández-Calderón : Ó. Lozano
Department of Personalidad, Department of Psychology, Universidad de Huelva,
Evaluación y Tratamiento Psicológico, Huelva, Spain
Universidad de Granada,
Granada, Spain

A. Verdejo-García : M. Pérez-García J. C. Perales


Institute of Neuroscience F. Olóriz, Universidad de Granada, Department of Experimental Psychology,
Granada, Spain Universidad de Granada,
Granada, Spain
M. del Mar Sánchez-Fernández : L. M. Alonso-Maroto
Department of Psychology, Universidad de Jaén,
Jaén, Spain
A. Verdejo-García (*)
F. Fernández-Calderón Facultad de Psicología, Universidad de Granada,
Fundación Andaluza de Ayuda a las Drogodependencias Campus de Cartuja S/N,
e Inserción Social (FADAIS), 18071 Granada, Spain
Andalusia, Spain e-mail: averdejo@ugr.es
378 Psychopharmacology (2010) 210:377–392

regulation, reversal learning, and emotion processing. Peak and decision making in recreational users (De Sola et al.
and binge alcohol and drug use were positively correlated 2008; Fisk and Montgomery 2009; Hanson et al. 2008;
with positive urgency, and negatively correlated with Quednow et al. 2007). Nevertheless, some of these effects
performance on executive indices. have been attributed to the frequent co-abuse of cannabis
Conclusion Rave attenders have selective alterations of among MDMA recreational users (Clark et al. 2009; Croft
impulsive personality and executive functions. These et al. 2001; see Gouzoulis-Mayfrank and Daumann 2006
findings can contribute to delineate the neuropsychological for a review). Methamphetamine use has been related to
profiles that distinguish recreational polysubstance use from impaired performance on processing speed, response
substance dependence. inhibition, delay-discounting and decision-making tests
(Monterosso et al. 2005; Paulus et al. 2002; Salo et al.
Keywords Raves . Impulsivity . Executive function . 2005; see Scott et al. 2007 for a review). Furthermore,
Neuropsychology . Addiction . Prefrontal cortex . recent studies indicate that recreational use of drugs like
Inhibition . Drug abuse alcohol and cocaine can produce significant impairments
in particular components of executive functions, such as
response inhibition, switching (Colzato et al. 2007, 2009),
Introduction and decision making (Goudriaan et al. 2007; Johnson et al.
2008).
There is currently no consensus on the best definition for The fact that these drugs are frequently co-abused in a
“rave” (Boeri et al. 2004). However, there are a number of single rave session raises additional questions about their
common characteristics which are typical of these types of additive deleterious (or protective) effects on brain function
parties: they are held in venues of difficult access (deserted and neuropsychological performance (Bolla et al. 2000;
buildings, beaches, mountains, or forests) (Anderson and Gonzalez et al. 2004; Jatlow 1993). Similarly, the fact that
Kavanaugh 2007), they are long-lasting and alternative to these drugs are frequently used in “binge” patterns also raise
the typical recreational circuits (Boeri et al. 2004), they are concerns on increasingly detrimental neuropsychological
self-organized and without commercial purposes, and they effects (Field et al. 2008; Stephens and Duka 2008). On
revolve around music (Sanders 2006) and dance (Romaní the other hand, many “rave attenders” seem to be somewhat
and Sepulveda 2005). Rave attenders have been character- resistant to addiction, since they are able to parcel out
ized as a fragmented “subculture” (Goulding et al. 2002), consumption periods from adaptive standard activities,
meaning they are made up by socially integrated people making up an interesting model of drug exposure without
who maintain normalized activities and lifestyles according drug dependence. Although this characteristic may be partly
to their societies' standards, but who spend part of their shared with other polysubstance abusers who maintain a job
leisure time attending raves. Therefore, all classes or social, or courses of studies, the “rave attenders” constitute a
economic, and cultural levels can be equally represented in uniquely homogeneous subculture characterized by coupling
these parties (Abanades et al. 2004; Kavanaugh and high levels of drug use with low rates of treatment demand,
Anderson 2008). being neatly fragmented (drug use is typically restricted to
On the other hand, raves are also characterized by high the rave environment), and lacking some of the socio-
levels of drug use and frequently by polysubstance-using demographic (low education or IQ) and psychopathological
patterns (Forsyth 1996; Riley and Hayward 2004), which (e.g., anxiety or depression) confounders usually found in
may be especially harmful for general and brain health. The more heterogeneous samples of polysubstance abusers
preferred drugs among rave attenders are known as “club (Goulding et al. 2002; Kavanaugh and Anderson 2008).
drugs” or “dance drugs” (including 3,4-methylenedioxyme- Furthermore, the rave movement has similar common
thamphetamine (MDMA), methamphetamine, or gamma characteristics in different countries across Europe, and
hydroxybutyrate among others), but considerable rates of therefore our results could be more readily generalized
alcohol, cannabis, cocaine, and hallucinogens use are also (than in the case of a more heterogeneous group of
detected (Barrett et al. 2005; Boys et al. 1997; Lenton et al. polysubstance abusers) and their clinical implications
1997; Yacoubian et al. 2003). The use of several of these could be useful to prevention or clinical approaches in
drugs have been associated with significantly elevated levels different countries.
of impulsivity, which are regarded as having dysfunctional Both impulsivity and executive functions are key con-
and detrimental effects on neuropsychological perfor- structs to explain processes of vulnerability to drug use, drug
mance measures (see Verdejo-García et al. 2004, 2008 self-administration patterns, transition to drug dependence,
for reviews). MDMA use has been associated with and different drugs use-related consequences (Belin et al.
significant declines on measures of processing speed, 2008; Dalley et al. 2007; Verdejo-García et al. 2008).
verbal fluency, working memory, reflection impulsivity Furthermore, both of them are complex multidimensional
Psychopharmacology (2010) 210:377–392 379

constructs that need to be addressed by comprehensive Measures


assessments (Verdejo-García and Pérez-García 2007;
Verdejo-García et al. 2008); no studies to date have Information on patterns of drug use
performed such a comprehensive assessment in groups of
rave attenders. The main aims of the study were: (1) To Interview for Research on Addictive Behavior—revised
assess multidimensional aspects of impulsivity. (2) To (IRAB; Verdejo-García et al. 2005) This interview provides
characterize neuropsychological performance on executive an estimation of several patterns of drug taking referring to the
function measures in polysubstance-using rave attenders, as multiple substances used by this sample of rave attenders.
compared to drug-free comparison individuals. These drug use parameters included: (1) average regular and
peak monthly use of each substance (regular quantity per
month and peak quantity per month), (2) total duration of use
Methods of each substance (duration in years), and (3) age at onset of
use of each substance. We also collected information on
Participants patterns of binge use of each of the substances by querying
about the maximum amount of units of a certain drug taken in
Twenty-five regular rave attenders and 27 healthy compar- the time frame of 1 h. Descriptive scores for all these variables
ison individuals participated in this study. Rave attenders in the present sample are displayed in Table 2. Inter-
were recruited through a non-governmental organization correlations between the patterns of use of the different
(Energy Control) specialized in providing harm reduction drugs taken by the rave attenders group in the last month are
guidelines among drug users. Specifically, we used mailing displayed in Table 3. Since we performed 45 different
lists and web-based adverts to recruit rave attenders among correlations, we adjusted the alpha level following the
members and users of this organization. Inclusion criteria Bonferroni correction (0.05/45=0.001) to avoid inflated type
were: (1) having attended at least one rave in the last year I error. Therefore, in Table 3, we only report as significant
(descriptives for self-reported rave attendance in the last those correlations yielding a p value below 0.001.
year are reported in Table 1), (2) being polysubstance users
of at least two of the following drugs: cocaine, metham-
phetamine (speed), MDMA, hallucinogens, ketamine, or Questionnaire measures of impulsivity
opiates, which are typically used at rave settings, and (3)
being otherwise healthy, i.e., never sought or received UPPS-P impulsive behavior scale (Whiteside and Lynam
treatment for neurological, psychiatric, or systemic diseases 2001) This scale is a 59-item inventory designed to measure
affecting the central nervous system. Healthy comparison five distinct personality pathways to impulsive behavior:
individuals were recruited through word of mouth among negative urgency, lack of perseverance, lack of premeditation,
friends and acquaintances of the research team who fulfilled sensation seeking, and positive urgency. The total scores of
criterion (3) and did not meet criteria (1) and (2). Both each of these five dimensions were obtained for analyses.
groups had similar (non-significantly different) distributions
for sex, age, education, depression symptoms, and anxiety Delay-discounting questionnaire, now or later (Kirby et al.
symptoms (the two latter measured with the Hamilton 1999) This is a monetary-choice questionnaire asking for
scales) (Table 1). As intended, both groups sharply differed individual preferences between smaller, immediate rewards
on patterns of drug taking: healthy comparison individuals and larger, delayed rewards varying on their value and time
had only used tobacco and alcohol (regularly) and to be delivered. The questionnaire is composed of a fixed
marijuana (incidentally, none of them had regular cannabis set of 27 choices; the amounts of money and delays used in
use) throughout their lifetime. all 27 trials are reported in Kirby et al. (1999). The

Table 1 Descriptive scores


and between-group comparisons RvA (n=25) HCI (n=27) Chi-square or t test p
for socio-demographic and
psychological measures of rave Number of raves attended (last year) 9.75 (5.89)
attenders (RvA) and healthy Gender (% male) 60% 44.4% 1.258 0.262
control individuals (HCI) Age (Mean, SD) 24.92 (3.07) 25.22 (4.04) −0.3 0.76
Years of education (mean, SD) 14.1 (2.85) 14.2 (2.55) −0.087 0.931
Anxiety (mean, SD) 6.72 (7.42) 5.96 (5.88) 0.409 0.684
Depression (mean, SD) 3.88 (4.53) 3.74 (4.26) 0.114 0.909
380 Psychopharmacology (2010) 210:377–392

Table 2 Descriptive scores of consumption patterns for the different drugs used in the polysubstance-using rave attenders group

Drugs Any time (%) Last Quantity LM Quantity RU Quantity MxU Binge use Abstinence
month (%) mean (SD) [Mdn] mean (SD) [Mdn] mean (SD) [Mdn] mean (SD) (week) mean
[Mdn] (SD) [Mdn]

Marihuana 96 80 10 (20.3) [3] 16.5 (23.1) [6] 36.7 (35.2) [26] 1 (1) [0.6] 56.8 (113.7) [9]
Hashis 96 84 24.4 (30.2) [12] 27.3 (29.3) [16] 39.2 (32.2) [31] 1.4 (1.4) [1] 3.8 (4.7) [2]
Cocaine 80 48 11 (13.7) [4.5] 8.1 (14.7) [0.55] 23.9 (38.7) [6] 0.5 (0.3) [0.4] 48.7 (80.2) [12]
Amphetamine 28 12 – 2.7 (2.3) [1.5] 40.6 (88.8) [1.5] 1 (0.5) [1] –
Speed (meth-) 92 52 5.4 (6) [2] 4.5 (4.4) [3] 9.6 (13.4) [6] 0.6 (0.5) [0.5] 18.8 (21.3) [4]
Hallucinogens 76 44 1.2 (1) [1] 0.9 (0.6) [1] 3 (4.6) [1] 0.7 (0.5) [0.5] 26 (31.7) [10]
MDMA 88 28 2.7 (3.5) [2] 2.1 (2.1) [1] 4.8 (4.2) [4.2] 0.4 (0.4) [0.2] 30.8 (22.1) [24]
Benzodiazepine 8 8 – – – – –
Ketamine 12 8 – – – – –
Tobacco 96 92 333.5 (226.9) [270] 368.7 (223.2) [300] 515.8 (327.1) [580] 4.7 (4) [5] –
Wine & Beer 96 96 40.7 (26.7) [30] 53 (46.6) [45] 68 (48.8) [60] 2.8 (1.9) [2] –
Liquors, Cocktails, 92 80 34.9 (26.4) [30] 41.6 (35.2) [42] 68.3 (47.8) [60] 2.9 (1.5) [3] –
Mixers

For those drugs with less than 20% of responses (n<5) we did not display mean, SD, or median values
Mdn Median, quantity LM quantity of use in the last month, quantity RU quantity of use during regular use, quantity MxU quantity of use during
maximum use

dependent measure was based on the area under the curve participants to replace numbers with specified symbols as
(AUC) methodology (Myerson et al. 2001), as employed in fast and accurately as possible. This is followed by the
recent studies investigating delay discounting in substance incidental memory probe which tests participants learning
abusers (Field et al. 2006; Field et al. 2007). The AUC was of the association between numbers and codes. In the
calculated for each of the three reward magnitudes included copy subtest symbols (rather than numbers) are printed in
in the questionnaire (small, medium, and large), according the upper half of each box; participants are instructed
to the formula (x2−x1)[(y1−y2)/2], where x1 and x2 are simply to copy each symbol into the lower half. The
successive delays, and y1 and y2 are the subjective values main dependent measures were the raw scores from the
associated with these delays. This formula defines different three subtests.
trapezoids, and the area under the empirical discounting
function is equal to the sum of the areas of these trapezoids. Working memory—letter number sequencing (LNS) (Wechsler
1997) Participants are asked to listen a sequence in which
letters and numbers are combined, and are asked to
Neuropsychological assessment reproduce the sequence, first placing the numbers in
ascending order and then the letters in alphabetical order.
Processing speed—digit symbol (coding, incidental learning, The dependent variable from this test was the total number
and copy) (Wechsler 1997) Digit symbol coding requires of hits.

Table 3 Intercorrelations
between the use of the different Marih Hashis Cocaine Amph Speed Halluc. MDMA Keta. Tob.
substances during lifetime
Marih. 1
Hashis 1a 1
Correlation analyses were Cocaine 0.102 0.102 1
conducted using the phi Amph. 0.327 0.327 0.134 1
coefficient for dichotomic
Speed 0.060 0.060 0.147 0.183 1
variables
Halluc. 0.115 0.115 0.047 0.067 0.166 1
Marih. marihuana, Amph.
amphetamine, Halluc. MDMA 0.075 0.075 0.123 0.318 0.109 0.081 1
hallucinogens Ketamine 0.075 0.075 0.123 0.044 0.345 0.081 0.621a 1
a
Significant correlations after Tobacco 0.042 0.042 0.102 0.127 0.692a 0.115 0.075 0.075 1
Bonferroni corrections: 0.05/45, Alcohol 1a 1a 0.102 0.327 0.060 0.115 0.075 0.075 0.042
p<0.001
Psychopharmacology (2010) 210:377–392 381

Analogical reasoning—similarities (Wechsler 1997) Pairs whether the absence of response had been right (no-go
of words are read that represent common objects or trials) or wrong (go trials). The main dependent variables
concepts, and participants have to indicate how these from this test were hit and false alarm rates. These variables
objects/concepts are similar or what they have in common. were analysed across six blocks of 10 trials to explore
The dependent variable from this test was the number of effects of learning and switching during the task.
correct answers.
Reversal learning—probabilistic reversal The task was
Attentional interference/response inhibition and switching— based on the Probabilistic Reversal Learning (PROB)
Stroop test (Delis–Kaplan Executive Functions System; Delis described in Swainson et al. (2000). Briefly, each trial of
et al. 2001) This test consists of four different conditions, the task involves the simultaneous presentation of two
each containing 50 items. The first condition presents stimuli (two squares, drawn in thick colored lines) that
patches of colors and participants have to name them as differ only in line color. In each phase of the task, one
quickly and accurately as they can. The second condition stimulus is considered the “correct” one, as choosing it
presents the words “red”, “blue”, and “green” printed in provides reward in most cases, and the other is the “wrong”
black ink and participants are asked to read aloud the words one, as choosing it was penalized most of the times. The
written. The third condition introduces the condition of stimuli shifted positions randomly to avoid the motor
interference: the words “red”, “blue”, and “green” are perseveration.
printed in incongruent colors ink and participants have to In phases 1 and 2 of the task (trials 1–80), the correct
name the color and ignore the word. In the fourth condition, selection was probabilistically rewarded in 7 out of 10
the items are similar to condition three but participants have cases, and penalized 3 out of 10; and the incorrect selection
to switch their response between naming the color of the was penalized in 7 out of 10 trials, and rewarded in the
ink and ignoring the word or reading the word (when the remaining 3 out of 10. This means that on 30% of the trials,
item is inside a little box). The main dependent variables the computer provided false feedback, i.e., selecting the
used in this test were the composite time measures: correct stimulus was followed by false negative feedback
inhibition vs. color naming (time part 3–time part 1) and and selecting the incorrect one was followed by false
switching vs. inhibition (time part 4–time part 3), and the positive feedback (still, for the sake of simplicity, we keep
number of unadverted and self-corrected errors committed on labelling the two colors as “correct” and “incorrect”, as,
in conditions 3 (inhibition errors) and 4 (switching errors). a priori, the former is the one most likely to be rewarded,
and the latter the least likely to be rewarded). Negative and
Motor response inhibition—no/no go A computer-based positive feedback were presented acoustically (by two
implementation of the go/no-go task was used (Verdejo- different tones), and involved winning or losing five points.
García et al. 2007b). The task consisted of 60 trials. In the The total amount of points accrued so far was continuously
first 30 trials (pre-switch), participants were asked to press present on one corner of the screen.
a key as quickly as they could whenever the go stimulus (a Phases 3 and 4 (trials 81–160) were identical to phases 1
letter) was presented, and to withhold the response when and 2, respectively, but the probability of rewarding for the
the no-go stimulus (a different letter) was presented. The correct response was lowered to 60% and the proportion of
assignation of stimuli to the go and no-go conditions were rewarding for the incorrect one was raised to 40%.
counterbalanced across subjects. In the second 30 trials of Most importantly, the color corresponding to the right
the task (post-switch), participants were asked to switch the choice and the one corresponding to the wrong choice
assignation of the response from the go to the no-go shifted after every 40 trials (after every phase), that is, the
stimulus (which obviously became the post-switch go trial); stimulus that was previously correct became incorrect, and
in other words, they were asked to respond to the vice versa (see Table 4).
previously no-go stimulus and not to respond to the The main dependent measure for this task was the
previously go stimulus. The proportion of go vs. no-go proportion of correct choices for each 5-trial block in each
trials on both phases (pre- and post-switch) was 70/30. The task phase (1–4). Extra analyses were carried out on the
inter-stimulus interval (ISI) was set at 100 ms, and each probability of holding the prior trial choice after being
stimulus was presented during 1,000 ms. Auditory feedback rewarded, and after being penalized. This second dependent
(one of two distinctive sounds) was provided after each measure is aimed at detecting differential choice dependen-
response to indicate whether that response had been right or cies on reinforcement and punishment for the two groups.
wrong. If participants did not respond in the 1,000 ms
response window, the two same sounds were used as Self-regulation—Revised Strategy Application Test (R-SAT)
positive and negative feedback for not responding. That is, (Levine et al. 2000) This is a multitasking test that consists
if no response was given, the same sounds indicated of three types of activities: figure tracing, sentence copying,
382 Psychopharmacology (2010) 210:377–392

Table 4 Top panel depiction of events' sequence in each single trial during the probabilistic reversal task; bottom panel reward/penalization
contingencies for each of the two options in each phase of the task
a) Event sequence during the probabilistic reversal learning task.

1. Warning cue 2. Choice options 3. Choice 4. Feedback

b) Reward/penalization contingencies during the probabilistic reversal learning task.


1st Phase: Acquisition (trials 1-40).
-Black square: “Correct”, 70% of choices of this stimulus rewarded,
30% penalized.
-Grey square: “Incorrect”, 30% of choices of this stimulus
rewarded, 70% penalized.

2nd Phase: Reversal 1 (trials 41-80).


-Black square: “Incorrect”, 30% of choices of this stimulus
rewarded, 70% penalized.
-Grey square: “Correct”, 70% of choices of this stimulus rewarded,
30% penalized.

(No reversal warning provided)

3rd Phase: Reversal 2 (trials 81-120).


-Black square: “Correct”, 60% of choices of this stimulus rewarded,
40% penalized.
-Grey square: “Incorrect”, 40% of choices of this stimulus
rewarded, 60% penalized.

(No reversal warning provided)


4th Phase: Reversal 3 (trials 121-160).
-Black square: “Incorrect”, 40% of choices of this stimulus
rewarded, 60% penalized.
-Grey square: “Correct”, 60% of choices of this stimulus rewarded,
40% penalized.

(No reversal warning provided)

In the actual task the stimuli were of two different colors randomly chosen from the green, yellow, red, and blue set; and the positions (right/left)
of the colors were randomly set. Messages on screen have been translated from Spanish. The “hand” icon for the illustration in each phase (bottom
panel) signals the correct (most probably reinforced) option

and object numbering. The activities are presented on two (to-be-discovered) is to complete only the brief items to the
different stacks (A and B), each containing 120 items. The exclusion of lengthy items, which the subjects must learn to
main goal of the task is to win as many points as possible, skip as they are introduced in later pages of the test; this
considering that large items score 0 points, and small items way subjects can optimize long-term profit by completing
score 100 points each. However, both small and large items more items during the time limit. We also asked participants
can be of different difficulty: some of them are easy and to tick a box every time they thought 1 min had passed (we
quick to complete (i.e., they take a couple of seconds and previously asked them to remove their watches if they had
are defined as “brief items”) whereas others are very any). The main dependent variable from the R-SAT is the
laborious and time-consuming (i.e., they can take longer proportion of brief items completed in relation to the total
than 1 min and are defined as “lengthy items”). Given the number of items attempted. Additional dependent measures
limitation of time (10 min), the most efficient strategy are: the number of action slips (number of obvious motor
Psychopharmacology (2010) 210:377–392 383

inhibition mistakes; e.g., completing large items) and the scheduled testing session. All testings were conducted on
proportion of time marks with respect to the total number of human research testing rooms at the Biomedical Research
minutes employed (i.e., this is a measure of appropriate Building of the Institute of Neuroscience (University of
time estimation during task performance). Granada). Prior to study onset, all participants signed an
informed consent form. Abstinence status was self-reported
Affective decision making—Iowa gambling task (IGT) by participants before testing session onset; no other
(Bechara et al. 2001) This is a computer task that factors objective abstinence checks were conducted because
several aspects of decision making, including uncertainty, participants were not treatment-enrolled or treatment
risk, and evaluation of reward and punishing events. The seekers and there was no objective reason to provide
IGT involves four decks or cards, decks A′, B′, C′, and D′. inaccurate information to researchers. Questionnaires and
Each time a participant selects a card, a specified amount of neuropsychological tests were administered by Ph.D.
play money is awarded. However, interspersed among these students with a master's degree in clinical psychology.
rewards, there are probabilistic punishments (monetary The IRAB was administered first and then questionnaire
losses with different amounts). Two of the decks of cards measures were counterbalanced across subjects. Neuropsy-
(A′ and B′) produce high immediate gains; however, in the chological tests administration was arranged to alternate
long run, these two decks will take more money than they between verbal and non-verbal tasks and between more and
give, and are therefore considered to be the disadvanta- less demanding tasks; these tests were administered in a
geous decks. The other two decks (C′ and D′) are fixed order to all participants. The total duration of the
considered advantageous, as they result in small, immediate session was approximately 2 h. Participants were paid 15
gains, but will yield more money than they take in the long euros for their collaboration. We made clear before the
run. The main dependent variable from this task was the net initial interviews that in case of reporting having taken any
score for each block of the task (5 blocks of 20 trials). We drug, the testing session would be simply rescheduled but
calculated net scores by subtracting the number of they would not miss the opportunity to participate in the
disadvantageous choices (decks A and B) from the number study.
of advantageous choices (decks C and D) for each block.
We also calculated the global IGT net score applying the Data analysis
same formula to the 100 trials of the task.
Statistical analyses were implemented on SPSS v.17. We first
Test of emotion recognition: Ekman Faces Test (EFT) (Young explored dependent variables to examine missing data points
et al. 2002) The Ekman Faces Test (EFT) is a computer task and normality of distributions (tested by Kolgomorov–
that assesses recognition of facial emotional expressions. Smirnov tests) and presence of outliers (defined by the
The task uses stimuli from the Facial Expressions of Explore command of SPSS v.17). Data from some neuropsy-
Emotion: Stimuli and Tests (FEEST; Young et al. 2002). chological measures were missing due to technical problems
A series of 60 stimuli featuring faces portraying basic during data collection (the sample size of the rave attenders
emotions were presented. Faces depicted expressions of group is n=23 for the Stroop and digit symbol measures, and
anger, disgust, fear, happiness, sadness, and surprise n=24 for similarities). On those variables that followed a
(6 emotions, 10 faces each). Photographs were posed by each normal distribution (UPPS-P subscales, delay discounting
of 10 models (six female, four male). Each face was presented AUC, LNS, similarities, symbol digit, Stroop composite time
on a computer monitor for a maximum of 5 s and individuals scores, go/no go, probabilistic reversal, Ekman faces test,
were asked to select one of the six expression labels (listed and Iowa gambling task) we conducted independent samples
above) that best described the emotion expressed. The labels t tests to examine differences between rave attenders and
were visible throughout testing, thus minimizing working healthy comparison individuals. On those variables that
memory demands, and individuals were given as much time failed to meet normality assumptions (Stroop number of
as they required to respond. No feedback was given regarding errors and self-corrections and R-SAT) we used non-
the appropriateness of their responses. We obtained the sum parametric Mann–Whitney U tests to examine differences
score of total correct identifications (total recognition, ranging between rave attenders and healthy comparison individuals.
0–60) as the dependent variable. We also conducted mixed-design repeated measures
ANOVAs to track task performance dynamics on the go/
no-go, the probabilistic reversal, and the IGT. In addition, to
Procedure further explore the association between patterns of drug use
and trait impulsivity and neuropsychological performance,
All participants were asked to abstain from any drug taking we performed four series of bivariate correlation analyses
(with the exception of tobacco) for at least 48 h before the between (1) peak quantity of use of each drug, (2) duration
384 Psychopharmacology (2010) 210:377–392

of use of each drug, and (3) binge use of each drug and the symbol (coding and incidental learning), t=−2.28, df=1,
dependent variables. We restricted these correlation analyses 48, p<0.05 and t=−2.21, df=1, 48, p<0.05, respectively,
to those drugs that had been used by at least by 70% of rave R-SAT number of time marks, U=213, df=1, 50, p<0.05,
participants (cannabis, cocaine, methamphetamine, MDMA, and IGT net score, t=−1.99, df=1, 50, p=0.05 (see Table 5).
hallucinogens, and alcohol) and to the dependent variables Rave attenders also committed significantly more errors on
that differed significantly between groups. Furthermore, due the third condition of the Stroop (inhibition), U=219.5, df=1,
to the considerable number of correlation analyses, we 48, p<0.05, and significantly more self-corrections on the
applied Bonferroni correction and set the alpha level for fourth condition of this test (switching), U=214.5, df=1, 48,
statistical significance at p≤0.001 (0.05/48 contrasts) to p<0.05 (see Table 5). Following Cohen´s interpretation of
protect against inflated type 1 error. effect sizes (Zakzanis 2001), the effect size of group
differences was large for similarities, medium-large for
incidental learning, medium for coding, LNS, Stroop
Results inhibition and switching errors, and IGT, and small for
R-SAT number of time marks. We found no significant
Questionnaire measures differences between groups on the remaining dependent
variables.
Rave attenders scored significantly higher than healthy
comparison individuals on the UPPS-P subscales of IGT learning curve
negative urgency, t=2.61, df=1, 50, p<0.05, positive
urgency, t=2.04, df=1, 50, p<0.05, and (lack of) persever- For the IGT, the learning curve was explored using a 2
ance, t=2.94, df=1, 50, p<0.05 (see Fig. 1). Following (group) × 5 (block) mixed-design ANOVA. Results showed
Cohen´s interpretation of effect sizes (Zakzanis 2001), the no significant effects of group or the group × block
effect size of group differences was large for (lack of) interaction. Visual inspection of the plot indicated that the
perseverance, and medium for positive urgency and lack of effects was probably due to the fact that healthy
negative urgency. We did not find significant differences comparison individuals did not develop steady learning
for (lack of) premeditation, t=2.94, df=1, 50, p>0.1, and across blocks (see Supplementary material).
sensation seeking, t=0.60, df=1, 04, p>0.1. We also failed
to find significant differences for the different reward In-depth analysis of go/no-go and probabilistic reversal
magnitudes of the delay-discounting AUC: small, t=0.57,
df=1, 50, p>0.1, medium, t=0.52, df=1, 50, p>0.1, and Rave attenders and controls also differed in their dynamic
large, t=−0.04, df=1, 50, p>0.1. response patterns in the go/no-go and reversal learning
tasks.
Neuropsychological measures Hit rate in the go/no-go task was computed as the ratio
between hits and the sum of hits and misses. Figure 2 (top
Rave attenders performed significantly more poorly than panel) shows mean hit rates for each block and each group.
healthy comparison individuals on LNS, t=−2.21, df=1, 50, Only the effect of block was significant, F(5, 230)=6.717,
p<0.05, similarities, t=−5.02, df=1, 49, p<0.001, digit MSE=0.017, p<0.001. As can be seen in the figure, hit
rates gradually grew across blocks and locally decreased
50.00 when the letter assignation to the go and no-go stimuli was
45.00 Rave attenders
Healthy Comparison Indiv. shifted (after block 3). Rates returned to asymptotical
40.00
values right after the post-shift block. This pattern was
UPPS Scores

35.00 * *
30.00 qualitatively and quantitatively similar for the two groups,
*
25.00 although the main effect of group was not far from
20.00 significance [F<1 for the block×group interaction, and
15.00 F(1, 46)=2.659, MSE=−0.035, p=0.109 for the main
10.00 group effect].
5.00
False alarm rates in the go/no-go task (computed as the
0.00
Neg. Ur. Pos. Ur. (lo) Prem (lo) Pers Sseek ratio between the number of false alarms and the sum of
UPPS Dimensions false alarms and correct rejections) yielded significant
differences between groups (see Fig. 2, bottom panel).
Fig. 1 Descriptive scores and significant differences between groups
on the UPPS-P dimensions. Effect sizes for variables showing
Neither the main effect of block [F(5, 230)=1.443, MSE=
significant differences were d=0.72 for negative urgency, d=0.56 for 0.069, p=0.209] nor the main effect of group (F<1) reached
positive urgency, and d=0.81 for lack of perseverance significance. However, the interaction [F(5, 230)=2.250,
Psychopharmacology (2010) 210:377–392 385

Table 5 Descriptive scores and


between group comparisons for Test Dependent variables RvA HCI t/U p ES
neuropsychological performance
of rave attenders (RvA) and Digit symbol Coding 70.47 (19.46) 80.56 (11.17) −2.28 0.03 0.65
healthy control individuals Inc. learn. 7.35 (1.40) 8.26 (0.76) −2.91 0.005 0.75
(HCI) Copy 115.91 (28.91) 120.81 (15.01) −0.73 0.45
LNS Hits 10.36 (2.94) 12.11 (2.76) −2.21 0.03 0.59
Similarities Hits 13.12 (4.00) 19.67 (5.14) −5.02 0.000 1.41
Stroop Inhibition vs. Col. N 20.61 (11.01) 19.70 (16.10) 0.23 0.82
Switching vs. inhibition 7.61 (13.47) 1.03 (16.13) 1.55 0.13
Errors inhibition 1.09 (1.50) 0.44 (0.84) 219.5 0.04 0.56
Errors switching 0.87 (1.14) 0.56 (0.97) 257.5 0.24
Self-corrections inhibition 1.18 (1.26) 1.07 (1.24) 279.5 0.71
Inc. learn incidental learning, Self-corrections Switching 1.17 (1.43) 0.44 (0.69) 214.5 0.04 0.67
LNS letter number sequencing, R-SAT Proportion brief items 0.84 (0.10) 0.87 (0.11) 274.5 0.25
Stroop Col. N. Stroop colour Action slips 1.76 (2.39) 1.59 (3.04) 292.5 0.38
naming, R-SAT revised-strategy
application test, IGT Iowa gam- Time marks/real time 0.70 (0.18) 1.01 (1.01) 213 0.02 0.42
bling task, EFT Ekman faces IGT Net score −4.36 (16.19) 5.11 (17.90) −1.99 0.05 0.55
test, ES effect size calculated as EFT Total recognition hits 48.16 (7.06) 50.04 (4.47) −1.15 0.25
Cohen's d

MSE=0.069, p=0.050] between the two factors unveiled cance when the analysis was restricted to phases 1 and 2
differential block effects across groups. Specifically, controls [Fs for the block×group interaction were F(7, 350)=2.039
showed a fairly constant false alarm rate across the whole and F(7, 350)=2.039, p=0.049 and p=0.013, for phases 1
task (between 0.20 and 0.30, approximately), whereas rave and 2, respectively], but not in phases 3 and 4 [F<1 in both
attenders showed a normal false alarm rate in the pre-shift cases]. As can be seen in the figure, in both phases, the
blocks (1–3), and an anomalously high rate after shift proportion of correct choices reached higher levels in the
(blocks 4–6). In other words, shift seemed to provoke an group of rave attenders than in the group of controls.
abrupt rise in false alarms (the probability of responding to This pattern can be explained by three possible sub-
the no-go trials) that remained approximately constant during patterns: (1) rave attenders are less prone to change their
the rest of the task. This impression was confirmed by the choice when they were penalized for choosing that option
detailed analysis of the interaction. Restricted ANOVAs in the previous trial (low relative sensitivity to punishment);
showed that the effect of block was not significant for (2) they are more prone to hold their choice when they are
controls, F<1, but was significant for rave attenders, F(5, rewarded (high relative sensitivity to reward); or (3) they
110)=2.58, MSE=0.078, p=0.03. More specifically, LSD are both oversensitive to reward and undersensitive to
tests showed this effect to be exclusively due to the penalization. In accordance with this, we calculated the
difference between blocks 3 and 4 (p=0.03). On the other probability of holding the choice after being penalized and
hand, the difference between rave attenders and controls was after being rewarded in each 20-trial block and each phase
not significant in any of the blocks (min p=0.13). for each group. Figures 4 and 5 display these probabilities
Performance in the reversal learning task was firstly across block and phase conditions. Groups did not differ in
analyzed in a standard fashion, computing the proportion of their sensitivity to punishment (Fig. 4), as their tendency to
correct choices for each five trial block in each 40 trial hold the same choice after being penalized did not differ
phase, for the two groups. As expected (see Fig. 3), the across blocks (F<1) for all interactions involving the group
proportion of correct choices gradually grew across blocks factor. Only the effect of block was significant, as the
in each phase, F(7, 350)=37.145, MSE=0.064, p<0.001. probability of holding the choice was consistently higher
Globally, the proportion of correct choices was also higher for the second half of each phase than for the first half,
in phases 1 and 2, than in phases 3 and 4, F(3, 150)=6.887, F(1, 50)=30.780, MSE=0.038, p<0.001.
MSE=0.142, p<0.001 (note that in phases 1 and 2 the Results regarding sensitivity to reward seem to be clearer
proportion of reinforced “correct” choices was 0.70, (Fig. 5). The probability of holding the choice after being
whereas it was 0.60 in phases 2 and 3; so this effect reflect rewarded varied across phases, F(3, 150)=5.23, MSE=
sensitivity of choices to reinforcement levels). Most 0.030, p=0.002. More interestingly, although the effect of
interestingly, however, block marginally interacted with group was not globally significant, F(1, 50)=2.870, MSE=
group, F(7, 150)=1.867, MSE =0.064, p=0.074. This 209, p=0.096, it was significant when restricted to phase 2,
marginally significant interaction clearly reached signifi- F(1, 50)=4.485, MSE=0.083, p=0.039. We are aware that it
386 Psychopharmacology (2010) 210:377–392

Hit rate (h) rates across blocks


performance on similarities, r=−0.53, p=0.000. In addition,
peak amount of use of cocaine, r=0.66, p=0.001 was
1.0 significantly correlated with Positive Urgency.

Total duration of use Duration of hallucinogens use was


significantly correlated with LNS performance, r=−0.75, p=
h (hit rate)

0.8 0.000. Duration of alcohol use was significantly correlated


with similarities performance, r=−0.48, p=0.001.

Binge use (number of units used in a row during a 1-h period)


0.6 Binge use of methamphetamine (speed) was significantly
correlated with R-SAT number of time marks, r=0.61, p=
1 2 3 4 5 6
0.001. In addition, binge use of alcohol was significantly
Block correlated with Positive Urgency, r=0.46, p=0.001.
False alarm rates (f) across blocks
0.6

Discussion
f (false alarm rate)

0.4
The results from the study showed that polysubstance-using
rave attenders had significantly elevated scores on impul-
sivity indices of lack of perseverance and positive and
0.2 negative urgency, and a significantly poorer performance
on indices of processing speed, working memory, analog-
ical reasoning, inhibition/switching errors, time estimation,
and decision making. The effect size of group differences
0.0 were large for the personality trait of lack of perseverance
1 2 3 4 5 6
Block and cognitive indices of incidental learning (in the context
of fast/accurate processing speed demands) and analogical
Fig. 2 Mean hit rate across blocks in the go/no-go task for the control
reasoning and medium for all other indices (with the
and rave attending participants (top panel). Mean false alarm rates rate
across blocks in the go/no-go task for the control and rave attending exception of a small effect size for an index of time
participants (bottom panel) estimation). On the other hand, rave attenders did not differ
from drug-free controls on indices of inhibition/switching
time cost, self-regulation or emotional perception, and
could be argued that this analysis of simple effects is decoding. Correlations between the patterns of use of the
unjustified, given the non-significance of either the main different drugs co-abused and the dependent variables
effect of group or the interaction. However, it still seems to showed that, for personality variables, cocaine peak
show that, with regard to the effects seen analysis of quantity of use, and alcohol binge use were significantly
proportions of correct responses, differences in sensitivity associated with Positive Urgency. For neuropsychological
to reinforcement seem to carry more weight than differences indices, peak quantity of cocaine use was significantly
in sensitivity to punishment. In other words, if we accept this correlated with slower processing speed, quantity and
argument, rave attenders were more prone to hold to duration of alcohol use were significantly correlated with
response after being rewarded, but showed choice strategies poorer analogical reasoning, and quantity of use of
similar to those of controls when penalized. We will hallucinogens was significantly correlated with poorer
reconsider this pattern and its possible implications in the working memory skills.
discussion section. These results are broadly consistent with previous
findings obtained in groups of recreational alcohol and
Correlation analyses drug users, and there is also some degree of overlap with
findings on treatment-enrolled alcohol and drug abusers.
Peak quantity of use Peak amount of cocaine use was For personality variables, lack of perseverance was the
significantly correlated with poorer performance on digit more prominent impulsivity pathway among rave attenders.
symbol coding, r=−0.67, p=0.001 and peak amount of Lack of perseverance (i.e., an inability to remain focused on
alcohol use was significantly correlated with poorer a task that may be boring or difficult) was theoretically
Psychopharmacology (2010) 210:377–392 387

Proportion of correct choices across Phases (1-4) and Blocks (1-8)


1.00

0.75
Proportion of correct choices

0.50

0.25

0.00 Control
1 2 3 4 5 6 7 8 1 2 3 4 5 6 7 8 1 2 3 4 5 6 7 8 1 2 3 4 5 6 7 8 Rave
Phase 1 Phase 2 Phase 3 Phase 4

Fig. 3 Proportion of correct choices for each block (1–8) and each phase (1–4) in the reversal learning task. Reward contingency reversals
occurred after each 40-trial phase. Blocks are composed of five trials

proposed to be linked with attention deficit/hyperactivity sensation seeking may be relevant to predict the frequency
disorder symptoms (Whiteside and Lynam 2001) and it is of early drug exposure (Cyders et al. 2009), but not so
also significantly elevated in polysubstance-dependent indi- sensitive to discriminate between regular or pathological
viduals with principal use of alcohol and psychostimulants drug users and drug-free controls.
(Verdejo-García et al. 2007a). Furthermore, rave attenders For cognitive measures, effect sizes results showed that
had significantly elevated scores on both negative and analogical reasoning (i.e., the ability to infer the association
positive urgency, the latter being significantly correlated between two words or concepts) was the most robustly
with peak estimates of cocaine use and with the maximum impaired process in rave attenders. Although analogical
number of drinks taken in the interval of 1 h (alcohol binge reasoning is highly correlated with educational level, we
use). These results are consistent with the prominent role of should note that our groups were well matched on years of
emotion-driven impulsivity (i.e., urgency traits) in alcohol education; therefore, it is unlikely that performance differ-
and drug use (Whiteside and Lynam 2003; Verdejo-García et ences can be explained in terms of premorbid educational
al. 2007a) and with recent data indicating that positive background. On the other hand, poor performance on
urgency significantly predicts the quantity of alcohol that analogical reasoning was significantly associated with
students consume at any given drinking episode and the heavier use of alcohol. The association between alcohol
negative outcomes experienced from drinking (Cyders et al. abuse and abstraction skills had been previously observed
2009). On the other hand, both groups did not differ on in social drinkers (Tracy and Bates 1994) and clinical
levels of lack of premeditation, an impulsivity dimension samples of alcoholics (Beatty et al. 2000; Ratti et al. 2002).
that was elevated in a sample of substance dependents Furthermore, analogical reasoning skills are also robustly
(Verdejo-García et al. 2007a) and that correlated with impaired in clinical samples of polysubstance abusers
disadvantageous decision-making skills in healthy volunteers (Fernández-Serrano et al. 2010a). Rave attenders also
(Zermatten et al. 2005). Groups did not differ on sensation performed moderately worse than controls on a well-
seeking either. Previous evidence indicates that higher validated measure of working memory (Letter Number
388 Psychopharmacology (2010) 210:377–392

Fig. 4 Probability of holding Probability of holding choice after punishment


the same choice after being 1.00
penalized in the previous trial
across blocks (25 trials) and
phases (40 trials), for the control
and rave attending participants

0.75

Holding choice probability


0.50

0.25

0.00 Control
1 2 1 2 1 2 1 2
Rave
Phase 1 Phase 2 Phase 3 Phase 4

Sequencing). Several previous studies have shown an deficits on working memory are dose-dependent (Fernández-
association between recreational use of MDMA (De Sola Serrano et al. 2010b; Verdejo-García et al. 2005); whereas
et al. 2008) and alcohol binge drinking (Crego et al. 2009) cocaine recreational use effects seem to spare working
and poorer working memory performance. Cannabis-related memory skills (Colzato et al. 2009). In our correlation

Fig. 5 Probability of holding Probability of holding choice after reward


the same choice after being 1.00
rewarded in the previous trial
across blocks (25 trials) and
phases (40 trials), for the control
and rave attending participants

0.75
Holding choice probability

0.50

0.25

0.00 Control
1 2 1 2 1 2 1 2
Rave
Phase 1 Phase 2 Phase 3 Phase 4
Psychopharmacology (2010) 210:377–392 389

analyses, working memory performance was significantly Stroop. These elevated error scores did not produce parallel
correlated with quantity of hallucinogens use (e.g., psyloci- declines on the main composite time performance indices;
bin, LSD, or ayahuasca, but not ketamine or MDMA which they are therefore mild indicators of inhibitory/switching
were coded separately in the drug-taking interview). Acute deficits, which can be overall compensated in terms of final
administration of these hallucinogenic drugs has been behavioral output. The performance pattern in the go/no-go
associated with increased activation of both frontomedial task is also accountable in terms of poorer inhibition and
and frontolateral sections of the prefrontal cortex (Riba et al. switching skills. Once the response to the go trial has been
2006; Vollenweider et al. 1997) and with declines of firmly learnt, to stop responding to that stimulus seems more
attentional tracking skills (Carter et al. 2005) in humans— difficult for rave attenders than for controls. In this task,
both congruent with detrimental effects on working memory. these inhibition difficulties seem to be quite long lasting, as
In spite of the associations with specific substances, both rave attenders take several blocks to recover their pre-shift
deficits on working memory and reasoning should be alarm rate level.
interpreted in the context of polysubstance use. Therefore, The results observed in the probabilistic reversal learning
they might be associated with detrimental effects of task are somewhat counterintuitive. In previous studies, drug-
polysubstance use on executive control, or with certain pre- abusing and drug-dependent individuals have been observed
morbid personality traits or neuropsychological dysfunctions to present reversal difficulties—perseverance at choosing the
that convey vulnerability for drug use (Verdejo-García et al. same option after the reinforcement contingencies have
2008). Additional methodological efforts are warranted to changed (Ersche et al. 2008). Rave attenders do not show
address this important question. Irrespective of their etiology, reversal problems, as they are as fast as controls to detect
the cognitive decline of these executive skills, which are contingency changes. However, they do show significant
involved in the ongoing updating and manipulation of differences with controls: a higher proportion of correct
relevant information for on-line tasks, can importantly choices seemingly based on a stronger tendency to maintain
compromise everyday cognitive activities even in the their choice after reward. Therefore, unlike controls, rave
absence of an obvious functional impairment. attenders failed to show probability matching. Some authors
Other medium-size additional deficits were observed in (Unturbe and Corominas 2007; although see Shanks et al.
performance measures of psychomotor response speed and 2002; Perales et al. 2005) have accounted probability
inhibition and monitoring errors (during Stroop and go/no-go matching in terms of intentional hypothesis testing and
performance). Peak cocaine use was significantly correlated sequence discovery. In contrast to non-human animals,
with slowed psychomotor speed, consistent with previous humans do not always consider forced-choice tasks as
evidence of dose-related detrimental effects of this drug on essentially probabilistic, but try to unveil the existence of
processing speed (Bolla et al. 2000). MDMA and cannabis sequences that could explain why a given choice is rewarded
use have also been associated with slower speed of or not in each particular occasion. These conscious attempts
processing (Medina et al. 2007; Wareing et al. 2007). These are strongly dependent on planning and executive functions,
deficits may have important implications for several other but make performance become sub-optimal. If this is the case
performance domains, since neuropsychological studies here, reward dependence—as observed in rave attenders—
indicate that processing speed is a key variable to energize can result from diminished planning or executive capacities.
and optimize the resources of frontal systems and executive The fact that, in our study, rave attenders also showed low
functions (Stuss et al. 2005). A related issue in this sample of performance levels in other executive function indexes (LNS,
rave attenders is that of mild alterations in time perception, similarities, Stroop) thus supports the idea that probability
specifically characterized by underestimation of the passage matching and planning/executive capacities may depend on
of time across a 10 min lapse. The opposite pattern common brain circuits (Wolford et al. 2000).
(overestimation of time intervals) had been previously It is worth commenting on the fact that rave attenders
observed in psychostimulant users measured with specific showed unimpaired performance patterns in a number of
time estimation tasks and interpreted in terms of increased neuropsychological indices previously shown to discriminate
impulsivity (Wittmann et al. 2007). However, our time between substance-abusing/dependent individuals and
estimation index was obtained in the context of a multitask- healthy comparison individuals, including reversal learning
ing self-regulation test, in which participants had to tick a (i.e., perseveration errors), self-regulation, and emotional
box anytime they thought 1 min had passed; therefore, perception. The discrepancy between neuropsychological
underestimation may be viewed as an index of difficulties to findings on chronic users vs. rave recreational users (who
set the pace of their performance in absence of external cues. maintain functional activities and abstain from drug use
Additionally, rave attenders showed an increased number of during most of the time) may have implications for a better
errors during the inhibition phase of the Stroop and increased understanding of the neuropsychological mechanisms that
number of self-corrections during the switching phase of the differentiate “functional” vs. “dysfunctional” drug users.
390 Psychopharmacology (2010) 210:377–392

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Acknowledgements The research described here has been supported Peña Y, Murphy ER, Shah Y, Probst K, Abakumova I, Aigbirhio FI,
by grants SEJ2006-08278/PSIC, Spanish Ministry of Science, and P07- Richards HK, Hong Y, Baron JC, Everitt BJ, Robbins TW (2007)
HUM-03089 from the Council of Innovation, Science and Enterprise, Nucleus accumbens D2/3 receptors predict trait impulsivity and
Junta de Andalucía (PI: Mguel Pérez-García) and PSI2009-13133 (PI: cocaine reinforcement. Science 315:1267–1270
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