Biological Psychology 94 (2013) 388 396

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Biological Psychology

journa l h om epa ge: www.elsev ier .com/

Negative reward expectations in Borderline Persopatient

Daniel V sa, Antoni Ra Servei de Psiq elonab Unitat de Psic s, UnivBellaterra, Barcc Neurodynami rcelond Department o t, Barce Cognition and de Llof Catalan Instit

a r t i c l

Article history:Received 12 MAccepted 8 August 2013Available online 19 August 2013

Keywords:Borderline Personality DisorderFeedback-Related NegativityRewardErrorTheta oscillato

) patt a d

investigated these processes in a sample of 18 BPD patients and 18 matched healthy controls, usingan event-related brain potentials methodology. Results revealed a reduction in the amplitude of theFeedback-Related Negativity of BPD patients, which is a neurophysiological index of the impact of nega-tive feedback in reward-related tasks. This reduction, in the effect of negative feedback in BPD patients,was accompanied by a different behavioral pattern of risk choice compared to healthy participants. Thesendings conrm a dysfunctional reward system in BDP patients, which might compromise their capacity

1. Introdu

Borderlious mentalinstability otionships anZanarini, Sca heterogenReich, & Fitzmanent andKlonsky, 20propose thacritical infocontingencactions) wh(Crowell, B

Corresponversity of BarcTel.: +34 9340

E-mail add(J. Marco-Palla

0301-0511/$ http://dx.doi.ory activity

to build positive expectations of future rewards and decision making. 2013 Elsevier B.V. All rights reserved.

ction

ne Personality Disorder (BPD) is a complex and seri- disorder with a characteristic pervasive pattern ofn affect regulation, impulse control, interpersonal rela-d self-image, and severe functional impairment (Lieb,

hmahl, Linehan, & Bohus, 2004). Although it seems to beeous and less stable diagnosis (Zanarini, Frankenburg,maurice, 2010), emotion dysregulation is the most per-

frequent criterion (Carpenter & Trull, 2013; Glenn &09). Some inuential accounts on the etiology of BPDt patients present an impairment in the processing ofrmation in the adaptation of behavior to environmentalies (e.g., rewards and punishments associated with theirich would compromise their emotional self-regulationeauchaine, & Linehan, 2009). Nevertheless, studies on

ding author at: Department Basic Psychology, Campus Bellvitge, Uni-elona, FeixaLlarga s/n, 08907 LHospitalet, Barcelona, Spain.34768; fax: +34 934024268.resses: josepmarco@gmail.com, josepmarco@hotmail.comrs).

the processing of rewarding outcomes as well the expectations ofreceiving a reward have been scarce in these patients.

Emotional reactivity and cognitive control have been proposedas two features of the BPD emotional difculties and, additionally,have been related to their attachment style which plays a cen-tral role in the development of the disorder (Agrawal, Gunderson,Holmes, & Lyons-Ruth, 2004; Minzenberg, Poole, & Vinogradov,2008; Steele & Siever, 2010). Rodent models and human neu-roimaging have related the attachment system with the rewardnetwork due to a shared neural circuit which links a neuropeptide-sensitive mechanism (oxitocin/vasopressin), within the anteriorhypothalamus, to the ventral tegmental area (VTA) and nucleusaccumbens (see for a review Insel & Young, 2001). In addition,from a gene-environment perspective, the dopamine DRD4 poly-morphism in children has been related to disorganized attachmentpatterns with parents (Lakatos et al., 2000). The reward system isrelated to a variety of motivated behaviors and cognitive processes,such as reinforcement learning, novelty processing, action moni-toring, decision making or addiction (Camara, Rodriguez-Fornells,Ye, & Mnte, 2009). Therefore, the interaction between these twosystems (reward and attachment) may be especially important formediating the rewarding properties of social interaction as salient-motivating cue, and for affect and stress regulation (Strathearn &

see front matter 2013 Elsevier B.V. All rights reserved.rg/10.1016/j.biopsycho.2013.08.002s: Neurophysiological evidence

egaa,b,e, ngel Sotoa, Juli L. Amengualc, Joan Ribaodrguez-Fornellsd,e,f, Josep Marco-Pallarsd,e,

uiatria i Salut Mental, Hospital dIgualada (Consorci Sanitari de lAnoia), Igualada, Barcologia Mdica, Departament de Psiquiatria i Medicina Legal & Institut de Neurocincieelona, Spainc Laboratory, Departament of Psychiatry and Clinical Psychobiology, Universitat de Baf Basic Psychology, Campus Bellvitge, University of Barcelona, LHospitalet de Llobrega

Brain Plasticity Group [Bellvitge Biomedical Research Institute - IDIBELL], LHospitaletution for Research and Advanced Studies, ICREA, Barcelona, Spain

e i n f o

arch 2013

a b s t r a c t

Borderline Personality Disorder (BPDimpulse control which could reeclocate /b iopsycho

nality Disorder

Rafael Torrubiab,

08700, Spainersitat Autnoma de Barcelona, 08193

a, 08035 Barcelona, Spainelona 08097, Spainbregat, Barcelona 08097, Spain

ients present profound disturbances in affect regulation andysfunction in reward-related processes. The current study

D. Vega et al. / Biological Psychology 94 (2013) 388 396 389

Mayes, 2010; Vrticka, Andersson, Grandjean, Sander, & Vuilleumier,2008).

The idea of a dysfunctional reward system in the BPD hasreceived growing theoretical interest in recent years (Bandelow,Schmahl, Fresearch hareward systthermore, eimpulsive cBjork, HuckChanen, 20reinforceme(Kirkpatrickbrain potenRenneberg,Feedback-Rative to conInterestinglpresentatiorect action 1997). The dforcement lthat the FRVTA dopamments (Schuto the ventthe medial a possible tquences of aoutcomes sthan unexpdescribed aoutcomes, also might trating ada(Cohen, ElgNo previouBPD.

In the prrelates (ERPprocessing studies (Schoutcomes wparticipantsor lose realby objectivefor exampleSchuermanand punishto study thciated withpredictionsble. In addireliable FRN(Gehring & Pallars et apresent gamnor objectivin BPD pattheir risky crisk after ceMallorqu, Caddition, ginegative exet al., 2009less impact

negative prediction error), yielding a reduction in the amplitude ofthe FRN component and theta oscillatory activity.

All these hypotheses were tested in a group of BPD women(double diagnostic interview by independent evaluators). Com-

ntariterizual dy parcalesch-ack pgulat

thatomp

(seeJohanassess (Veng ef

ods

ticipan

ty-sixe BPD

of IguTR (Arecrui

exclumajorntelligicipanrovedBPD parainedw for s. Boted Cli

Monrhe BPilton De BPD

serot usedther temog

terials

elf-repSensit

et al.lity m

scale functioifferenssess a scalangedroduc

euro rodu

euro le lossct of pce and

edicat scaleiatricnt, ant = 0, ldicatiics wes a realkai, & Wedekind, 2010; Friedel, 2004). Previouss reported impaired opioid activity, linked with theem (Prossin, Love, Koeppe, Zubieta, & Silk, 2010). Fur-mpirical data show that the BPD individuals make

hoices that result in fast appetitive rewards (Dougherty,abee, Moeller, & Swann, 1999; Lawrence, Allen, &10). Several studies have suggested a dysfunctionalnt processing during both reward and loss feedbacks

et al., 2007; Vllm et al., 2007). A recent event-relatedtial (ERP) study (Schuermann, Kathmann, Stiglmayr,

& Endrass, 2011) showed reduced amplitude on theelated Negativity (FRN) component in BPD patients (rel-trols) who were performing an Iowa Gambling Task.y, this ERP component is elicited 250300 ms after then of a feedback, indicating a monetary loss or incor-(Gehring & Willoughby, 2002; Miltner, Braun, & Coles,ynamics of the FRN have been explained using the rein-earning model (Holroyd & Coles, 2002) which proposesN is indirectly reecting the inuence of decrease ininergic signals in the midbrain after unexpected punish-ltz, 1998). This reinforcing signal might be transmitted

ral striatum, as well as other cortical regions such asprefrontal cortex. The FRN has been associated witheaching signal concerning worse than expected conse-ctions. Considering this proposal, unexpected negativehould elicit larger amplitude in the FRN componentected positive outcome. In addition, several studies haven enhancement of theta power activity after negativewhich might not only be related to ACC activity, butreect a broader neural network involved in orches-ptive adjustments after errors or negative feedbackser, & Ranganath, 2007; Marco-Pallares et al., 2008).s research has studied theta power modulations in the

esent study we evaluated the neurophysiological cor-s and theta oscillatory activity) associated with rewardin a sample of BPD patients. In contrast to previousuermann et al., 2011), we used a paradigm where theere not predictable, a monetary gambling task in which

had to choose between two numbers in order to win money. In this paradigm the behavior is not guided

probabilities of receiving a reward or punishment (as, in reversal learning tasks or the Iowa Gambling Task;n et al., 2011), but by internal expectations as rewardsments are delivered at random. Therefore, we aimede differences between BPD and healthy subjects asso-

an uncertain environment or contexts in which clear about the outcome of their actions were not possi-tion, this paradigm has been shown to provide a very

component and theta oscillatory activity in loss trialsWilloughby, 2002; Marco-Pallares et al., 2008; Marco-l., 2009). We hypothesized that the characteristics of thebling task, in which there is neither correct responsee rule, could induce a differential behavioral pattern

ients compared to healthy participants, especially inhoice patterns (that is, the tendency to increase theirrtain outcomes; Gehring & Willoughby, 2002; Pedro,ucurell, Marco-Pallars, & Rodrguez-Fornells, 2013). Inven the tendency of BPD to form unrealistic goals andpectations about the outcomes of their actions (Crowell), we hypothesized that monetary losses would have

in BPD patients than in healthy participants (reduced

plemecharacindividhealthment sapproafeedbation reshownERPs csystem2012; col to samplefoundi

2. Meth

2.1. Par

Thirstudy. ThHospitalDSM-IV-women der. Thecurrent and an IThe partwas app

The uators tInterviediagnosiStructurAlvarez,1997). Tthe Hamtion in thselectivethe mosand ano(N = 5). D

2.2. Ma

2.2.1. SThe

TorrubiapersonaishmentSystem vidual d

To amoney, which rimpact pand 0.50impact pand 0.50a possibthe impaon valen

2.2.2. MThis

in psychdepressaas abseneach mepsychot2004). Aly to the clinical instruments, and in order to bettere the reward system in the sample and to control theifferences in reward processing between patients andticipants, we used the Sensitivity to Reward and Punish-

(Torrubia, vila, Molt, & Caseras, 2001), to measurevoidance conicts at cognitive level which could biasrocessing (for a review on decision making and emo-ion see Mitchell, 2011). Finally, as previous studies have

certain psychopharmacological drugs could affect theonents as well as the responsiveness of the reward brain

for example: Abler, Grn, Hartmann, Metzger, & Walter,nes, Wieringa, Nager, Dengler, & Mnte, 2001) a proto-s total medication load, previously used in psychiatricderman et al., 2012), was used to control possible con-fects.

ts

women ranging in age from 18 to 45 years old were included in the participants were 18 outpatients of the Psychiatry Department of thealada (Barcelona, Spain) who met the diagnostic criteria according toPA, 2000). The Healthy Control (HC) group consisted of 18 healthyted via local advertisement without history of any psychiatric disor-sion criteria were the presence of brain injury, psychotic, bipolar, or

depressive disorder, drug or alcohol abuse in the previous month,ence Quotient (IQ) below 80. Groups were matched by age and IQ.ts were paid, and the study followed the Declaration of Helsinki and

by the local Scientic and Ethics Committee.tients underwent a double diagnostic interview by independent eval-

in the administration of the Spanish validation of the DiagnosticBorderlines-Revised (Barrachina et al., 2004), in order to ensure theh BPD and HC groups were assessed with a Spanish adaptation of thenical Interview for DSM-IV Axis II Personality Disorders (Prez-Prieto,os, Sarria, & Prez-Marn, 2008) and for DSM-IV Axis I (First & Gibbon,D depressive symptoms ranged from 4 to 17 (M = 11.55, SD = 4.27) inepression Rating Scale (HDRS, Hamilton, 1960). Medication prescrip-

group was stable along the study (M = 2.33, SD = 1.84, range: 05). Thetonin reuptake inhibitors (N = 10) and benzodiazepines (N = 9) were, followed by mood stabilizers (N = 7), atypical antipsychotics (N = 4)ype of drugs such noradrenergic and serotoninergic antidepressantsraphic and clinical variables can be observed in Table 1.

ort measuresivity to Punishment and Sensitivity to Reward Questionnaire (SPSRQ,, 2001) is a questionnaire developed and validated directly on Graysodel (Corr, 2004) and consists of two scales: the Sensitivity to Pun-(SP), which measures individual differences on Behavioral Inhibitionning, and the Sensitivity to Reward scale (SR), which measures indi-ces on Behavioral Activation System functioning.the assigned value given by participants to a determined amount ofe was created ad hoc. It consisted of four visual analog scales (VAS)

from 0 to 100 points. The rst two aimed to assess the subjectiveed by the possibility of receiving a certain amount of money (100 eurocent), and the others were used for the assessment of the subjectiveced by the possibility of losing a given amount of money (100 eurocent). High scores indicated that participants evaluated the impact of/gain as very important for themselves. This measure aimed to captureossible economic feedbacks considering four possibilities (depending

magnitude) in a daily virtual scenario.

ion load is a protocol to assess total medication load, previously used

samples (Vederman et al., 2012). For the implementation, anti-xiolytic, mood stabilizer, and anti-psychotic medications were codedow = 1, or high = 2, based on previously employed methods to converton to a standardized dose (Almeida et al., 2009; Sackeim, 2001). Anti-re converted into chlorpromazine dose equivalents (Davis & Chen,sult, we obtained a composite measure of total medication load by

390 D. Vega et al. / Biological Psychology 94 (2013) 388 396

Table 1Demographic characteristics, clinical and psychometric variables.

BPD (n = 18) HC (n = 18) t-test p-Value

Mean SD Mean SD

Age (years) IQ DIB-R (First)DIB-R (SeconSPSRQ

SR SP

VASReceive-MReceive-MLose-Max Lose-Min

18)

Right-handeSCID-I (curre

Anxious dEating disSubstanceDysthymia

SCID-I (lifetiMDD Anxious dEating disSubstance

SCID-IIDependenAvoidant Paranoid HistrionicAntisocial

IQ, intelligenc sts (Wto PunishmenBorderlines-Re

summing all icategories for

2.2.3. GamblinA moneta

Willoughby (2presented on amouse buttonthey wanted tcated the selenumber 5. Aftegreen. If the nuamount in Euramount in Eura warning signipants began tencouraged toa brief practice

The experivalue of moneinuences of amulated amouthe participan

2.3. Procedure

The clinicaand socio-dem

EEG (Synapass lter, 50located at 29 Cp1/2, Cp5/6, gambling tasktwo mastoid p30.94 5.96 27.44 96.85 8.49 99.46 8.06 0.93

d) 7.89 1.18

11.38 4.11 6.94 17.66 4.76 9.22

ax 58.94 26.71 60.61in 23.22 23.35 28.11

59.72 24.27 44.11 12.88 15.82 12.16

BPD (n = 18) HC (n =

n (%) n

d 15 83.3 17 nt)isorder 10 55.5order 5 27.7

misuse 7 38.8 4 22.2me)

14 77.8isorder 4 22.2order 7 38.8

misuse 6 33.4

t 4 22.23 16.61 5.5

1 5.5 5 27.7

e quotient, estimated through matrix reasoning, vocabulary and digits span subte

t and Sensitivity to Reward Questionnaire; SP, Sensitivity to Punishment; SR, Sensitivityvised; MDD, major depressive disorder.

ndividual medication codes for each individual medication withineach BPD patient.

g taskry gambling task similar to the one described by Gehring and002) was used (see Fig. 1A). In this task two numbers (25 and 5) were

computer screen. Participants had to make an obligatory left or right press response with their right index-nger, indicating the numbero bet. For instance in case of a [25][5] display, a left button press indi-ction of the number 25, and a right button press the selection of ther the selection, one of the numbers turned red while the other turnedmber selected changed to red, the participant lost the correspondingo cents, whereas if subject selected the green number he won thiso cents. After 2 s, the following trial began with the presentation ofal (*; 500 ms duration), followed by a new set of numbers. Partic-he task with an initial 1000 points (1 point = 1 Euro cent) and were

gain as much as possible and were familiarized with the task during block.ment comprised 17 blocks with 40 trials each, with the mean expectedtary outcome of zero on each block, to avoid potential confounding

differential probability of gains or losses. Every 10 trials, the accu-nt of money was presented for 7 s, and at the end of the experiment,ts were paid the nal amount.

l interviews (DIB-R only BPD group) and self-reported, intelligenceographical were gathered by a trained clinicians.mps, Neuroscan) was recorded at 250 Hz sampling rate (0.01 Hz high

Hz notch lter) using tin electrodes mounted in an elastic cap andstandard positions (Fp1/2, Fz, F7/8, F3/4, Fc1/2 Fc5/6, Cz, C3/4, T7/8,Pz, P3/4, P7/P8, Po1/2, O1/2) while participants were performing the. Biosignals were referenced off-line to the mean of the activity at therocesses. Vertical eye movements were monitored with an electrode

at the infraorbduring all the

2.4. Statistica

Firstly, deconcerning bawere tested utwo-tailed indwere used to m

Differencewere analyzedwithin-subjecback magnitud(group, BPD vone within-su(group, BPD vs

EEG was averaged fromexceeding 1the timefreqepochs were gexceeding 10data was convvarying energied frequenciecomputed foraverage. For thtude (large, smgroup (BPD, Hamplitude at Pallares et al., the maximumafter feedbackwhen appropr6.9 1.62 0.118.05 0.94 0.35

0.54 0.59

3.4 3.52 0.0015.01 5.18

D. Vega et al. / Biological Psychology 94 (2013) 388 396 391

Fig. 1. (A) Gam(n1, x axis) in25 instead of 5behavioral riskprevious trial (lack of sequento the control

3. Results

3.1. Psycho

The resuNo signicano betweenmined amoand the SenBPD group

3.2. Behavi

Participatrol (56.4 were no sichoices (t(3of risky choWilloughbywas observwithin factofactor (grou(F(1,34) = 4.groups (mashown in Fiincreased t

losing the largest amount of money (25; magnitude effect for con-trol participants, F(1,17) = 6.5, p = 0.02). In contrast, BPD patientsdid not show this adjustment pattern, and bet independently from

tcome of the previous trial (magnitude effect, F(1,17) = 0.08, see add

e mup . Nen vaant ent

outc diffee reGehrwa, &ition

rev) = 3.ant b

6962 ms,.

P da

2A ur ds 5)the oup = 0.8,

In valenca grop = 0.5)betweesignicadjustmby theclearlyfrom th2010; Takasa

AddANOVA(F(1,34signic25, M =M = 65p = 0.8)

3.3. ER

Fig.the fo25, losbling paradigm used in the experiment. (B) Effect of previous trial the risk pattern observed in the following trial (percent of choice of), in the BPD and control groups. The lines represent the percent ofy choices (total bets to 25) in function of the feedback received in thefour possible outcomes: gain 25, gain 5, loss 5 and loss 25). Notice thetial adjustment of risk patterns in the BPD patients when comparedgroup.

metric scales

lts of the psychometric scales are shown in Table 1.nt differences were found on the VAS scales, indicating-group differences in the assigned value to a deter-unt of money. Furthermore, the Sensitivity to Rewardsitivity to Punishment were signicantly higher in thethan in the control group.

oral results

nts tended to bet 25 more than 5, both in the con- 10.0%) and in the BPD (56.0 9.4%) group. Theregnicant differences among groups in percent of 254) = 0.1, p = 0.5). However, when analyzing the patternices considering previous outcome (based on Gehring &, 2002), a differential behavior pattern among groupsed (Fig. 1B). Repeated-measures ANOVA with twors (valence and magnitude) and one between-subjectsp) revealed a signicant main effect for magnitude4, p = 0.04), which was signicantly different in the twognitude group, F(1,34) = 5.6, p = 0.02). Therefore, asg. 1B, this interaction indicated that control participantsheir risk (betting more on 25 than 5) after winning or

backs (monto monetaWilloughbyures ANOV(gain/loss),(Fz, Cz, Pz)as betweenvalence (F(ativity obsestandard fronicant valAnalysis alsp = 0.01), insmall feedb

Fig. 2B smonetary gpresented ainteractionsignicant p = 0.3), norloss minusprevious stthe best mison betwe(t(17) = 6.92Finally, in tion, we anin the repeasignicant

3.4. Timef

Fig. 3 sand 40 Hz the controelectrode. MFig. 1B).ition we also found a marginal signicantagnitude effect (F(1,34) = 3.5, p = 0.07) but withouteffect (valence magnitude group F(1,34) = 0.564,ither valence (F(1,34) = 1.3, p = 0.3) nor the interactionlence and group (F(1,34) = 1.5, p = 0.2) yielded furthereffects. Thus, regarding trial-by-trial risk-sequentials, the choices of the BPD group were uninuencedome received in the previous trial, a pattern that isrent from the one observed in the control group andsults obtained in previous investigations (Camara et al.,ing & Willoughby, 2002; Masaki, Takeuchi, Gehring,

Yamazaki, 2006; Pedro et al., 2013).ally, a reaction time analysis was conducted. Theealed a marginal main effect of the bet magnitude9, p = 0.06) indicating a fast betting to 25 than 5. Noet magnitude group interaction was found (BPD: bet

ms, SD = 236; bet 5, M = 725 ms, SD = 280; HC: bet 25, SD = 324; bet 5, M = 687 ms, SD = 338; F(1,34) = 0.04,

ta

shows the Event Related Potentials associated withifferent feedback conditions (gain 25, gain 5, loss. In the 260300 ms time range the negative feed-etary losses) presented a negative deection comparedry gains compatible with the FRN ERP (Gehring &, 2002; Marco-Pallares et al., 2008). A repeated meas-A carried out at this time range with feedback valence

feedback magnitude (25/5) and electrode location as within-subject factors and Group (BPD/Control)-subject factor revealed a main signicant effect of1,34) = 40.1, p < 0.001), indicating the increase of neg-rved after negative feedbacks. This effect presented antocentral topography (see Fig. 2B) as revealed by a sig-ence electrode interaction (F(2,68) = 16.0, p < 0.001).o revealed a signicant magnitude effect (F(1,34) = 7.3,dicating an increase in activity for large as compared toacks (25 > 5).hows the different waveforms (monetary loss minusains) for the Fz and Pz electrodes. The control group

larger FRN than the BPD (signicant valence group, F(1,34) = 4.5, p = 0.04). Post hoc analyses revealed nodifferences between groups in the gain (t(34) = 1.0,

in loss conditions (t(34) = 0.07, p = 0.9), but in the gain condition (t(34) = 2.13, p = 0.04). Interestingly,udies have suggested that the difference waveform isarker of the FRN processing (Holroyd, 2004). Compar-en gain and loss trials was signicant in both control, p < 0.001) and BPD participants (t(17) = 2.64, p = 0.02).

order to discard any effect associated to the medica-alyzed the medication load, including it as a covariateted-measures ANOVA in the BPD group. There was no

valence load interaction (F(1,16) = 1.2, p = 0.3).

requency

hows the power changes at frequencies between 1associated with positive and negative feedbacks forl (Fig. 3A) and the BPD (Fig. 3B) group at the Fz

onetary losses were characterized by greater theta

392 D. Vega et al. / Biological Psychology 94 (2013) 388 396

Fig. 2. (A) Eve ain (sand minimum trodeand 300 ms fo fect isat the Cz elect ity hasignicant diff iffereand BPD (right der is

band activiitive feedbfrequency bsentation. valence eing an incat frontocevalence effeof group invalence ea signicanp < 0.01) buelectrode (Fa signicanmagnitude effects were

Then wecentral elecgains (valensponding Aand BPD grrange (valedifference higher thanno signicap = 0.2), norloss minusther controp = 0.1) shoditions. In of valence (valence lorigin of th

en d andany

= 0.9nt-Related Potentials associated to the four studied types of feedback: maximum g loss (dashed red) for the control (left) and BPD group (right) at three midline elecr negative feedbacks compared to positive ones in the control group (FRN). This efrode for the control (blue) and BPD (orange) group. For illustration purposes, activerences between groups (260300 ms). Bottom, scalp topographical maps for the d) groups. (For interpretation of the references to color in this gure legend, the rea

ty (37 Hz) for negative feedback compared to pos-ack. We analyzed two different time ranges at thisand: 200300 ms and 300450 ms after feedback pre-In the former time range, we found a signicant

betwechoticswith F(1,16)lectrode interaction (F(2,68) = 19.7, p < 0.001), show-rease in theta band for loses compared to gainsntral electrodes (Fig. 3A and B), but not a mainct (F(1,34) = 0.1, p = 0.7). There was no signicant effect

the valence (valence group, F(1,34) = 2.4, p = 0.13;lectrode group, F(2,68) = 2.1, p = 0.14). We also foundt magnitude effect in this time range (F(2,68) = 8.2,t not a signicant interaction between magnitude and(2,68) = 1.9, p = 0.2). None of these interactions yieldedt group effect (magnitude group, F(1,34) = 1.1, p = 0.3; electrode group, F(2,68) = 0.3, p = 0.8). All the other

not signicant (F < 1.6, p > 0.2). analyzed the 300450 ms time range. Again, fronto-trodes showed a greater theta power for losses thance electrode, F(2,33) = 18.8, p < 0.001), and the corre-NOVA revealed signicant differences between controloups in the 37 Hz and 300450 ms timefrequencynce group, F(1,34) = 4.8, p = 0.04), indicating that thebetween gains and losses in the control group was

in the BPD group. Post hoc analyses again revealednt differences between groups in the gain (t(34) = 1.3,

in loss conditions (t(34) = 0.07, p = 0.9), but in the gain condition (t(34) = 2.2, p = 0.04). However, nei-ls (t(17) = 1.36, p = 0.2), nor BPD patients (t(17) = 1.72,wed signicant differences between gain and loss con-addition, we found a marginal signicant interactionand medication load for valence in the BPD groupoad F(1,16) = 3.1, p = 0.099). In order to determine theis marginal effect, we divided the medication load

ics, F(1,16)

4. Discussi

Reward-was evaluapatterns), tand the timetary gainsamplitude ity for the encountereprocessing tem of BPDvalence, bulead the pamaking pre

These rendings (Ksuggested aing both poInterestinglan Iowa Garisky choiceperformancshowed a rpatients alsitive and npatients prolid black), minimum gain (dashed black), maximum loss (solid red) locations (Fz, Cz, Pz). Notice the increase of negativity between 260

reduced in the BPD group. (B) Loss minus gain difference waveforms been ltered with a 12 Hz lowpass lter. Region in green indicatesnce waveform (loss minus gain) in the green region for control (left)

referred to the web version of this article.)

ifferent groups: antidepressants, anxiolytics, antipsy- anticonvulsants. We did not nd signicant differencesof the specic medication types (antidepressants,, p = 0.4; antipsychotics, F(1,16) = 1.3, p = 0.3; anxiolyt-

= 1.1, p = 0.3; anticonvulsants F(1,16) = 2.6, p = 0.13).

on

related feedback processing in a group of BPD patientsted, analyzing behavioral adjustments (change in riskyhe feedback related negativity ERP component (FRN)e frequency decomposition of EEG after receiving mon-

and losses (theta band power). A decrease in theof the FRN component and of the power of theta activ-BPD group in comparison to the control group wasd, suggesting an altered pattern of negative feedbackwhich could indicate an impairment in the reward sys-

patients. This decit might not only be related to thet also to unexpectedness of the outcome which mighttients to an incapacity for adjusting their behaviors anddictions according to the history of previous outcomes.sults are only partially in line with previous researchirkpatrick et al., 2007; Vllm et al., 2007) which haven altered reward processing in the BPD patients, follow-sitive and negative feedback (compared with controls).y, a recent study by Schuermann et al. (2011) usingmbling Task has shown that BPD patients made mores than healthy participants and did not improve theire nor learn during the task. Therefore BPD patientseduced ability to learn from feedback. In addition, BPDo showed reduced FRN amplitude following both pos-egative feedbacks. Our results also suggest that BPDesent an impairment in behavioral pattern indicated

D. Vega et al. / Biological Psychology 94 (2013) 388 396 393

Fig. 3. Timefand 40 Hz of: g

by the lackbut withouIn addition(Schuermanhowever, co

The FRNcould indictive feedbalosses in BPishments (Hare of grearonment cothe formatioptimize thnent indexethan the in& Willoughproposed thappears aftmight be ra predictionthe expecte2009; ChasFuentemillative feedbathe FRN anrequency plots at the Fz electrode for (A) the control and (B) the BPD group. From top to ain, loss and gain minus loss. The white rectangle indicates the timefrequency studied

of adjustment after large magnitude gains and losses,t an increase in the percentage of high magnitude bets., our study showed a reduction in the FRN amplituden et al., 2011) and theta oscillatory activity (the latter,rrelating with medication load).

and theta activity reduction found in the BPD groupate a reduction in the prediction error after the nega-ck, which could be yielded by a reduced impact of theD patients and/or a greater expectancy of receiving pun-ajcak, Moser, Holroyd, & Simons, 2007). These results

t importance because correct processing of the envi-ntingencies (rewards and punishments) is required foron of suitable predictions and expectations, which wille behavioral adaptation. In this context, the FRN compo-s the motivational impact of the outcome event moreformation content of the negative feedback (Gehringby, 2002). More specically, Holroyd and Coles (2002)at both the FRN as well as the theta activity increaseer worse than expected results of our actions, whichelated to a brain signature conveying information of

error; that is, the discrepancy between the real andd outcome of our actions (Cavanagh, Cohen, & Allen,e, Swainson, Durham, Benham, & Cools, 2011; Talmi,, Litvak, Duzel, & Dolan, 2012). Therefore, when nega-ck is unexpected or the loss is greater than predicted,d theta activity would be higher, as is the difference

between renote that reposed (Holraccount, neFRN) and, igoing deecits amplitudtion of FRNfeedback conale, Hajihothe ACC aftetheta oscillgain trials. FRN found iN200 amplwith both g2008, for a gest that BPassociated open debatnents and mfunctional i

The BPDthe high SRsue fast appSP could sbottom can be seen the power changes at the frequencies between 1area for the theta band (37 Hz, 300450 ms).

al and expected outcome. However, it is important tocently a new interpretation of the FRN has been pro-oyd, Pakzad-Vaezi, & Krigolson, 2008). According to thisgative feedbacks would produce a standard N200 (then contrast, positive feedbacks would elicit a positive-tion which would superpose to the N200-FRN, reducinge. Therefore, the important effect would be the reduc-

with positive outcomes, constituting the so-calledrrect-related positivity (fCRP). Following a similar ratio-sseini and Holroyd (2013) proposed that the activity inr unexpected positive outcomes would reduce both theatory activity and the N200 Event-Related Potential inAccording to this interpretation, the reduction in then BPD patients could be explained by a reduction in theitude due to decreased novelty processing associatedain and loss events (see, e.g., Folstein & Van Pettern,N200 review). In other words, this account would sug-D patients would be less sensitive to the novel impactto the feedback processing. However, there is still ane on the interpretation of the FRN-fCRP ERP compo-ore studies are needed in order to establish a correct

nterpretation for these responses. group scored high both in SR and SP. Thus, while

scores could indicate a pervasive tendency to pur-etitive rewards, at the same time, the high scores on

uggest an underestimation of potential rewards and

394 D. Vega et al. / Biological Psychology 94 (2013) 388 396

overestimation of possible risks, punishment or non-rewardingoutcomes (Corr, 2002). This combination, in addition to alterationsin the feedback processing (FRN), could lead them to constant con-icts at the cognitive level and emotional instability which wasindirectly s2008). To coscales did similar impticular amoSPSRQ suggrelated to aincreased Sexpectancy

The presdopaminergroimaging In addition(Bandelow such as emotoms and pasuggest a dethermore, tshowing thwhich appHohnsbein,Meyer, & Ding an impsequential Ruchsow etreinforcemas a teachindiction erroreinforce coof this signafter errorsthere is nowere deliveferences incontrol andpattern in Pedro et atwo studiesdecisions cchoices afteor losses). IGehring andincreased liimportant tdifferent, thGehring anIn contrast,similar percThis behaviinformationvious trialsafter large manhedonia tpathologicacially after shown thattain scenariproposed thto reduced uation of fushow a gloof choosing

of risky choice after different outcomes. Therefore, the lack of asequential adjustment strategy in these patients could be explainedby a reduced impact of previous trial feedback and a subsequentimpairment in the activation of automatic adjustment mechanisms

mo009;manon onds blishe an

nt. Inimila

wet stra

ilar altein pratienMorethe drly et or alterity henonvirowhicenceals (t cou

sett of Bisten. In cions 2011ilityerefor losize

he paal toimpast th

maiD paaffecortanent

ts couce. Dhat parmauez-et al

loadectedect obe erequher cpareijn edy onceshown by the SPSRQ (Amodio, Master, Yee, & Taylor,mplement the SCSRQ, we created ad hoc a VAS. These

not show between groups differences, supporting aortance given to the possibility of receiving/losing a par-unt of money. This result combined with the scores ofests that the reduction of FRN and theta activity is not

reduction of the impact of losses (as BPD patients showP values) but more likely linked to an increase in the

to lose.ent results might reect impairment in the mesolimbicic system (Marco-Pallars et al., 2009), in line with neu-ndings (see for a review Mauchnik & Schmahl, 2010).

, some theoretical approaches to borderline etiologyet al., 2010; Friedel, 2004) as well as some clinical traitstion dysregulation or impulsivity, psychotic-like symp-rtial efcacy of antipsychotic drugs among others, alsoregulation of the reward system in these patients. Fur-he current results are in line with previous researchat the Error Related Negativity, a parallel componentears after the commission of an error (Falkenstein,

Hoormann, & Blanke, 1991; Gehring, Goss, Coles,onchin, 1993) is also reduced in BPD patients, suggest-aired capacity to learn from errors and to implementcognitive control adjustments (de Bruijn et al., 2006;

al., 2006). It is important to note that, according to theent learning theory (Holroyd & Coles, 2002), the FRN actsg signal after worse than expected events (negative pre-r, but see Holroyd et al., 2008) and it might be used torrect responses and inhibit erroneous ones. Impairmental might result in non-optimal adaptation of behavior

or negative feedbacks. While in the present experiment correct strategy per se (as rewards and punishmentsred at random without participants knowledge), dif-

the behavioral adjustments (risk patterns) between BPD group supports this idea (see Fig. 1B). The riskthe control group is very similar to the one found inl. (2013) (but see Gehring & Willoughby, 2002). In the, control participants showed an increase in their riskyharacterized by a greater selection of high magnituder large magnitude outcomes (whether monetary gainsnterestingly, this patter differs from the one shown in

Willoughby (2002), in which the risky-choice patternnearly, from high gains to high losses. However, it iso note that both experimental paradigms are slightlye current paradigm being a simplied version of the

d Willoughby (2002) (see Marco-Pallares et al., 2008). BPD patients showed a at risky-choice pattern, withentage of high magnitude selection after any outcome.or seems to suggest that patients did not use previous

and bet independently from the outcome of the pre-. This result is also similar to the reduced risky choices

agnitude trials in participants with high values in therait (Pedro et al., 2013). In addition, patients with highl anxiety also show a reduced tendency to risk, espe-small gains (Giorgetta et al., 2012). Other studies have

schizophrenic patients reduce the exploration of uncer-os with higher risk (Strauss et al., 2011). It has also beenat the decrease of risk-taking behavior might be relatedexpectations of reward in the future (pessimistic eval-ture, Giorgetta et al., 2012). The present results do notbal reduction in risk-taking behavior (the percentage

25 is the same in the two groups), but in the pattern

elicitedet al., 2Schuerselectiit depeto estaoutcompendewith sequallycorrecwas sim

Thefound BPD psions. about that eacontexcould reactivThis pand ebiases experiproposcontexidatingtheoryinconstulatedconditet al., probabnot. Thning omaximafter tor signmight to adju

Thethe BPcould is impassessmpatienformangiven tchophRodrig(Abler icationnot afftial effmight timefalso otto com(de Brunot studifferest probably in the medial prefrontal cortex (Cavanagh Ridderinkhof, Ullsperger, Crone, & Nieuwenhuis, 2004;n et al., 2011). However in the present paradigm thef the magnitude is not an independent measure, buton the choice of the participant. This makes difcult

a causal link between the magnitude of the previousd the current selection, as they are not completely inde-

addition, it is important to note that both groups endedr amounts of money, that is, both performed the taskll. Therefore it cannot be stated which was the moretegy, although risky choice pattern in healthy controls

to previous studies (Pedro et al., 2013).ration of reward processing and adjusting behavioresent results might help understand the tendency ofts to make suboptimal, even disadvantageous, deci-over, the results are in accordance with some theoriesevelopment of BPD psychopathology, which proposenvironmental factors (i.e. invalidating developmentalneglect) (Linehan, 1993), as well as genetic factors,

the reward pathways in the brain and cause hyper-of the attachment system (Fonagy & Bateman, 2006).menon is a vicious circle between attachment stylenmental experiences, resulting in certain cognitiveh complicate the decision making based on previouss and feedback, in line with current cognitive therapyClark & Beck, 2010). Interestingly, our experimentalld be considered as an experimental model of an inval-ing similar to that proposed by Linehan in her biosocialPD (see for a review Crowell et al., 2009), in which ant use of punishment and reward by progenitors was pos-ontrast to other experimental approaches in which riskor specic rule probabilities were used (Schuermann), in the present study participants neither knew the

of each choice nor whether a correct strategy existed orre, the uncertainty created by the gambling task (win-

ing 5 or 25 at random while participants are trying to their gains) might generate an ambiguous situationrticipants choice, as they did not have any evidence

trust in their election or strategy, which in patientsir the capacity to use the history of previous outcomese behavior.n limitation of present study arises from the fact thattients were on medication during the study whicht the effects in brain electrical activity. However, itt to note that the prescription was stable along the

process, and that the symptoms of unmedicated BPDld hinder (even make impossible) the experiment per-espite this, we have included a standardized measurerevious ndings have suggested an effect of several psy-cological drugs on for example, action monitoring (Riba,Fornells, Munte, & Barbanoj, 2005) or reward processing., 2012). Thus, we found only a marginal effect of med-

in theta oscillatory activity, but importantly, FRN was by medication. This dissociation between the differen-f medication in theta (marginal) and FRN (no effect)xplained by the poorer temporal resolution of thetaency analysis, which might include not just FRN, butomponents such as P300. In addition it is not possible

this effect with previous study on BPD and FRN/ERNt al., 2006 Schuermann et al., 2011) because they didscillatory activity. Nevertheless, in the present study

in FRN between controls and BDP are not affected by

D. Vega et al. / Biological Psychology 94 (2013) 388 396 395

medication evidencing a dysfunctional reward processing in BPDpatients, concretely in the negative feedback processing whichmight lead to decits in learning and decision making due to animpaired capacity to elicit correct expectations and predictions.These results contribute to understanding the BPD psychopathol-ogy supporthe disordecost-benebetter approf therapeuwork), drug

Acknowled

This rese(2009-092409101 and supported b

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Negative reward expectations in Borderline Personality Disorder patients: Neurophysiological evidence1 Introduction2 Methods2.1 Participants2.2 Materials2.2.1 Self-report measures2.2.2 Medication load2.2.3 Gambling task

2.3 Procedure2.4 Statistical analysis

3 Results3.1 Psychometric scales3.2 Behavioral results3.3 ERP data3.4 Timefrequency

4 DiscussionAcknowledgmentsReferences