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Social Neuroscience

ISSN: 1747-0919 (Print) 1747-0927 (Online) Journal homepage: http://www.tandfonline.com/loi/psns20

Social context modulates cognitive markers in


Obsessive-Compulsive Disorder

Hernando Santamaría-García, Carles Soriano-Mas, Miguel Burgaleta, Alba


Ayneto, Pino Alonso, José M. Menchón, Narcis Cardoner & Nuria Sebastián-
Gallés

To cite this article: Hernando Santamaría-García, Carles Soriano-Mas, Miguel Burgaleta, Alba
Ayneto, Pino Alonso, José M. Menchón, Narcis Cardoner & Nuria Sebastián-Gallés (2017): Social
context modulates cognitive markers in Obsessive-Compulsive Disorder, Social Neuroscience,
DOI: 10.1080/17470919.2017.1358211

To link to this article: https://doi.org/10.1080/17470919.2017.1358211

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Accepted author version posted online: 26


Jul 2017.
Published online: 03 Aug 2017.

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SOCIAL NEUROSCIENCE, 2017
https://doi.org/10.1080/17470919.2017.1358211

ARTICLE

Social context modulates cognitive markers in Obsessive-Compulsive Disorder


Hernando Santamaría-Garcíaa, Carles Soriano-Masb,c,d, Miguel Burgaletaa, Alba Aynetoa, Pino Alonsob,c,e,
José M. Menchónb,c,e, Narcis Cardonerb,c,e and Nuria Sebastián-Gallésa
a
Center for Brain and Cognition, Department of Technology, Universitat Pompeu Fabra, Barcelona, Spain; bDepartment of Psychiatry,
Bellvitge University Hospital, Bellvitge Biomedical Research Institute-IDIBELL, Barcelona, Spain; cDepartment of Psychiatry, CIBERSAM
(Centro de Investigación Biomédica en Red de Salud Mental), Barcelona, Spain; dDepartment of Psychobiology and Methodology of Health
Sciences, Universitat Autònoma de Barcelona, Barcelona, Spain; eDepartment of Clinical Sciences, School of Medicine, University of
Barcelona, Barcelona, Spain

ABSTRACT ARTICLE HISTORY


Error monitoring, cognitive control and motor inhibition control are proposed as cognitive Received 21 June 2016
alterations disrupted in obsessive-compulsive disorder (OCD). OCD has also been associated Revised 3 May 2017
with an increased sensitivity to social evaluations. The effect of a social simulation over electro- Published online 2 August
2017
physiological indices of cognitive alterations in OCD was examined. A case-control cross-sectional
study measuring event-related potentials (ERP) for error monitoring (Error-Related Negativity), KEYWORDS
cognitive control (N2) and motor control (LRP) was conducted. We analyzed twenty OCD patients Social hierarchy;
and twenty control participants. ERP were recorded during a social game consisting of a visual obsessive-compulsive
discrimination task, which was performed in the presence of a simulated superior or an inferior disorder; evoked potentials;
player. Significant social effects (different ERP amplitudes in Superior vs. Inferior player condi- error monitoring process;
tions) were found for OCD patients, but not for controls, in all ERP components. Performing the cognitive control; motor
task against a simulated inferior player reduced abnormal ERP responses in OCD to levels control
observed in controls. The hierarchy-induced ERP effects were accompanied effects over reaction
times in OCD patients. Social context modulates signatures of abnormal cognitive functioning in
OCD, therefore experiencing a social superiority position impacts over cognitive processes in OCD
such as error monitoring mechanisms. These results open the door for the research of new
therapeutic choices.

Introduction Moreover, different studies have provided compelling


evidence of the impact of social context on cognitive
Fronto-striatal circuits are essential for behavioural regula-
functioning in healthy subjects (Santamaría-García,
tion mechanisms such as error monitoring and cognitive
Pannunzi, Ayneto, Deco, & Sebastián-Gallés, 2013; Zink
and motor control processes (Koban & Pourtois, 2014;
et al., 2008). In other words, establishing social compar-
Mansouri, Tanaka, & Buckley, 2009). Together, those cogni-
isons with fellow individuals, or experiencing a role within
tive processes have been postulated to be at the core of
a social context i.e., adopting a dominant social position
cognitive alterations in OCD (Chamberlain et al., 2008;
(social superiority) or a submissive position (social infer-
Dittrich & Johansen, 2013; Menzies et al., 2007; Purcell,
iority), can influence a wide array of cognitive processes,
Maruff, Kyrios, & Pantelis, 1998). As in other mental disor-
such as sensory-perceptual mechanisms (Chiao et al.,
ders with anxiety symptoms, OCD is also associated with an
2008; Santamaría-García et al., 2013), decision-making
increased sensitivity to social evaluations, leading to impair-
(Rilling & Sanfey, 2011), feedback assessment (Boksem,
ments in social functioning (Grisham, Henry, Williams, &
Kostermans, Milivojevic, & De Cremer, 2011), and execu-
Bailey, 2010; Harrison et al., 2012; Koban & Pourtois, 2014).
tive functions (Smith, Dijksterhuis, & Wigboldus, 2008;
Indeed, OCD patients display disruptions in their ability to
Smith, Jostmann, Galinsky, & van Dijk, 2008).
interact with other individuals and generally show inflex-
The above-presented findings become especially rele-
ibility (Dittrich & Johansen, 2013) as well as, anxiety symp-
vant in the context of the altered social sensitivity typically
toms related to social evaluations (Calkins, Berman, &
described in OCD patients (Grisham et al., 2010). The
Wilhelm, 2013; Grisham et al., 2010; Pace, Thwaites, &
current study addresses to what extent the social context
Freeston, 2011).

CONTACT Hernando Santamaría-García nanosanta@gmail.com; hernando.santamaria@javeriana.edu.co Carrer tanger 122, (80018) Barcelona, Spain;
Carles Soriano-Mas carles.soriano.mas@gmail.com Bellvitge Biomedical Research Institute-IDIBELL, Psychiatry Department, Bellvitge University
Hospital, Feixa Llarga s/n 08907, Hospitalet de Llobregat, Barcelona, Spain
The supplemental data for this article can be accessed here
© 2017 Informa UK Limited, trading as Taylor & Francis Group
2 H. SANTAMARÍA-GARCÍA ET AL.

may modulate fronto-striatal activity underlying core cog- et al., 2015; Melloni et al., 2012). The LRP-r component,
nitive processes in OCD such as increased self-monitoring, in turn, captures cognitive control processes that
difficulties in cognitive control and disrupted motor con- extend into immediate control of action, encompassing
trol mechanisms. For this purpose we used Event Related response, inhibition, response conflict, and error mon-
Potentials (ERP), which reliably reflect error monitoring, itoring (Danielmeier, Wessel, Steinhauser, & Ullsperger,
cognitive and motor control (Danielmeier, Wessel, 2009; Johannes et al., 2001). Available evidence has
Steinhauser, & Ullsperger, 2009; Falkenstein, Hoormann, shown an altered pattern of LRP-r component in OCD
Christ, & Hohnsbein, 2000; Kappenman et al., 2012; patients, which has been hypothesized to be due to a
Melloni et al., 2012; Otten & Jonas, 2013). In particular, dysfunctional fronto-striatal circuitry, likely underlying
error monitoring activity is captured by the Error Related impairments in motor inhibition related to compulsive
Negativity (ERN) and Error Positivity (Pe) components behaviour (Johannes et al., 2001; Lei et al., 2015). Thus,
(Chamberlain & Menzies, 2009; Endrass et al., 2010; van our complementary goal was to explore how the social
Veen & Carter, 2006), while mechanisms of cognitive con- context could modulate the N2 and LRP-r components
trol and conflict adaptation can be measured by the in OCD patients in comparison to healthy subjects.
frontal N2 component (Otten & Jonas, 2013; Yeung & In this study, a sample of OCD patients and healthy
Cohen, 2006). Motor control and inhibition processes are controls took part in an experimental framework in
reflected in the Lateralized Readiness Potentials (LRP-r) which the social context was created by using a social
(Ibanez et al., 2012; Kappenman et al., 2012; Töllner, hierarchy (Santamaría-García, Burgaleta, & Sebastián-
Rangelov, & Müller, 2012). Gallés, 2015; Santamaría-García et al., 2013; Zink et al.,
Different studies have reported larger amplitudes of 2008). Previous studies have reported that across ani-
ERN and Pe components in OCD patients, reflecting an mal species social hierarchy is a crucial social domain
amplified error-monitoring processing (Melloni et al., involved in different biological processes such as survi-
2012; Menzies et al., 2007; Riesel, Endrass, Kaufmann, val, reproductive success, cognitive processing, motiva-
& Kathmann, 2011). The ERN component is a robust, tion and social behaviour regulation (Boyce, 2004;
trait-like electrophysiological index associated to the Mehta, Jones, & Josephs, 2008; Sapolsky, 2004; Zink
functioning of the error-detection system (including et al., 2008). In this study ERP data was recorded while
the anterior cingulate cortex), which is considered a participants played a game consisting of a difficult
quantitative endophenotype of OCD. The ERN has visual decision task (numerosity) in the presence of
shown to be non-directly affected by disorder severity simulated inferior or superior players. Playing in the
or by the treatment (Menzies et al., 2007; Olvet & presence of an inferior player was expected to confer
Hajcak, 2008; Riesel et al., 2011), (Stern et al., 2010). a superiority position to the participant, whereas play-
Additionally, the Pe component has been described as ing in the presence of a superior player would have the
an index of awareness in detecting errors and has been opposite effect (Santamaría-García et al., 2015;
associated to activity in the posterior cingulate cortex Santamaría-García et al., 2013). Aiming to connect our
(Endrass et al., 2010; van Veen & Carter, 2006). These findings with the clinical features of the disorder, within
alterations in error processing underlie OCD’s obsessive the group of OCD patients, we evaluated to what
thoughts, concern over mistakes, high expectations extent the ERP and behavioural data during the social
from other people’s evaluations and repetitive beha- context correlate with the clinical measurements of
viours (Endrass et al., 2010; Melloni et al., 2012). OCD symptoms’ severity and the severity of comorbid
Therefore, given the well-established role of the ERN/ depressive and anxiety symptoms.
Pe as a neuromarker of OCD, the main goal of this We predicted that OCD patients, but not controls,
research was to assess to what extent the social context would display lower ERP amplitudes in the inferior
modulates such OCD-specific error monitoring compo- player than in the superior player condition for the
nents in comparison to healthy subjects. ERN/Pe and LRP-r components, and the inverse pattern
Furthermore, disruptions in cognitive and motor for the N2 component (denoting, respectively, reduc-
control mechanisms may also stem from OCD’s fronto- tion of error detection hyperactivity, enhanced motor
striatal dysfunction (Folstein & Van Petten, 2008; Otten control and better cognitive control when patients
& Jonas, 2013; Yeung & Cohen, 2006). Though larger adopted a superiority position). Furthermore, if the
amplitudes in N2 are associated with high conflict social effect is indeed a key factor for OCD cognitive
adaptation and improved cognitive control (Folstein & impairments, then it is expectable that the OCD pattern
Van Petten, 2008), OCD patients have exhibited lower of brain activity, when performing the task in a super-
negativities in the N2 fronto-central component, argu- iority position, would tend to approach the brain activ-
ably reflecting their impaired cognitive control skills (Lei ity levels observed for control participants. In addition,
SOCIAL NEUROSCIENCE 3

such differences in brain processing would be paral- Table 1. Clinical characteristics of OCD patients.
leled by behavioural changes, so that the presence of Variable Mean (SD), range
a social context might affect the accuracy and the Age, yrs a 33.1 (8.3), 27–40
Gender, m/f b 37/32
reactions times (RT) in the visual decision task. Education, yrs c 13.75 (2.8), 5–19
HDRS 11.7 (4.8), 6–18
HARS 18.1 (4.4), 16–26
Age at onset of OCD, yrs 18.8 (7.9), 5–40
Duration of illness, yrs 12.8 (9.4), 1–45
Methods Y-BOCS-Total 25.4 (2.4), 21–30
Comorbid mood/anxiety disorders no. (% cases)
Bipolar disorder type II 1 (5)
Participants Social phobia 1 (5)
Major depressive disorder 1 (5)
Twenty (right-handed) outpatients with OCD (10 females; Medication at time of study no. (% cases)
mean age 35.25, range 27 – 40 years, 13.75 ± 2.8 years of Medication-free (> 4 weeks) 2 (10)
Clomipramine 2 (10)
education, range 5–19) were recruited from the OCD Escitalopram 5 (40)
Clinic at the Bellvitge University Hospital (Barcelona, Fluoxetine 2 (10)
Fluvoxamine 2 (10)
Spain). All patients fulfilled DSM-IV criteria for OCD for a Sertraline 1 (5)
period of at least one year. Diagnoses were made on the Paroxetina 1 (5)
basis of structured interviews conducted independently HDRS = Hamilton Depression Rating Scale; HARS = Hamilton Anxiety
by two trained psychiatrists using the Structured Clinical Rating Scale; Y-BOCS = Yale-Brown Obsessive-Compulsive Scale.

Interview for DSM-IV Axis I Disorders-Clinician Version


(SCID-CV). Exclusion criteria were aged under 18 or over
Materials
65 years, psychoactive substance abuse/dependence
(either current or in the past six months), mental retarda- Social context setting
tion, psychotic or bipolar disorders, or severe organic or Social context was created using a procedure validated
neurological pathology. Comorbid major depression and in previous studies (Zink et al., 2008) (Santamaría-García
other anxiety disorders were not considered an exclusion et al., 2013) (see Figure 1). We used brief social videos
criterion provided that OCD was the main diagnosis and to introduce simulated players’ profiles and establish
the primary reason for seeking assistance. All the patients the initial hierarchical features, followed by an interac-
had been taking stable doses of medication for at least tive game in which the participants performed a visual
3 months prior to the time of testing. OCD severity was discrimination task in the presence of other (simulated)
assessed using the Spanish version of the clinician-admi- players and received updated information about both
nistered Yale-Brown Obsessive-Compulsive Scale (Y- participant’s and opponent’s performance to generate a
BOCS) (Vega-Dienstmaier et al., 2002), and depressive continuous social comparison context.
and anxiety symptoms were assessed by means of the
17-item Hamilton Depression Rating Scale (HDRS) Social videos. A total of eight different video profiles
(Hamilton, 1960) and 14-item Hamilton Anxiety Rating (approximately 2 min each) were created. The profiles
Scale (HARS) (Hamilton, 1959). Table 1 provides the clin- crossed gender (male, female) and hierarchy (high, low
ical information of the OCD participants. Twenty (right- status), and were interpreted by four confederates (two
handed) healthy controls from the same socio-demo- males, two females). Each confederate followed two
graphic environment and with a comparable age and scripts (high or low status) that presented the character’s
gender distribution (10 females; mean age 33.59; age personal, work and academic achievements. Implicit cues
range 29 – 40 years 13.2 +/- 1.8 years of education, related to the social superiority of the confederates were
range 10–16) were also included. Each control subject controlled to avoid substantial differences in age, facial
underwent the Structured Clinical Interview for DSM-IV expressions and attire. Each participant saw two video
non-patient version to exclude the presence of any Axis I profiles, one for the superior player and one for the
psychiatric disorder. Remaining exclusion criteria were the inferior player. Half of the participants saw the superior
same as those applied to OCD patients. Written informed and then the inferior confederate, while the other half
consent was obtained from each participant after a full saw them in the reverse order.
description of the study, which was conducted in compli-
ance with national legislation and the principles set out in Visual discrimination task. In each trial of the visual
the Declaration of Helsinki. The ethics committee of discrimination task, we presented two rectangles of
Bellvitge University Hospital and the ethics committee of red dots (of constant diameter, shape and brightness)
the Brain Cognition Centre of the Pompeu Fabra on a black background, one at the top of the screen,
University also approved the study. and the other at the bottom. The two rectangles
4 H. SANTAMARÍA-GARCÍA ET AL.

Figure 1. General procedure. The procedure consisted of three stages: Social Video Profiles (stage 1), Neutral trials (2) and Social
trials (3). During stage 2, two confederates represented the superior and the inferior player. During stage 1, participants performed
70 trials in a neutral context (here, a hierarchical scenario was avoided). During stage 3, participants performed the visual
discrimination task while comparing their performance to the simulated players.
This figure is reproduced with permission of Journal of Neuroscience.

contained a different number of dots, and partici- Procedure to build social context. Each trial of the
pants were asked to decide which rectangle con- game started with a 2 s presentation of the opponent’s
tained more dots. The sum of the dots displayed in photograph, along with three or one ranking stars (for
the two rectangles was 1000 dots, each rectangle the superior and inferior player respectively), followed
having a different percentage of this total amount. by the visual discrimination task. The dot rectangles
The percentage of red dots was complementary were presented during 1 s. Participants then decided
between the rectangles (e.g., if one had 49% of the which rectangle contained more dots and answered
dots, the other had 51%; see Figure 1). We created with the corresponding joystick movement (up or
nine levels of dot percentages (44, 46, 48, 49, 50, 51, down) using their right hand. Behavioural Reaction
52, 54, 56). The visual discrimination task and the times (RT) and accuracy were recorded. They were
dynamic game structure were designed using given feedback on their response that stayed on the
MATLAB version 7.9.0 (R2009b) with the screen for 2 s. The feedback consisted of pictures of the
Psychophysics Toolbox version 3.0.8. participant with the opponent above, and the outcome
SOCIAL NEUROSCIENCE 5

(a money bill meaning correct, an “X” meaning incorrect performance would be compared to that of the two
or a “time over” message) below. Both participant and players who already completed the task, and that all
simulated player could win or lose in a trial. The trial three players would be ranked depending on their
ended with a fixation cross for 0.5 s. The participants performance during the game. The participants were
could rest for up to 2 min between blocks. Regardless told that their performance could be compared to that
of the results of the game, participants did not receive of future participants as well. To reinforce the credibility
any real monetary compensation. on the procedure, participants were told that at the end
In order to be familiarized with the visual task, all of the game, they would record a brief video where
participants were required to perform 70 trials of the they spoke about themselves, reporting on their jobs,
task in a neutral context (see Figure 1). This set of trials activities and achievements.
was used as a baseline measure (“social-free” scenario)
of the performance of each participant. Afterward, par-
ticipants performed the visual discrimination task in the EEG/ERP methods
hierarchical social context. The game began right after All participants were tested in an electrically-shielded
training, including five blocks of 36 trials each (180 testing room in the Neuroscience laboratories of the
total, 90 in presence of each simulated player). In each Centre for Brain and Cognition (Pompeu Fabra
block (approximately 5 min), the participants played University, Barcelona, Spain) where electro-encephalo-
nine consecutive trials in presence of a simulated player graphy (EEG) activity was recorded. Participants were
followed by nine trials in presence of the other simu- situated approximately 50 cm in front of a 19-inch
lated player, and this sequence was repeated once, screen, at an angle of vision of around 35°. The experi-
followed then by the presentation of the updated rank- ment began after electrode application.
ing. Rank order was set by adjusting the superior or The EEGs were recorded from 31 scalp sites. We
inferior player’s behaviour following an algorithm pre- placed two bipolar electrodes above and below each
viously developed (Santamaría-García et al., 2013). participant’s left eye to record eye movements, two
To maintain the hierarchy based on skills in the electrodes on the mastoids, and a reference electrode
game, we simulated performance of the hierarchical on the nose. The EEG recordings were digitized at
players in the game. One of the simulated players 250 Hz. All electrode impedances were below 3
performed, on average, better than the participant, KOhms. The EEG data was low and high-pass filtered
thus consistently holding a higher rank status. The (30–0.03 Hz). All the EEG data was semi-automatically
other simulated player showed lower performance, screened offline for eye movements and muscle arte-
and hence had a lower rank status. Important to note, facts. The segments containing such artefacts were
is the participant’s results were not simulated/ rejected. We rejected a similar proportion of segments
manipulated. (around 5%) in both groups (patients and controls). ERP
The social status simulated during the social videos components were then extracted.
was consistent with the simulated ranking during the We performed two types of analyses: Stimulus-
game. The role played by confederates was counter- locked (locked at presentation of visual discrimination
balanced across participants. The nature of the game task, in order to analyze social modulation of N2 com-
was non-competitive because the participant and the ponent) and response-locked analyses (locked after
simulated players could win, lose or have different out- response selection in the visual discrimination task in
comes in the same trial. As the social role of each order to analyse ERN/Pe and LRP-r components). For
simulated player was maintained constant throughout stimulus-locked analyses, the EEGs were segmented
the game, the social hierarchy could be considered into 1100-ms epochs ranging from 100 ms before
stable. Thus, each participant was always in presence stimulus onset, to 1000 ms post onset. Before aver-
of a superior (inferiority position) or an inferior player aging, segments were baseline-corrected by subtract-
(superiority position). The whole experiment was ing the mean amplitude of the pre-stimulus interval
designed to increase participants’ feeling of being (−100–0 ms). In the response-locked analysis, the EEGs
involved in a realistic game. data was segmented into 1100-ms epochs ranging
To control for possible interactions between gender from 200 ms before response onset to 900 ms post
and hierarchy, male participants played with male simu- response. Before averaging, segments were baseline-
lated participants, and female participants with females. corrected by subtracting the mean amplitude of the
Participants were first informed that they would play a pre-stimulus interval (−200–50 ms) as done in previous
visual decision game, and then were notified that their studies (-Falkenstein et al., 2000).
6 H. SANTAMARÍA-GARCÍA ET AL.

Extraction of ERP components Statistical analyses


Error monitoring components. The ERN component
Separate analyses of variance (ANOVA) on the ampli-
was studied in the time window 50–200 ms after
tude and latency of each component were conducted
error-response, and the Pe component was analyzed
with Group (patients vs. healthy controls) with a
between 500–650 ms upon error-response. Both com-
between-subjects factor, and Hierarchy (superior and
ponents were studied in the same group of frontocen-
inferior) with a within-subjects factor. By using
tral electrodes (F3, F4, FZ), following previous studies
Bonferroni correction we controlled for error through
(Melloni et al., 2012; Xiao et al., 2011). Mean amplitudes
multiple comparisons in all analyses. For the sake of
in these electrodes were averaged. Note that we pre-
completeness, we used a similar design to study poten-
viously found no significant differences in modulation
tial effects over behavioural measures (mean reaction
of ERN and Pe in these electrodes (p > .1).
time (RT) and accuracy). For reaction times, we have
also analyzed intra-individual variability (standard
Frontal N2 component. The frontal N2 component deviation and coefficient of variation (see
was studied in the range of 250-350ms after stimulus Supplementary materials, section 1.2)). For both ERP
onset, in frontocentral electrodes (FZ /F3/F4 and CZ). and behavioural analyses we assessed effect sizes,
We chose these sets of electrodes and time windows which were calculated through the partial eta squared
based on the topographical distribution of grand aver- (η2) ratio. Finally, correlations between the amplitude
aged ERP activity and on previous studies (Folstein & of the different ERP components and clinical data were
Van Petten, 2008; Yeung & Cohen, 2006). Mean ampli- assessed by means of Pearson correlation analyses. All
tudes in these electrodes were averaged, as no signifi- the analyses were performed using MATLAB version
cant differences in modulation of N2 were found 7.9.0 (R2009b).
between these electrodes (p > 0.1).

Lateralized readiness potentials. LRP-r waveforms Results


were calculated using the difference in contralateral-ipsi- ERP
lateral activation for C3 and C4 electrode pairs in each
hemisphere, following previous studies (Miller, Patterson, We performed separate 2 × 2 ANOVAs (Group (OCD vs
& Ulrich, 1998; Töllner et al., 2012). LRP-r components healthy controls by Hierarchy (Superior vs. Inferior) for
were computed using a baseline of −800 to −600 ms for amplitudes of the ERP components related to the function-
response-locked averages. Given that participants used ing of core cognitive processes in OCD (ERN/pe, N2, LRP).
their right hand to respond, we computed a contralateral The analyses revealed a significant main effect of
(C3) – ipsilateral (C4) difference waveform. Such waveform Group (OCD vs. healthy controls) in the amplitudes of
was extracted separately for each condition (trials in pre- all ERP components (ERN: F1, 39 = 6.32, p < .01, η2 = 0.2;
sence of superior player vs. trials in presence of inferior Pe: F1, 39 = 7.02, p < .01, η2 = 0.21; N2: F1, 39 = 5.67,
player). LRP-r amplitudes and latencies were measured p < .01, η2 = 0.16; LRP-r: F1, 39 = 4.54, p < .01, η2 = 0.11).
from the resulting difference waves. We used 90% of the Furthermore, the Group by Hierarchy interaction was
maximum LRP-r activation as optimal criteria for defining significant for all four analyzed components (ERN: F1,
LRP-r onset latencies following a procedure used in pre- 39 = 6.05, p < .01 η2 = 0.19; Pe: F1, 39 = 5. 97, p < .05,

vious studies (Töllner et al., 2012; Ulrich & Miller, 2001). η2 = 0.15; N2: F1, 39 = 6.31, p < .01, η2 = 0.21; LRP-r: F1,
The amplitudes of the LRP-r were calculated by averaging 39 = 3. 83, p < .05, η2 = 0.06).

five sample points before and after the maximum deflec- All components showed the same pattern of inter-
tion obtained in the time window of 100–20 ms pre- action. Firstly, effects of social hierarchy were only
response. We controlled noise on latency measure using observed in the patient group. For the OCD group the
a low-pass filter prior to the latency measures (Gaussian ERN, Pe, N2 and LRP-r components had larger ampli-
impulse response function, half-amplitude cut- tudes in trials played with a superior player (inferiority
off = 23.2 Hz, full width at half maximum = 18.8 ms). position) (see Table 2, it displays the different statistical
Furthermore, incorrect trials and trials with artefacts values). Secondly, patients and controls only differed
were excluded prior to averaging following previous stu- when playing in presence of a superior player (inferior-
dies (Töllner et al., 2012). A schematic figure of brain sites ity position), while showing equivalent responses in
of analyses of each ERP component is included in the presence of an inferior player (superiority position)
supplementary material (see Supplementary Figure 1). (see Table 2, and see also Figures 2–5).
SOCIAL NEUROSCIENCE 7

Behaviour

The table shows the statistical descriptive analyses for each ERP component (Error Related Negativity, ERN; Error Related Positivity, Pe; frontal N2; response-locked Lateralized Readiness Potential, LRP-r), considering the
group (OCD, patients) and condition (performing the task against a Superior or Inferior player). F statistics, p values and N2 and effect sizes are shown for the Group by Hierarchy interaction. The “ns” symbol means no-
OCD_inf vs. Controls inf
We performed separate 2 × 2 ANOVAs (Group by
Hierarchy) for accuracy and RTs (mean and dispersion)

ns

ns

ns

ns
during the visual discrimination task. Significant results
were observed for RT-based measures, but not for accu-
racy. First, concerning mean RT analysis, we observed a
Group effect (F1, 39 = 6.29, p < .01, η2 = 0.13). On
average, OCD patients were slower than healthy con-
OCD_sup vs. Controls sup

p < 0.01; η2 = 0.29

p < 0.05; η2 = 0.17

p < 0.05; η2 = 0.31

p < 0.05; η2 = 0.19


trols. We also observed a main effect in the Group by
Statistical analyses

Hierarchy interaction (F1, 39 = 2.77, p < .04, η2 = 0.05).


Independent comparisons (for OCD patients and con-
trols) showed a significant effect of hierarchy only for
the OCD patients (p < .05, η2 = 0.06). On average, OCD
patients were faster when they performed the task in
presence of inferior players. Analyses for the control
p < 0.01; η2 = 0.19

p < 0.05; η2 = 0.15

p < 0.05; η2 = 0.06

group did not reach significant effects due to social


p < 0.01;η2 = 0.21
Group* Hierarchy

hierarchy (p > .7)(see Figure 6).


F1, 39 = 5. 97,

F1, 39 = 3. 83,
F1, 39 = 6.05,

F1, 39 = 6.31,

Correlations
Lastly, we evaluated the correlations between the ampli-
Stat.

Stat.

Stat.

Stat.

tude of each ERP component in the presence of each


Sig.

Sig.

Sig.

Sig.

hierarchical player and the scores in three different clinical


scales assessing OCD symptom severity and the severity of
Inferior
1.57

−0.49

−2.01

−0.19
2.7

2.2

3.6

1.2

comorbid depressive and anxiety symptoms (Y-BOCS,


HDRS and HARS scales, respectively). We found a significant
significant differences. Results revealed significant differences due to social hierarchy only for OCD group

correlation between the Y-BOCS score and the difference in


Table 2. Statistical descriptive for ERP components in OCD patients and healthy controls.

Control Sup vs. Control Inf = ns

Control Sup vs. Control Inf = ns

Control Sup vs. Control Inf = ns

Control Sup vs. Control Inf = ns

amplitude of the ERN component in presence of a superior


Controls

vs. inferior player (superiority position) (r = 0.42, p < .05).


Likewise, a significant correlation was also observed
Superior

between the Y-BOCS score and the amplitude of the N2


1.54

−0.52

−1.92

−0.21
2.5

2.0

3.8

1.1

component in the presence of a superior player (inferiority


position), (r = 0.52, p < .05). No significant correlations were
observed between the Y-BOCS score and behavioural mea-
sures between neither the former nor the severity of
comorbid depressive and anxiety symptoms.
Inferior
1.57

−0.74

−1.99

−0.29
2.3

2.1

4.4

1.0

Discussion
=

Can social context influence the core cognitive processes


OCD Sup vs. OCD Inf

OCD Sup vs. OCD Inf

OCD Sup vs. OCD Inf

OCD Sup vs. OCD Inf


OCD

p < 0.01; η2 = 0.11

p < 0.01; η2 = 0.24

p < 0.01; η2 = 0.29

p < 0.01; η2 = 0.16

involved in the physiopathology of OCD? More specifically,


Superior
−1.21

1.52

−0.05

−0.65

can a social hierarchy scenario modulate OCD’s fronto-


2.8

2.2

4.1

0.9

striatal alterations such as error monitoring, cognitive con-


trol and motor control processes? Here we addressed
these questions by analyzing ERP data in a social hierarchy
context, and observed striking differences between OCD
Social-Effect

Social-Effect

Social-Effect

Social-Effect

patients and healthy controls in the way contextual social


information modulates error-monitoring, cognitive control
Mean

Mean

Mean

Mean

and motor control brain activity. Critically, performing a


SD

SD

SD

SD

visual discrimination task in a superiority position (i.e.,


playing with an inferior player) reduced the levels of aber-
LRP-r
ERN
ERP

N2
Pe

rant ERP signals in OCD patients to match the normal brain


8 H. SANTAMARÍA-GARCÍA ET AL.

Figure 2. Baseline differences between OCD patients and controls in ERP components. Differences over ERN/Pe, N2 and LRP-r
components were analyzed between patients and healthy controls. Larger amplitudes were found for patients compared to controls
in ERN/Pe (A) and LRP-r (C), whereas controls displayed higher N2 amplitudes than patients (B). *p < .05.

activity patterns of healthy controls. The following para- Social effects on ERN and Pe components
graphs will discuss these results in detail.
Crucially, aside from the observed differences between
patients and controls in the ERP-based cognitive function-
ing, we observed social effects on error-monitoring pro-
ERPs results cesses, reflected in ERN and Pe modulations, as ERN and Pe
amplitudes were larger in presence of superior player than
First, we found larger amplitudes in the ERN and Pe
in presence of an inferior player (see Figure 3 and
components in patients when compared to healthy con-
Supplementary Figure 2). Higher ERN and Pe amplitudes
trols, consistently with the usual pattern reported in pre-
displayed by patients in the presence of a superior player
vious studies (Endrass et al., 2010; Riesel et al., 2011) (see
(i.e., when patients was placed in an inferiority position), are
Figure 2 and Supplementary Figure 1). Amplified error
consistent with the well-known social sensitivity of OCD
signals (larger ERN and Pe) in OCD have been hypothe-
patients (Bystritsky et al., 2001; Pace et al., 2011). In healthy
sized to underlie obsessive thoughts, concern over mis-
populations there is evidence suggesting that different
takes, high expectations from people’s evaluations and
emotional, affective or motivational factors might affect
repetitive behaviours (Endrass et al., 2010; Melloni et al.,
the amplitude of the ERN response (Fishman & Ng, 2013;
2012).
SOCIAL NEUROSCIENCE 9

Figure 3. Social effects on Error-Monitoring processes. The upper panel shows social modulations on the ERN and the Pe
components in the OCD group. Significant differences were only found when OCD patients performed the task in the presence
of superior players (i.e., when OCD patients were placed in an inferiority position). The central panel shows no significant effects of
Hierarchy in controls. For visualization purposes, the bottom panel shows results for OCD and controls superimposed, illustrating the
significant Group x Hierarchy interaction for both ERN and Pe components. Squared regions indicate the windows of significant
interactions. * p < .05.

Melloni et al., 2012; Olvet & Hajcak, 2008). For instance, the Conversely, OCD patients and controls exhibited
ERN may be influenced by certain personality traits char- similar amplitudes in ERN and Pe components in pre-
acterized by a higher emotional reaction to errors (e.g., sence of an inferior player. In other words, adopting a
high neuroticism) (Fishman & Ng, 2013). Consistently, our superiority role diminished OCD patients’ ERN signals to
results suggest that social context is of special value in the those levels observed in healthy participants. Arguably,
specific case of OCD patients, perhaps because increased facing an inferior opponent (thus assuming a superior
social sensitivity translates into a higher emotional load role) may indeed decrease social anxiety and/or impact
associated with the hierarchical scenario. the emotional evaluation of the social context,
10 H. SANTAMARÍA-GARCÍA ET AL.

Figure 4. Social effects on N2 component. The upper panel shows social modulations on the N2 component in the OCD group.
Significant differences were only found when OCD patients performed the task in the presence of superior players (i.e., when OCD
patients were placed in an inferiority position). The central panel shows no significant effects of Hierarchy in controls. For
visualization purposes, the upper and central panels are superimposed in the bottom panel, illustrating the significant Group x
Hierarchy interaction for N2. Squared regions indicate the windows of significant interaction * p < .05.

therefore reducing abnormal error-monitoring pro- frontal N2 component (Folstein & Van Petten, 2008).
cesses in OCD patients. We supported previous evidence showing that OCD
patients display lower negativities in the N2 fronto-
central component (see Figure 2), indexing poor cog-
Social effects on N2 component
nitive control and conflict adaptation (Folstein & Van
We went one step further by showing that social Petten, 2008; Yeung & Cohen, 2006). Importantly,
effects were not specific to the ERN, but extended results also showed social effects on N2 amplitudes
into components indexing cognitive and motor con- in OCD patients. In particular, OCD patients exhibited
trol. To measure cognitive control we focused on the lower N2 amplitudes when performed the task in the
SOCIAL NEUROSCIENCE 11

Figure 5. Social effects on lateralized readiness potentials. The upper and central panels show the LRP-r waveforms elicited from
patients and controls, respectively. In the patients group, but not in controls, significant differences were found when OCD patients
performed the task in presence of superior players (i.e., when OCD patients were placed in an inferiority position). For visualization
purposes, the bottom panel displays the upper and central panels superimposed, illustrating the significant Group x Hierarchy
interaction *p < .05.

Figure 6. Social effects on participants’ behavioural performance. A main effect of Group was observed for reaction times. A
significant hierarchy effect over participant’s reaction times was observed within the OCD patients group. Error bars represent s.e.m.
Empty star depicts a p < .05.

presence of superior players (i.e., when OCD patients been reported in conditions that evoke anxiety and
assumed an inferiority role) than in the presence of in situations with high requirements of attentional
inferior players (see Figure 4 and Supplementary resources (Folstein and Van Petten 2008; Melloni
Figure 2). Modulations over N2 amplitudes have et al. 2012). In addition, N2 amplitudes have been
12 H. SANTAMARÍA-GARCÍA ET AL.

reported, as reflecting monitoring of cognitive and In addition, our results showed that when OCD
emotional conflict (Larson & Clayson, 2011). Those patients performed the task in presence of an inferior
evidences suggest that OCD patients may present player, the LRP-r signals were equivalent to those
reduced cognitive and emotional control abilities observed for controls. Lower LRP-r amplitudes in the
when they must assume an inferiority role. Again, presence of the inferior player could therefore be indi-
our results support that in OCD patients, the social cative of decreased accumulation and demands of
sensitivity may impacts a group of core cognitive motor evidence in a social context where patients had
processes usually reported as altered in those patients. a higher social position, leading to an increased motor
It is significant to mention that consistent with our inhibition process in this context.
previous work (Santamaría-García et al., 2013), results
did not revealed effects of social hierarchy over N2
Social effects on behavior
amplitudes in controls. In addition, as it was the case
for the ERN results, it is of note that OCD-specific At the behavioural level we observed larger group
amplitudes of frontal N2 in the presence of inferior effects in reaction times. Furthermore, we observed
players were not significantly different from the N2 significant effects of social hierarchy over reaction
amplitudes observed in healthy controls. times for the OCD group, but not in healthy controls.
OCD patients were slower and less consistent (as mea-
sured by intra-individual variability analyses (see sup-
Social effects on LRP-r
plementary materials section 1.2) in trials performed
Regarding our motor control analyses, we observed with a superior player than with an inferior player (see
larger LRP-r amplitudes in OCD patients vs. controls Figure 6). Although behavioural results obtained with
during the neutral trials confirming the difficulties in this particular experimental paradigm do not provide
motor inhibition and motor control mechanisms (larger fine-grained information about the main cognitive pro-
LRP-r amplitudes in OCD vs. controls) in these patients cesses of interest (and therefore lack the power of the
(Johannes et al., 2001). Interestingly, and following the ERP approach), they suggest a potential transfer from
pattern of results found for ERN/Pe and N2, OCD-spe- the experimental social setting to the actual patient’s
cific social hierarchy modulations on the LRP-r provided behaviour. Indeed, such findings are reinforced by the
additional information about how social context affects existence of positive correlations between the measure-
control mechanisms in patients, extending into motor ments of the two ERP components (ERN and N2) with
preparation and motor control mechanisms. The social obsessive-compulsive symptom severity.
context significantly modulated LRP-r, so that perform- Our results generate certain considerations that
ing the task in presence of a superior player induced require further investigation. Although it is true that
larger LRP-r signals than performing the task in pre- previous studies have shown that ERN, N2 and LRP-r
sence of an inferior player (see Figure 5 and components can be modulated by general mechan-
Supplementary Figure 2). This effect suggests reduced isms of distress, hyper arousal or trait measurement
motor control and inhibition abilities when the patients such as extraversion or anticipatory pleasure (Fishman
had an inferiority social role with respect to the simu- & Ng, 2013), some of our results allow us to support
lated player. This result can be interpreted in light of the notion that our findings are indeed reflecting a
recent evidence demonstrating a tight coupling social modulation of core cognitive processes relevant
between emerging decision variables and preparatory to OCD. The fact that we did not observe changes in
activation in cortical motor areas (Chamberlain et al., all ERP components, or in the ERP components more
2007). Indeed, activity in the pre-supplementary motor sensitive to arousal and distress mechanisms (such as
area (pre-SMA) is correlated to the amount of accumu- C1, P1, see supplementary materials, section 1.1), indi-
lated evidence in decision phases (De Wit et al., 2012; cates that the impact of social context in OCD
Gluth, Rieskamp, & Büchel, 2013; Töllner et al., 2012). patients is not only determined by unspecific changes
Considering those evidences it is possible that in OCD in arousal or secondary to general distress mechan-
patients, motor preparation and motor control pro- isms (Di Russo, Martínez, Sereno, Pitzalis, & Hillyard,
cesses are unregulated by enhanced social sensitivity 2002). By contrast, we observed a selective modula-
and emotional pressure associated to have an inferiority tion by social context over the ERP components
position. This result is in line with the results reported related to core cognitive process, namely ERN, PE,
for ERN, PE and N2 and supports a strong influence of N2 and LRP-r. Moreover, if the ERP results were due
the social context on the group of sensitive cognitive to modulation of unspecific processes related to gen-
processes in OCD patients. eral distress mechanisms and arousal, we should have
SOCIAL NEUROSCIENCE 13

observed significant correlations between ERP modu- cognitive processes. Our results open the door to addi-
lations and general anxiety indicators, such as the tional research on the impact of the social context on
HARS scale (some studies have related the anxiety OCD symptoms as well as on therapeutic options based
states to high levels of arousal and distress, this rela- on the simulation of this kind of social scenarios.
tionship has been supported by studies analysing ERP
data, see (Xiao et al., 2011)). Conversely, we have
observed significant correlations between two ERP
Acknowledgments
components and Y-BOCS scores, suggesting a specific This research was supported by grants from the Spanish
relationship with obsessive-compulsive symptoms. In Ministerio de Economía y Competitividad (PSI2012-34071),
this sense, it is worth highlighting the correlation the Catalan Government (SGR 2009-1521 and SGR 2014
1672) and the Carlos III Health Institute (PI09/01331, PI10/
between the ERN component and the Y-BOCS score,
01753, PI10/01003, CP10/00604, PI13/01958, CIBER-CB06/03/
since ERN has been considered as a suitable OCD 0034). C. Soriano-Mas is funded by a ‘Miguel Servet’ contract
endophenotype (Riesel et al., 2011), (Olvet & Hajcak, from the Carlos III Health Institute (CP10/00604). N. Sebastián-
2008). Therefore, it seems likely that social effects are Gallés received the “ICREA Acadèmia” prize for excellence in
indeed modulating the neural mechanisms specifically research, funded by the Generalitat de Catalunya. Burgaleta
related to OCD symptoms, but not interacting with Miguel is funded by Juan de la Cierva grant, code: FPDI-2013-
17528.
nonspecific mechanisms of anxiety.
Despite of these considerations, our results present
some limitations. We did not know to what extent Disclosure statement
social effects reported in the OCD patients could be
No potential conflict of interest was reported by the authors.
related to the presence of social phobia in this sample.
In fact, previous studies have reported that social pho-
bia and OCD can be simultaneously present in some Funding
subjects (Camuri et al., 2014) (Baldwin, Brandish, &
Meron, 2008). In addition, there are considerable evi- This work was supported by the Consejo Superior de
Investigaciones Científicas [PI09/01331, PI10/01753, PI10/
dences showing that patients with social phobia course 01003, CP10/00604, PI,PSI2012-34071]; Instituto de Salud
with higher social sensitivity (Boll et al., 2016; Gaebler, Carlos III [CP10/00604,FPDI-2013-17528].
Daniels, Lamke, Fydrich, & Walter, 2013; Veit et al.,
2002). Future studies should explore and control to
what extent in that social effects are related to the Ethics statement
presence of social phobia symptoms. Additional insight Permission from the Clinical Research Ethical Committees
regarding the specificity of social modulations observed (CEICs) was sought and obtained before the individual subjects
here could be gained by investigating potential effects were evaluated. A written consent process was used. We
over cognitive processes altered in patients with anxi- obtained a written consent of each patient and participant.
No participant refused to participate in the study. Since signed
ety and depressive disorders. consent forms constitute a possible source of concern for the
All in all, we observed that in OCD patients error- protection of respondents’ confidentiality, signatures were col-
monitoring processes were importantly modulated in lected during the written consent process. The study, including
the presence of a social hierarchy. To our knowledge, the written consent process and script, was reviewed and
this is the first evidence showing social effects on ERN approved by The Clinical Research Ethical Committees (CEICs)
of the Pompeu Fabra University Barcelona Spain and by the
in a group of patients with disrupted error monitoring
Ethical Committee of Bellvitge Hospital in Barcelona Spain.
processes. Here we provide novel evidence showing (http://www.imim.es/comitesetics/ceic/en_index.html).
that the functioning of the error-detection system in
OCD is affected by the presence of a social context,
likely suggesting a modulation of the activity of the References
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