Journal of Obsessive-Compulsive and Related Disorders 3 (2014) 65–70
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Response inhibition to emotional faces in childhood obsessive-compulsive disorder Allison M. Waters a,b,n, Lara J. Farrell a,b a b
School of Applied Psychology, Griffith University, Queensland 4222, Australia Griffith Health Institute, Griffith University, Queensland 4222, Australia
art ic l e i nf o
a b s t r a c t
Article history: Received 23 August 2013 Received in revised form 3 December 2013 Accepted 4 December 2013 Available online 12 December 2013
Background and objectives: Evidence regarding the role of response inhibition in obsessive-compulsive disorder (OCD) is inconsistent. Most prior research has examined response inhibition to emotionally neutral stimuli or task demands. Given that OCD is characterised by distress due to unpleasant and undesirable thoughts/images and compulsive behaviours, this study examined response inhibition to emotional stimuli in children with OCD compared to healthy controls. Methods: Children with OCD (N ¼12) and controls (N¼ 15) completed an emotional Go/No Go task in which they responded on some trials (i.e., Go trials) when neutral faces were presented amongst angry or happy faces to which children were instructed to avoid responding (i.e., No Go trials) or when angry and happy faces were presented as Go trials and children were instructed to avoid responding to neutral faces. Results: Children with OCD made more false presses on No Go trials than healthy controls, regardless of emotional expression. This was not due to a speed-accuracy trade-off. There were no significant group differences on Go trials. Limitations: The sample size was small and the emotional Go/No Go task did not include a neutral condition. Conclusions: Results are discussed in terms of response inhibition deficits in childhood OCD. & 2013 Elsevier Ltd. All rights reserved.
Keywords: Obsessive compulsive disorder Response inhibition Emotional faces Emotional Go/No Go task
1. Introduction Childhood obsessive-compulsive disorder (OCD) is a chronic and disabling neuropsychiatric condition with lifetime prevalence estimates between 1% and 3% (Flament et al., 1988; Reinherz, Giaconia, Lefkowitz, Pakiz, & Froast, 1993; Valleni-Basile et al., 1994; Zohar, 1999). This disorder has a severely negative impact on all aspects of a child's functioning including family relationships, school performance and social life (Piacentini, Bergman, Keller, & McCracken, 2003). Indeed, adults with a history of childhood OCD are less likely to be married/living with a partner, more prone to experience social/peer difficulties, isolation, unemployment, and to endure greater difficulties sustaining a job (Stewart et al., 2004). The prevalence and significant impairment caused by childhood OCD highlight the need to advance our understanding of the underlying mechanisms and determinants of these disorders. OCD is clinically characterised by two symptom dimensions: obsessions, which are unwanted, intrusive, recurrent and unpleasant
n Corresponding author at: School of Applied Psychology, Griffith University, Queensland 4222, Australia. Tel.: þ 61 7 3735 3434. E-mail address: a.waters@griffith.edu.au (A.M. Waters).
2211-3649/$ - see front matter & 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.jocrd.2013.12.004
thoughts that cause distress and are often concerned with contamination, checking or symmetry; and/or undesirable compulsions, which are repetitive behaviours carried out in relation to obsessions, including washing, household safety checking and object rearrangement (Diagnostic and Statistical Manual of Mental Disorders, Fifth Edition (DSM-5), American Psychiatric Association (APA), 2013). A growing body of neuropsychological research has emerged examining whether OCD is associated with cognitive impairments, and in particular, whether perseverative thoughts and behaviours which are symptomatic of the disorder may be due to deficits in inhibitory control of responses (Chamberlain, Blackwell, Fineberg, Robbins, & Sahakian, 2005). Inhibition refers to one's ability to suppress either irrelevant or interfering stimuli or behaviours (Garavan, Ross, & Stein, 1999). Several forms and measures of response inhibition have been studied including the Stroop task, the Stop-Signal Task and the Go/No Go task (Schachar et al., 2007). For example, in the Go/No Go task, participants respond to any letter (Go trials) but the letter ‘X’ to which they withhold a response (No Go trials) (e.g., Durston, Thomas, Worden, Yang, & Casey, 2002; Durston et al., 2002). The research on inhibition in adults with OCD is extensive. Whereas a number of studies have found that adults with OCD have dificulties withholding responses, resulting in increased commission errors
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(e.g., Bannon, Gonsalvez, Croft, & Boyce, 2006, 2002; Chamberlain, Fineberg, Blackwell, Robbins, & Sahakian, 2006; Enright & Beech, 1993; Hartston & Swerdlow, 1999; Kuelz, Hohagen, & Voderholzer, 2004; Penades et al., 2007), others have noted no differences in performance on these tests between adults with OCD compared to controls (Boone, Ananth, Philpott, Kaur, & Djenderjian, 1991; Rao, Reddy, Kumar, Kandavel, & Chandrashekar, 2008; Maltby, Tolin, Worhunsky, O’Keefe, & Kiehl, 2005; Bohne, Savage, Deckersbach, Keuthen, & Wilhelm, 2008; Page et al. 2009; see Abramovitch, Abramowitz, & Mittelman, 2013 for a review), while still others have indicated dificulties only when introducing additional cognitive demands such as reversing the Go/No-Go rules (Watkins et al., 2005). Such mixed results have contributed to the small effect size found for response inhibition deficits in OCD across studies indexing response inhibition in terms of commission errors (d¼ .33) (Abramovitch et al., 2013). The literature on response inhibition in paediatric OCD lags behind research with adults, yet the published studies to date suggest similar inconsistencies. Rosenberg et al. (1997) examined a range of cognitive functions in paediatric OCD, including the ability to suppress reflexive responses to external cues (e.g., a target light), volitionally execute delayed responses and anticipate predictable events. Results showed that children with OCD demonstrated more response suppression failures compared to controls. By contrast, two imaging studies reported no difference between children with OCD and controls in performance on switching and stop tasks (Rubia et al., 2010; Woolley et al., 2008). A similar discrepancy was found between studies examining performance on the Stroop test, where two studies reported impaired inhibitory performance on this task (Andres et al., 2007; Isik, Erdogan, & Oner, 2011), while others did not (Beers et al., 1999; Woolley et al., 2008; Ornstein, Arnold, Manassis, Mendlowitz, & Schachar, 2010; Chang, McCracken, & Piacentini, 2007). Moreover, statistical correction in one of these studies eliminated the group effects found on the Stroop task (Andres et al., 2007). Finally, from scanning studies (Gruner et al., 2012), higher functional anisotropy in the left dorsal cingulum bundle in children with OCD was correlated with better performance on two measures of response inhibition/cognitive control, even though children with OCD did not differ from healthy controls in behavioural performance on the Stroop task. Thus, functional abnormalities may serve a compensatory mechanism, allowing children with OCD to perform equivalently with controls when confronted with conflicting task requirements. A notable feature of almost all studies of response inhibition conducted to date with both adults and children with OCD it that they have employed emotionally neutral stimuli and tasks primarily taken from standardized neuropsychological test batteries. Yet OCD by definition is characterised by distress and impairment triggered by unpleasant and undesirable obsessional thoughts and compulsive behaviours (APA, 2013). Thus, studies that utilise emotional stimuli might extend upon previous research by determining whether or not response inhibition is a general neuropsychological deficit in paediatric OCD or deteriorates in response to emotionally negative stimuli. In a Go/No-Go task that used punishments or rewards to promote response activation or inhibition, Morein-Zamir et al. (2013) found that adults with OCD made more errors of commission on punishment trials than healthy controls. However, using a novel priming-based inhibitory task with threat and neutral words, Bannon. Gonsalvez, and Croft (2008) found that adults with OCD showed poorer inhibition for both neutral and threat words compared to controls and adults with panic disorder. Two studies with (non-OCD) anxious children have utilised an emotional Go/No Go task to assess response inhibition to emotional face stimuli and found that anxious youths were slower to respond to neutral face Go trials when angry face No Go trials were embedded amongst them (Ladouceur et al., 2006; Waters & Valvoi,
2009). These findings suggest that the aversive context created by angry faces interfered with the task of responding to neutral faces. However, there were no differences between anxious children and controls on the No Go trials, suggesting that (non-OCD) anxiety disorders are not associated with difficulties in withholding responses to emotional stimuli. To the authors' knowledge, there have been no studies published to date on response inhibition to emotional stimuli in children with OCD. However, if children with OCD have difficulty inhibiting responses (e.g., such as compulsive behaviours) following distressing thoughts and/or images for example (APA, 2013), then given that angry faces possess strong evolutionary threat value and good ecological validity (Waters, Mogg, Bradley & Pine, 2008), one hypothesis is that children with OCD will make more false presses (i.e., more commission errors) on angry face No Go trials compared to happy and neutral face No Go trials. On the other hand, the other anxiety disorders, as opposed to OCD, are known to be associated with enhanced responses to threat and feared stimuli as evidenced by differences in neural circuitry implicating the amygdala and related areas in imaging studies (see Waters, Farrell, & Schilpzand, 2013 for a review). However, in the absence of studies on inhibitory responding to emotional stimuli in paediatric OCD, it is unclear if this distinction also applies to response inhibition deficits which form one of a number of executive functions associated with frontal–striatal circuitry (Graybiel & Rauch, 2000; see Waters et al., 2013). Therefore, the present study examined whether paediatric OCD is associated with response inhibition deficits on emotional No Go trials compared to healthy control children. We hypothesised that children with OCD would make more errors of commission (i.e., more false presses) when angry face No-Go trials compared to happy face No-Go trials appeared amongst neutral Go trials. However, this would not be due to a speed-accuracy trade-off and as such, OCD children would not differ from healthy controls on reaction-time on false press trials. Moreover, if difficulties are specific to response inhibition and not response facilitation deficits to emotional stimuli, then children with OCD and controls were not expected to differ in reaction-time on angry versus happy Go trials, or in errors of commission to neutral face No-Go trials.
2. Method 2.1. Participants Participants included 27 children between 9 and 12 years of age; 12 children with a principal (i.e., most severe) diagnosis of OCD (6 girls; M Age¼9.2 years, SD ¼1.2) and 15 healthy control children (8 girls; M Age¼10.05; SD ¼1.1). Children were excluded if they had psychosis or an organic mental disorder or IQ suspected to be below 70, based on parent responses to screening items administered during an initial telephone screen. Children recruited for the control group were excluded if they met criteria for psychiatric diagnoses including anxiety disorders, depressive disorders, externalising disorders or developmental disorders. Children recruited for the OCD group were excluded if their likely diagnosis was a disorder other than OCD based on screening items administered during an initial telephone screen. Based on these criteria, all 12 consecutive referrals of children with OCD were retained in the final sample. For control children, the final 15 children were recruited from a sample of 22 children whose mother returned consent forms. Four children were excluded due to the presence of clinically significant anxiety and were referred elsewhere. A further two withdrew due to ongoing conflicting commitments and one child was excluded due to high rates of error responses on the emotional Go/No-Go task ( 450% of trials). The OCD sample had moderate-high OCD severity based on the Children's YaleBrown Obsessive-Compulsive Scale (CY-BOCS) (M¼ 20.18; SD ¼ 8.25) and the Clinician Severity Rating (CSR) for their principal OCD diagnosis derived from the Anxiety Disorders Interview Schedule for DSM-IV Parent Version (ADIS-IV-C/P) (M ¼ 5.91; SD ¼ 1.3). Eighty-three per cent of the OCD group had at least one comorbid diagnosis of either generalised anxiety disorder (n¼ 7), social phobia (n ¼3), or specific phobia (n¼ 2). One third of the children with OCD (n¼ 4) were stabilised on a Serotonergic medication (SSRI) at the time of assessment.
A.M. Waters, L.J. Farrell / Journal of Obsessive-Compulsive and Related Disorders 3 (2014) 65–70 The OCD group were treatment seeking, with parents responding to advertisements in local papers for a free CBT research programme at the university. Non-clinical children were recruited from a local primary school. The average Spence Children's Anxiety Scale—Parent Version (SCAS—P; Spence, 1998) total score for the latter group was in the non-clinical range (M¼ 12.34, SD¼ 6.14). Further, no children in the nonclinical group met criteria for any psychological disorder, based on the diagnostic interviews (using the ADIS-IV-C/P—see below). All children participated in an experimental protocol that was approved by the Institutional Human Research Ethics Committee and required parental written informed consent. 2.2. Materials Anxiety Disorders Interview Schedule for DSM-IV: Parent version (ADIS-IV-C/P, Silverman & Albano, 1996). The ADIS-P is a semi-structured clinical interview for the diagnosis of childhood anxiety disorders, depressive disorders, externalising disorders and screens for other childhood problems. A clinician severity rating (CSR) is given for each diagnosis where DSM-IV criteria is met on a 9-point scale of severity (0 ¼no interference to 8¼ severely disabling). The CSR rating that is the highest is deemed the principal diagnosis. In this study, the ADIS-IV-C/P was completed by parents of children in both groups. In order to ensure the reliability of the diagnoses, a postgraduate clinical psychology student who was blind to diagnoses reviewed 25% of the videotaped interviews, with results indicating excellent reliability (primary diagnosis κ ¼1.0; secondary diagnosis κ ¼0.84; tertiary diagnosis κ ¼ 0.83). The ADIS-IV-C/P has established sound psychometric properties, with excellent retest reliability for combined, parent and child ratings of anxiety disorders (Silverman, Saavedra, & Pina, 2001). Children's Yale-Brown Obsessive-Compulsive Scale (CY-BOCS: Scahill et al. 1997). The CY-BOCS is a clinician-rated, semi-structured interview, assessing the severity of OCD symptoms, which was administered to children in the OCD group. The CY-BOCS rates severity of obsessions and compulsions across five scales (frequency interference, distress, resistance, and degree of control over symptoms), and also provides a total severity score (range 0–40). The CY-BOCS has demonstrated reasonable reliability and validity, with good to excellent inter-rater agreement and high internal consistency for total score of.87 (Scahill et al. 1997). 2.2.1. Multidimensional Anxiety Scale for Children (MASC: March, 1997) The MASC is a 39-item, 4-point Likert self-report screen for anxiety symptoms in children and adolescents aged 8–19 years. The psychometric properties of the MASC, including the factor structure, reliability and validity have been found to be satisfactory (March, Parker, Sullivan, Stallings, & Conners, 1997). The MASC is routinely used in paediatric OCD outcome trials (Garcia et al. 2010; Barrett, HealyFarrell, & March, 2004) to assess co-occurring anxiety symptom severity. 2.2.2. Spence Children's Anxiety Scale (SCAS-P; Spence, 1998) The SCAS is a 44-item measure, developed for assessing dimensions of child anxiety disorders in community samples. The SCAS is composed of subscales assessing obsessions and compulsions, separation anxiety, social phobia, panic, agoraphobia, generalised anxiety, and physical injury concerns. Respondents rate the frequency with which they experience each of the symptoms on a 4-point scale, ranging from 0 (never) to 3 (always). The SCAS has been demonstrated to have acceptable psychometric properties (Spence, 1998) and was used to screen the nonclinical sample for anxiety symptoms prior to conducting the diagnostic interviews given it has well-established Australian normative data. 2.2.3. Children's Depression Inventory (CDI: Kovacs, 1992) The CDI is a 27-item child-report measure assessing depressive symptoms in children and adolescents aged 7–17 years. Each item of the CDI comprises three statements that are graded in severity and assigned numerical values with 0 (absence of symptom), 1 (mild symptoms) and 2 (definite symptom). The CDI is a widely used measure which possesses good psychometric properties (Kovacs, 1992). 2.2.4. The emotional Go/No Go task The task was programmed using DMDX and was presented on two identical Dell PCs with 17″ 75 Hz CRT colour monitors: one at the primary school and one in a research laboratory at Griffith University. Participants pressed the right shift key if a particular emotional face appeared on the screen (i.e., Go trials) and avoided pressing the key if any other facial expression was presented (i.e., No Go trials). Face stimuli consisted of full-colour angry, happy and neutral expressions from 12 adults of Caucasian appearance (6 females; 6 males) selected from the Nim Stim facial set (Research Network on Early Experience and Brain Development) and were sized to 506 650 pixels. The faces were not cropped and included a mix of open and closed mouth expressions in each emotional category. The task consisted of four blocks of 60 trials each in which 70% (i.e., 42) were Go trials and 30% (i.e., 18) were No Go trials. The following four blocks were presented: angry Go/neutral No Go; happy Go/neutral No Go; neutral Go/angry No Go; neutral Go/happy No Go. The presentation order of blocks and trials within each block was randomised across participants.
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2.3. Procedure 2.3.1. OCD group Upon contacting the university OCD Treatment Programme, parents interested in participating were given information about the Programme and they completed a semi-structured screening interview over the phone to determine whether OCD was a likely diagnosis and whether the inclusion and exclusionary criteria were met. Families of eligible children attended a face to face assessment session, whereby parents completed the ADIS-IV-C/P diagnostic interview. Comorbid internalising and externalising disorders were not exclusionary criteria so long as they were not the principal diagnosis. However, no children met criteria for these disorders as assessed using the ADIS-IV-C/P. Children completed the CY-BOCS concurrently with a separate interviewer. Child questionnaires and the emotional Go/No-Go task were completed with the interviewer, whilst parent questionnaires were completed at home.
2.3.2. Non-clinical group Following ethical approval from the university, Catholic Education, and the school principal, research information was disseminated to all children across Grades 4–7, including a brief flyer outlining the study, a research consent form, the SCAS-P and a reply paid envelope. The initial inclusion and exclusion criteria and the ADIS-IV-C/P (Silverman & Albano, 1996) were administered via the telephone with mothers of children who returned the written consent form to confirm that children met criteria for inclusion in the control group. Children who did not meet the criteria for any disorder on the ADIS-IV-C/P (N ¼ 16) completed the emotional Go/No Go task and SCAS-C individually in a resource room at the primary school while being supervised by a research assistant. This was done within a week of the phone call to mothers.
2.3.3. Emotional Go/No Go task At the commencement of the emotional Go/No Go task, the research assistant read aloud written instructions presented on the computer screen. These informed participants that when a particular face appeared on the screen (i.e., happy, angry or neutral), they were to press the response key when they saw that face (i.e., Go trials) and avoid pressing if they saw any other face (i.e., No Go trials). Participants received new instructions read aloud and presented on the screen at the start of each block. Each trial consisted of a centred black fixation cross for 1500 ms set against a grey background. Next, a face was presented for 500 ms centred on the screen and offset with the child's response or after 2000 ms. Then the fixation cross appeared for between 1250 and 1750 ms heralding the next trial. Children completed 10 practice trials before the task, including trials from all conditions. Reaction-time on Go trials and number and speed of false presses on No Go trials were recorded. The research assistant then read aloud the items from the SCAS-C and recorded children's answers verbatim to avoid variation in reading ability affecting responses.
2.3.4. Response definitions, data screening and statistical analyses Reaction-time on Go trials was recorded in milliseconds and inspected for outliers (i.e., o 100 ms or 4 1000 ms), consistent with Waters and Valvoi (2009) and Ladouceur et al. (2006). Errors of omission on Go trials, defined as failing to press the response key, were recorded throughout the task. There were no significant group differences in outliers (1.4% of trials) or errors of omission (2.6%). The number of false presses on No Go trials, and the associated reactiontimes in milliseconds were also recorded. False press reaction-times were also inspected for outliers and no group differences observed (1.1% of trials). Reaction-time on correct Go trials and the number of false presses on No Go trials as well as the associated RT were examined separately, consistent with Waters and Valvoi (2009) and Ladouceur et al. (2006). When the emotional faces were the Go trials, a 2 Face Type (angry Go/neutral No Go; happy Go/neutral No Go) 2 Group (control; OCD) mixed factorial analysis of variance (ANOVA) was conducted for reaction-time on Go trials, and number of, and reaction-time for, false presses on No Go trials. Similarly, when the emotional faces were the No Go trials, reaction-time to the neutral face Go trials with angry and happy face No Go trials embedded amongst them, the number of, and reaction-time for, false presses for angry and happy face No Go trials were analysed using a 2 Face Type (neutral Go/angry No Go; neutral Go/happy No Go) 2 Group (control; anxious) mixed factorial ANOVA. Additional analyses including children's age and gender revealed no significant effects and are not reported further. The multivariate test reported for all analyses is Wilks' lambda. Significant effects were followed up with comparisons using Bonferroni corrections. All analyses were evaluated against the .05 alpha level. Partial eta-squared (ɳ2) was used as a measure of effect size.
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were not significant, F'so.68. There were no significant effects for the false press reaction-time data, all F'so4.00, n.s.
3. Results 3.1. Group characteristics The OCD group had scores within the moderate-severe range on the C-YBOCS (M¼21.4; SD ¼8.9) and the MASC (M ¼60.5; SD ¼19.9). Children in the control group had total scores on the SCAS-P (M¼17.6; SD ¼11.6) and the SCAS-C (M¼19.7; SD ¼8.2) that were within the non-clinical range on these measures (see Section 2.2). Groups did not differ significantly on CDI t-scores (OCD M ¼48.3; SD ¼10.2; Control M¼45.8; SD¼ 6.8), t(25) ¼.77, p ¼.44.There were no significant differences between groups in child gender, parental marital status or socioeconomic status based on annual income, all χ2 o2.7, n.s. 3.2. Performance when emotional faces were Go trials and neutral faces were No Go trials 3.2.1. Reaction-time to emotional face Go trials The 2 (Group) 2 (Face Emotion) ANOVA of children's reactiontime to happy and angry Go trials revealed no significant differences, all F's o1.9 (angry Go/neutral No-Go: OCD M ¼557, SD ¼ 125; Control M ¼568, SD ¼154; happy Go/neutral No-Go: OCD M¼ 517, SD¼ 86; Control M ¼573, SD¼ 144).
Mean number of false presses
3.2.2. False presses on neutral face No-Go trials The 2 (Group) 2 (Face Emotion) ANOVA of false presses for neutral No-Go trials embedded amongst either happy or angry Go trials revealed a significant main effect of Group, F(1, 25)¼8.03, p¼ .009, ɳ2 ¼.24. As shown in Fig. 1, children with OCD had significantly greater difficulty inhibiting a response to neutral faces when embedded amongst emotional Go trials compared to control children. The Face Emotion main effect and Face Emotion Group interaction 12
3.3.1. Reaction-time to neutral face Go trials The 2 (Group) 2 (Face Emotion) ANOVA of children's reactiontime to neutral Go trials embedded amongst angry and happy face No-Go trials revealed no significant differences, all F's o.35 (neutral Go/angry No-Go: OCD M¼554, SD ¼ 133; Control M ¼539, SD¼ 109; neutral Go/happy No-Go: OCD M ¼517, SD¼ 85; Control M¼530, SD ¼83). 3.3.2. False presses on emotional face No-Go trials The 2 (Group) 2 (Face Emotion) ANOVA of false presses for angry and happy No-Go trials embedded amongst neutral Go trials revealed a significant main effect of Group, F(1, 25) ¼9.37, p ¼.005, ɳ2 ¼.27. As shown in Fig. 1, children with OCD had significantly greater difficulty inhibiting a response to emotional faces in general compared to control children. The Face Emotion main effect and Face Emotion Group interaction were not significant, F'so.55, n.s. For false press reaction-times to emotional face NoGo trials, there was a significant Face Emotion main effect, F(1, 25)¼ 4.46, p ¼.045, ɳ2 ¼.16, but no other significant effects, F'so2.1, n.s. This reflected shorter reaction-times on false presses to angry compared to happy No-Go trials (neutral Go/angry NoGo: OCD M¼ 464, SD ¼69; Control M¼ 546, SD ¼152; neutral Go/ happy No-Go: OCD M ¼505, SD ¼114; Control M¼ 620, SD ¼232).1 3.4. Supplementary analyses There were no significant correlations between children's reaction-time data on Go trials or false press data on No Go trials and symptom severity scores on either the C-YBOCS, the MASC, or the SCAS-P (all r'so .5).
10 8
4. Discussion
6 4 2 0 Happy No Go/Neutral Go
Angry No Go/Neutral Go
Control
Mean number of false presses
3.3. Performance when neutral faces were Go trials and emotional faces were No Go trials
Happy No Go/Neutral Go
Angry No Go/Neutral Go
OCD
12 10 8 6 4 2 0 Neutral No Go/Angry Go
Neutral No Go/Happy Go
Control
Neutral No Go/Happy Go
Neutral No Go/Angry Go
OCD
Fig. 1. Mean number of false presses for happy and angry face No Go trials (upper panel) and neutral face No Go trials (lower panel) as a function of group.
The present study examined whether children with OCD committed more errors of commission when responding to threatening stimuli to which they were required to inhibit a response compared to emotionally positive stimuli and relative to healthy control children. We expected that group differences would not be due to a speedaccuracy trade-off in children with OCD. Moreover, it was hypothesised that group differences would be specific to response inhibition difficulties on No Go trials, in that the groups were not expected to differ significantly in response facilitation on Go trials. Partial support was found for the hypotheses in that children with OCD made significantly more errors of commission on No Go trials compared to controls. However, this was not specific to threat No Go trials, but rather, was observed across all facial expressions. Additional analyses confirmed that results did not simply reflect on a speed-accuracy trade-off in children with OCD. Moreover, consistent with hypotheses, no group differences were observed in response facilitation on Go trials. Findings on No Go trials are consistent with some prior studies that have found deficits in response inhibition in adults and children with OCD compared to healthy controls (Bannon et al., 2002, 2006; 1 Additional analyses to examine speed-accuracy trade-offs were computed using the formula: [(accuracy/reaction-time) 100] for each condition. However, the ANOVA using these data revealed identical effects as the false press reactiontime data. The reaction time data are presented to allow comparisons with previous studies (Waters & Valvoi, 2009).
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Chamberlain et al., 2006; Enright & Beech, 1993; Hartston & Swerdlow, 1999; Kuelz et al., 2004; Penades et al., 2007; MoreinZamir et al., 2013; Rosenberg et al., 1997; Andres et al., 2007; Isik et al., 2011). However, findings are not consistent with other studies that have failed to find significant group differences (Beers et al., 1999; Woolley et al., 2008; Ornstein et al., 2010; Chang et al., 2007). The mechanisms underlying such variation in results are unclear. However, methodological differences across studies are likely to contribute to the inconsistencies. Small sample sizes of children across a wide age range have typically been assessed in studies utilising comprehensive test batteries that result in a large number of dependent variables in which statistical correction to avoid inflation of type-1 errors has rarely been employed (see Abramovitch, Mittelman, Henin, & Geller, 2012). However, prior paediatric studies (i.e., Ladouceur et al., 2006; Waters & Valvoi, 2009) of non-OCD anxiety and depressive disorders using the emotional Go/No-Go task, as used in the present study, found no significant group differences on No-Go trials. Conversely, those studies found significant group differences on Go trials that were not observed in the present study. One might argue that because neutral No Go trials were always embedded amongst angry and happy face Go trials, and children were required to either respond or inhibit a response based on the emotional valence of faces in this task, that the requirement for response inhibition always occurred in an emotional context. Although a completely neutral condition was not included in the present task which would have provided a more accurate assessment of response inhibition deficits independent of stimulus valence, the fact that children with OCD committed more false press errors on happy and angry No Go trials and on neutral face No Go trials embedded in happy and angry face Go trials suggests that deficits in response inhibition were not threat-specific. Thus, the present results may be interpreted as consistent with some previous research that has documented broader response inhibition deficits in paediatric OCD (e.g., Rosenberg et al., 1997; Andres et al., 2007; Isik et al., 2011). Moreover, they are consistent with some findings from adult studies using a novel priming-based task with threat and neutral words in which adults with OCD showed poorer inhibition to both neutral and threat words compared to controls and adults with panic disorder (Bannon et al., 2008). Taken together, evidence across Go and No Go trials from the present study relative to prior studies is consistent with distinctions between other anxiety disorders and OCD in terms of links between enhanced reactivity to threat and feared stimuli and amygdala reactivity in other (non-OCD) anxiety disorder, and possibly response inhibition deficits and frontal–striatal circuitry in OCD (Graybiel & Rauch, 2000). Further studies that examine underlying neural circuitry of children with other anxiety disorders, OCD and controls while performing an emotional Go/No Go task would help elucidate the nature of these distinctions. No significant correlations were observed between response inhibition or facilitation measures and symptom severity. Previous findings regarding these associations have been inconsistent. One study with adults reported an association between higher selfreported OCD symptoms with increased punishment-related commission errors (Morein-Zamir et al., 2013). However, another study found no significant associations between OCD symptom measures and inhibition effects to threat and neutral words (Bannon et al., 2008). Moreover, Bannon et al. (2008) reported that both symptomatic OCD and remitted OCD groups equally displayed poorer inhibition of threat and neutral words which, together with a lack of significant correlation effects, were interpreted as suggesting that inhibitory differences may be related to diagnosis rather than to symptomatic status. Nevertheless, given the paucity of evidence in relation to these associations, these conclusions are preliminary at this stage. Additional studies comparing children with OCD and other anxiety and depressive disorders would be useful in addressing common and specific neuropsychological factors associated with
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these disorders. Moreover, the Go/No-Go task involves responding to stimuli presented one at a time and thus, does not require selective orientation of attention between simultaneously presented stimuli. This format of the Go/No-Go task also asked children to respond on the basis of the emotional valence of the face, rather than based on an emotionally neutral characteristic such as gender or hair colour. Therefore, additional studies that attend to these methodological differences will be important for delineating the parameters of children's biases as a function of OCD and other emotional disorders. Although these results are encouraging in that they may help to isolate mechanisms underlying the expression of OCD in children, the study had several limitations. The sample sizes were small which limits generalisability and specificity to OCD children with differing types of compulsive behaviour and symptom severity. Also, an anxious (non-OCD) control group was not included. Although previous research found no group effects on No-Go trials in anxious (non-OCD) children compared to controls (i.e., Waters & Valvoi, 2009), future research would be strengthened by the inclusion of this group. Also, the study was cross-sectional in nature and does not elucidate whether response inhibition processes play a contributing role to disorder development. Longitudinal studies are required in that regard. Also, methodological features could be addressed in future research, such as the inclusion of an emotionally neutral condition, response requirements based on non-emotional facial characteristics, and also varying the probability of Go versus No-Go trials to determine if response inhibition differences intensify with increasing inhibitory demand. Nevertheless, the present findings have clinical implications. A general difficulty with inhibiting responses to a wide range of stimuli might in part contribute to the way in which emotionally benign behaviours such as repeating routine tasks, ordering, counting, and symmetry become compulsive behaviours in children with OCD. Given that response prevention is a major component of cognitive-behavioural therapy for childhood OCD (Farrell, Waters, Milliner, & Ollendick, 2012), encouraging the inhibition of responses to a wide variety of stimuli in addition to anxiety-provoking triggers could be important in terms of offsetting relapse and preventing generalisation. On the other hand, these findings are preliminary and based on a small sample size. Therefore, it is possible that the present findings and the task used to assess response inhibition may not be important for understanding the development and treatment of childhood OCD. Additional, larger-scale studies are required. In summary, the present study found that children with OCD made significantly more false presses for face stimuli when instructed to inhibit responding compared to controls. This finding is consistent with some adult and paediatric OCD studies and suggests children with OCD have difficulty inhibiting responses to a broad range of stimuli. Future studies should investigate response inhibition differences in children with OCD versus other anxiety disorders and healthy controls as well as the underlying neural circuitry to determine the extent to which inhibitory deficits are unique to paediatric OCD. Acknowledgements The authors declare no conflicts of interest. Thanks are due to Lisa Kokkoris and Donna Hourigan for assistance with data collection. References Abramovitch, A., Mittelman, A., Henin, A., & Geller, D. (2012). Neuroimaging and neuropsychological findings in pediatric obsessive-compulsive disorder: A review and developmental considerations. Neuropsychiatry, 2, 313–329. Abramovitch, A., Abramowitz, J. S., & Mittelman, A. (2013). The neuropsychology of adult obsessive-compulsive disorder. Clinical Psychology Review, 33, 1163–1171. American Psychiatric Association (2013). Diagnostic and statistical manual from DSM-IV. Washington, DC: American Psychiatric Association.
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Andres, S., Boget, T., Lazaro, L., Penades, A., Morer, A., Salamero, M., et al. (2007). Neuropsychological performance in children and adolescents with obsessivecompulsive disorder and influence of clinical variables. Biological Psychiatry, 61, 946–951. Bannon, S., Gonsalvez, C. J., Croft, R. J., & Boyce, P. M. (2002). Response inhibition deficits in obsessive-compulsive disorder. Psychiatry Research, 110, 165–174. Bannon, S., Gonsalvez, C. J., Croft, R. J., & Boyce, P. M. (2006). Executive functions in obsessive-compulsive disorder: State or trait deficits? Australian and New Zealand Journal of Psychiatry, 40, 1031–1038. Bannon, S., Gonsalvez, C. J., & Croft, R. J. (2008). Processing impairments in OCD: Is it more than inhibition! Behaviour Research and Therapy, 46, 689–700. Barrett, P., Healy-Farrell, L., & March, J. S. (2004). Cognitive-behavioral family treatment of childhood obsessive-compulsive disorder: A controlled trial. Journal of the American Academy of Child & Adolescent Psychiatry, 43, 46–62. Beers, S. R., Rosenberg, D. R., Dick, E. L., Williams, T., O’Hearn, K. M., Birmaher, B., et al. (1999). Neuropsychological study of frontal lobe function in psychotropicnaive children with obsessive-compulsive disorder. American Journal of Psychiatry, 156, 777–779. Bohne, A., Savage, C. R., Deckersbach, T., Keuthen, N. J., & Wilhelm, S. (2008). Motor inhibition in trichotillomania and obsessive-compulsive compulsive disorder. Journal of Psychiatric Research, 42, 141–150. Boone, K. B., Ananth, J., Philpott, L., Kaur, A., & Djenderjian, A. (1991). Neuropsychological characteristics of non-depressed adults with obsessive-compulsive disorder. Neuropsychiatry, Neuropsychology, and Behavioral Neurology, 4, 96–109. Chamberlain, S. R., Blackwell, A. D., Fineberg, N. A., Robbins, T. W., & Sahakian, B. J. (2005). The neuropsychology of obsessive compulsive disorder: The importance of failures in cognitive and behavioural inhibition as candidate endophenotypic markers. Neuroscience & Biobehavioral Reviews, 29, 399–419. Chamberlain, S. R., Fineberg, N., Blackwell, A., Robbins, T., & Sahakian, B. (2006). Motor inhibition and cognitive flexibility in obsessive-compulsive disorder and trichotillomania. American Journal of Psychiatry, 163, 1282–1284. Chang, S. W., McCracken, J. T., & Piacentini, J. C. (2007). Neurocognitive correlates of child obsessive compulsive disorder and Tourette syndrome. Journal of Clinical and Experimental Neuropsychology, 29, 724–733. Durston, S., Thomas, K. M., Worden, M. S., Yang, Y., & Casey, B. J. (2002). The effect of preceding context on inhibition: An event-related fMRI study. NeuroImage, 16, 449–453. Durston, S., Thomas, K. M., Yang, Y., Ulug, A. M., Zimmerman, R. D., & Casey, B. J. (2002). A neural basis for the development of inhibitory control. Developmental Science, 5, F9–F16. Enright, S. J., & Beech, A. R. (1993). Further evidence of reduced cognitive inhibition in obsessive-compulsive disorder. Personality and Individual Differences, 14, 387–395. Farrell, L. J., Waters, A. M., Milliner, E., & Ollendick, T. (2012). Comorbidity and treatment response in paediatric OCD: Outcomes of group cognitive behavioural therapy. Psychiatry Research, 199, 115–123. Flament, M. F., Rapoport, J. L., Whitaker, A., Davies, M., Kalikow, K., & Shaffer, D. (1988). Obsessive-compulsive disorder in adolescence: An epidemiological study. Journal of the American Academy of Child & Adolescent Psychiatry, 27, 764–771. Garavan, H., Ross, T. J., & Stein, E. A. (1999). Right hemispheric dominance of inhibitory control: An event-related functional MRI study. Proceedings of the National Academy of Sciences, 96, 8301–8306. Garcia, A. M., Sapyta, J. J., Moore, P. S., Freeman, J. B., Franklin, M. E., March, J. S., et al. (2010). Predictors and moderators of treatment outcome in the Pediatric Obsessive Compulsive Treatment Study (POTS I). Journal of the American Academy of Child & Adolescent Psychiatry, 49, 1024–1033. Graybiel, A. M., & Rauch, S. L. (2000). Toward a neurobiology of obsessivecompulsive disorder. Neuron, 28, 343–347. Gruner, P., Vo, A., Ikuta, T., Mahon, K., Peters, B. D., Malhotra, A. K., et al. (2012). White matter abnormalities in pediatric obsessive-compulsive disorder. Neuropsychopharmacology, 37, 2730–2739. Hartston, H. J., & Swerdlow, N. R. (1999). Visuospatial priming and stroop performance in patients with obsessive compulsive disorder. Neuropsychology, 13, 447. Isik, T. Y., Erdogan, B. E., & Oner, O. (2011). Impaired executive functions in paediatric obsessive-compulsive disorder patients. Acta Neuropsychiatrica, 23, 272–281. Kovacs, M. (1992). Children's depression inventory. Multi-Health Systems, Incorporated. Kuelz, A. K., Hohagen, F., & Voderholzer, U. (2004). Neuropsychological performance in obsessive-compulsive disorder: A critical review. Biological Psychology, 65, 185–236. Ladouceur, C. D., Dahl, R. E., Williamson, D. E., Birmaher, B., Axelson, D. A., Ryan, N. D., et al. (2006). Processing emotional facial expressions influences performance on a Go/No Go task in pediatric anxiety and depression. Journal of Child Psychology and Psychiatry, 47, 1107–1115. Maltby, N., Tolin, D. F., Worhunsky, P., O'Keefe, T. M., & Kiehl, K. A. (2005). Dysfunctional action monitoring hyperactivates frontal–striatal circuits in obsessive–compulsive disorder: An event-related fMRI study. NeuroImage, 24, 495–503. March, J. S., Parker, J. D., Sullivan, K., Stallings, P., & Conners, C. K. (1997). The Multidimensional Anxiety Scale for Children (MASC): Factor structure,
reliability, and validity. Journal of the American Academy of Child & Adolescent Psychiatry, 36, 554–565. Morein-Zamir, S., Papmeyer, M., Gillan, C. M., Crockett, M. J., Fineberg, N. A., Sahakian, B. J., et al. (2013). Punishment promotes response control deficits in obsessive-compulsive disorder: Evidence from a motivational Go/No-Go task. Psychological Medicine, 43, 391–400. Ornstein, T. J., Arnold, P., Manassis, K., Mendlowitz, S., & Schachar, R. (2010). Neuropsychological performance in childhood OCD: A preliminary study. Depression & Anxiety, 27, 372–380. Page, L. A., Rubia, K., Deeley, Q., Daly, E., Toal, F., Mataix-Cols, D., et al. (2009). A functional magnetic resonance imaging study of inhibitory control in obsessive-compulsive disorder. Psychiatry Research: Neuroimaging, 174, 202–209. Penades, R., Catalan, R., Rubia, K., Andres, S., Salamero, M., & Gasto, C. (2007). Impaired response inhibition in obsessive compulsive disorder. European Psychiatry, 22, 404–410. Piacentini, J., Bergman, R. L., Keller, M., & McCracken, J. (2003). Functional impairment in children and adolescents with obsessive-compulsive disorder. Journal of Child and Adolescent Psychopharmacology, 13, 61–69. Rao, N. P., Reddy, Y. C., Kumar, K. J., Kandavel, T., & Chandrashekar, C. R. (2008). Are neuropsychological deficits trait markers in OCD? Progress in Neuropsychopharmacological and Biological Psychiatry, 32, 1574–1579. Reinherz, H. Z., Giaconia, R. M., Lefkowitz, E. S., Pakiz, B., & Froast, A. K. (1993). Prevalence of psychiatric disorders in a community population of older adolescents. Journal of the American Academy of Child & Adolescent Psychiatry, 32, 369–377. Research Network on Early Experience and Brain Development. Available from: 〈http://www.macbrain.org〉. Rosenberg, D. R., Averbach, D. H., O’Hearn, K. M., Seymour, A. B., Birmaher, B., & Sweeney, J. A. (1997). Oculomotor response inhibition abnormalities in pediatric obsessive-compulsive disorder. Archives of General Psychiatry, 54, 831–838. Rubia, K., Cubillo, A., Smith, A. B., Woolley, J., Heyman, I., & Brammer, M. J. (2010). Disorder-specific dysfunction in right inferior prefrontal cortex during two inhibition tasks in boys with attention-deficit hyperactivity disorder compared with boys with obsessive-compulsive disorder. Human Brain Mapping, 31, 287–299. Scahill, L., Riddle, M. A., Swiggin-Hardin, M., Ort, S. I., King, R. A., Goodman, W. K., et al. (1997). Children's Yale-Brown Obsessive Compulsive Scale: Reliability and validity. Journal of the American Academy of Child & Adolescent Psychiatry, 36, 844–852. Schachar, R., Logan, G. D., Robaey, P., Chen, S., Ickowicz, A., & Barr, C. (2007). Restraint and cancellation: Multiple inhibition deficits in attention deficit hyperactivity disorder. Journal of Abnormal Child Psychology, 35, 229–238. Spence, S. H. (1998). A measure of anxiety symptoms among children. Behaviour Research and Therapy, 36, 545–566. Silverman, W., & Albano, A. M. (1996). The anxiety disorders interview schedule for children (DSM-IV). San Antonio: Psychological Corporation. Silverman, W. K., Saavedra, L. M., & Pina, A. A. (2001). Test-retest reliability of anxiety symptoms and diagnoses with the Anxiety Disorders Interview Schedule for DSM-IV: Child and parent versions. Journal of American Academy of Child & Adolescent Psychiatry, 40, 937–944. Stewart, S. E., Geller, D. A., Jenike, M., Pauls, D., Shaw, D., Mullin, B., et al. (2004). Long‐term outcome of pediatric obsessive-compulsive disorder: A metaanalysis and qualitative review of the literature. Acta Psychiatrica Scandinavica, 110(1), 4–13. Valleni-Basile, L. A., Garroson, C. Z., Jackson, K. L., Waller, J. L., McKeown, R. E., Addey, C. L., et al. (1994). Frequency of obsessive-compulsive disorder in a community sample of young adolescents. Journal of American Academy of Child & Adolescent Psychiatry, 33, 782–791. Waters, A. M., Mogg, K., Bradley, B. P., & Pine, D. S. (2008). Attentional bias for emotional faces in children with generalised anxiety disorder. Journal of the American Academy of Child & Adolescent Psychiatry, 47, 435–442. Waters, A. M., & Valvoi, J. S. (2009). Attentional bias for emotional faces in paediatric anxiety disorders: An investigation using the emotional Go/No Go task. Journal of Behavior Therapy and Experimental Psychiatry, 40, 306–316. Waters, A. M., Farrell, L. J., & Schilpzand, E. (2013). Neuropsychological assessment and clinical intervention for youth with anxiety disorders. In: L. A. Reddy, A. Weissman., & J. B. Hale (Eds.), Neuropsychological assessment and intervention for youth: An evidence-based approach to emotional and behavioral disorders (pp. 13–40). Washington DC: American Psychological Association Press. Watkins, L. H., Sahakian, B. J., Robertson, M. M., Veale, D. M., Rogers, R. D., Pickard, K. M., et al. (2005). Executive function in Tourette's syndrome and obsessivecompulsive disorder. Psychological Medicine, 35(4), 571–582. Woolley, J., Heyman, I., Brammer, M., Frampton, I., McGuire, P. K., & Rubia, K. (2008). Brain activation in paediatric obsessive compulsive disorder during tasks of inhibitory control. British Journal of Psychiatry, 192, 25–31. Zohar, A. H. (1999). The epidemiology of obsessive-compulsive disorder in children and adolescents. Child and Adolescent Psychiatric Clinics of North America, 8, 445–460.