Abstract
Pavlovian-to-instrumental transfer (PIT) refers to the effect of stimuli that have been associated with a pleasant or aversive event on instrumental behaviors. Given that obsessive–compulsive disorder (OCD) is linked to excessive compulsions, which in the laboratory can be tested via testing instrumental responses, we assessed PIT effects in individuals with subclinical levels of OCD. Participants from a nonclinical population were separated in groups with low (OC−) and high (OC+) levels of OCD. Participants learned to associate one button press (
Obsessive–compulsive disorder (OCD) is a chronic psychiatric disorder that is mainly characterized by persistent obsessions and compulsions (American Psychiatric Association, 2013). Briefly, obsessions are recurrent, persistent thoughts, and intrusive urges, or images, whereas compulsions are repetitive behaviors or mental acts that the individuals perform driven by an obsession or due to the rules that the individual wants to adhere to. The prevalence of OCD ranges from 0.7% to 3.5% (Gustavsson et al., 2011; Kessler et al., 2005; Ruscio et al., 2010). OCD is accompanied by significant impairments in daily functioning (e.g., loss in productivity), as well as substantial direct and indirect costs (American Psychiatric Association, 2013; Angst et al., 2004). Given the significant negative impact of OCD on individuals and society, a body of literature has focused on unveiling the factors that contribute to OCD psychogenesis (Pauls et al., 2014). Importantly, this knowledge could prove invaluable in the improvement of current treatments (Ost et al., 2015; Romanelli et al., 2014).
A way to gain insight into the nature of OCD is by using
To illustrate, Leplow et al. (2002) showed that when neutral CSs are used, inpatients with OCD show inferior differential learning compared to controls, which could suggest associative learning impairments in OCD. This hypothesis is also supported by findings of Apergis-Schoute et al. (2017), who showed that OCD patients failed to update the contingencies between the CS+/CS− and the US when those were reversed. In
Because maladaptive actions (compulsions) are a key component of OCD, further knowledge on the conditions under which these actions emerge could be useful in understanding OCD pathogenesis (Pauls et al., 2014). In this endeavor, insights from the learning and neuroscience literature could be useful. For instance, it has been suggested that instrumental responses toward a CS can be evoked even when the CS has never been explicitly trained with the specific instrumental behavior (Estes, 1948; Holmes et al., 2010; Kruse et al., 1983). This is the case of Pavlovian-to-instrumental transfer (PIT). Experimental findings show that animals and humans tend to perform the instrumental response more often during the CS presentation, relative to some control condition (e.g., a second control CS), although this behavioral response has never been explicitly paired with the CS (Holland, 2004). A PIT procedure typically entails three phases: Pavlovian, instrumental, and transfer. In the instrumental phase, participants receive rewarding stimuli (e.g., monetary rewards) when they perform an experimenter-defined response (e.g., press a button). In the Pavlovian phase, neutral stimuli (e.g., pictures; CSs) are paired with either the same rewarding stimuli as in the instrumental phase (i.e., in case of
Experimental findings show that human and nonhuman animals tend to perform the instrumental response, although this behavioral response has never been explicitly paired with the CS (Holland, 2004). PIT effects have been extensively studied in the addiction literature (Everitt et al., 2001). Specifically, it has been argued that PIT effects show how actions (e.g., smoking) can be triggered by environmental cues (e.g., a pack of cigarettes) that have been previously paired with a positive outcome (e.g., relaxation; Childress et al., 1992; Gawin, 1991), an observation that is particularly relevant when testing relapse in addiction. Although PIT has been used for addressing approach behavior, there is little work on human avoidance PIT (e.g., Claes et al., 2016; Garofalo and Robbins, 2017; Lewis et al., 2013; Nadler et al., 2011). Importantly, PIT effects have been investigated in many other mental disorders such as schizophrenia (Morris et al., 2015), alcohol abuse (Garbusow et al., 2014; Schad et al., 2018), and have been associated with stress and anxiety levels in subclinical populations (Charpentier et al., 2015; Quail et al., 2017). Studying PIT effects could be relevant for disorders such as OCD. Specifically, it can be hypothesized that instrumental responses (e.g., excessive checking) performed in the presence of largely neutral stimuli (e.g., a gas stove that is turned off) can be triggered without any previous
In this line, this study explored avoidance-based PIT in individuals with high and low levels of subclinical OCD symptomatology. As there are various subtypes of OCD (American Psychiatric Association, 2000, 2013), we chose to focus on checking behavior, which is the most prevalent type (Ruscio et al., 2010). 1 Accordingly, we developed a new task based on the avoidance-based human PIT introduced by Lewis et al. (2013) and Nadler et al. (2011) and the checking behavior task introduced by van den Hout and Kindt (2004). Specifically, in the first part of the task, participants learned to avoid two negative outcomes (i.e., a video of a house collapsing and a video of a house exploding) by means of two different button presses (i.e., one button cancelled the first outcome, whereas another button cancelled the second outcome). Then, different colors of stoves were presented with either the outcome they saw before, a novel negative outcome (i.e., a video of a house on fire), or two neutral outcomes (i.e., different symbols). Participants did not have to emit any response during this phase. In the last phase, the different stoves were presented and none of them were followed by any of the outcomes (i.e., the videos of the different houses or the different symbols) while participants were free to press any of the available buttons used in the first part of the task.
Because this is the first study on PIT effects in subclinical OCD, we did not have strong directorial hypotheses. However, we can predict that if excessive instrumental behavior toward a CS would characterize OCD, then individuals with higher levels of subclinical OCD symptomatology would exhibit higher levels of specific PIT, as indicated by elevated specific responses during the transfer phase toward the stimulus that was predictive of the same outcome, than participants with lower levels of subclinical OCD symptomatology. Conversely, if individuals with higher levels of subclinical OCD would not be able to discriminate between different Pavlovian cues due to high stress levels (see Quail et al., 2017), could explain the absence of a specific PIT effect in these individuals. This prediction is in line with studies showing nondiscriminatory learning in cases of high stress and anxiety (e.g., Charpentier et al., 2015) that also characterize OCD.
Apart from specific PIT effects, we explored the differences on general PIT by testing whether responses toward the stimulus that was previously paired with the novel negative outcome would be higher compared to responses to the two neutral outcomes.
Method
Participants
Similar to previous studies in our lab (e.g., Toffolo et al., 2013), we decided to recruit individuals with high and low levels of subclinical OCD. A total of 426 students at Utrecht University or Utrecht Hogeschool were screened for obsessive–compulsive symptomatology using the Obsessive–Compulsive Inventory–Revised (OCI-R) (Foa et al., 2002).
Participants could fill in the questionnaire online, using the University website and their log in information, or on paper during a break in a class. This questionnaire has been used to select individuals with subclinical levels of OCD in previous studies (e.g., Toffolo et al., 2013). To create two extreme groups, we invited 60 individuals to the laboratory session, using the top and bottom 12.5% of the checking subscale distributions scores as an a priori cutoff (i.e., participants with the 26 lowest and 34 highest scores were invited to participate in our study). The 12.5% is half the percentage that was used by Toffolo et al. (2013). We used more extreme cutoff scores for the OCI-R scale in order to maximize our chances of detecting an effect, if there was one. Only these 60 participants completed the behavioral task.
The data from 12 participants (6 in each group) were removed because they did not report the Pavlovian or the instrumental contingencies correctly (see “Procedure” section). The final sample consisted of 20 participants in the OC− group and 28 participants in the OC+ group. This sample allowed us to detect an effect size of
Material
Questionnaires
We screened participants for obsessive–compulsive tendencies using the OCI-R (Foa et al., 2002; Dutch version by Cordova-Middelbrink et al., 2007). The inventory includes 18 items and is designed to assess checking, hoarding, neutralizing, obsessing, ordering, and washing. Participants are asked to respond using a 5-point Likert-type scale (i.e., 0 =
We also assessed state and trait anxiety by means of the State and Trait Anxiety Inventory (STAI-S and STAI-T, respectively; Spielberger & Gorsuch, 1983; Dutch version by van der Ploeg, 2000). Each portion of the STAI consists of 20 items scored on a 4-point scale (1 =
Procedure
Preparation
Prior to the main experiment, all participants read the information letter and signed the consent form. Then, they filled in the state portion of STAI. After that, the PIT paradigm followed, which consisted of three phases: instrumental, Pavlovian, and transfer (see Table 1).
Schematic of the experimental design for the PIT study.
Instrumental phase
Participants received on-screen and verbal instructions about the
Although participants could press any button as often as they wanted, pressing both buttons within each trial would not prevent the outcome presentation. A single button press to the correct button was needed to prevent the outcome from being presented.
Figure 1 shows a visual depiction of the trial sequence. Each instrumental trial started with a picture of a building for 3,000 ms. Participants were allowed to press any button during this period. In case of no or a wrong response, the outcome would be presented for 2,000 ms. In case of a correct response, there was no presentation of the outcome but the picture was presented for the remaining 2,000 ms. Participants completed 24 instrumental trials, 12 trials for each

Experimental design. Top panel: trial sequence during the instrumental phase. Middle panel: trial sequence during the Pavlovian phase. Bottom panel: trial sequence during the transfer phase.
After the instrumental phase, the learned
Pavlovian phase
The Pavlovian phase consisted of the presentation of five different stoves (
Figure 1 shows a visual depiction of the trial sequence. Each Pavlovian trial started with a pretrial interval of 2,000–6,000 ms (steps of 1,000 ms). Then one of the stoves appeared. Gradually virtual fire appeared from four places of the stove.
2
After 2,550 ms, the outcome was presented for 1,000 ms. Which stove served as
At the end of the Pavlovian phase, participants had to choose which stove was followed by which outcome. All stoves were presented on the middle of the screen and pictures of each outcome were presented on the bottom of the screen. Participants could pick the outcome by using the computer mouse. The data of participants who did not correctly report any of the
Transfer phase
During the transfer phase, participants were instructed that they would see each stove again, one at the time, and they were allowed to press any button they wanted or choose to not respond at all. Then, the transfer phase started. Each stove was presented 12 times (60 trials in total), with fire coming out of four places from the stove as was done in the Pavlovian phase. Similar to the study by Lewis et al. (2013), no outcome was presented in this phase. Instead, all stoves were followed by the message “the gas is refilling,” which was presented for 2,000 ms.
3
Unless this message was presented, participants were allowed to press any button. We did not record any press responses unless any of the
Statistical analyses
To test whether participants learned to cancel the aversive events during the instrumental phase, we performed a 2 (
To test our specific PIT hypothesis, we compared between-group differences in responding to
Finally, to test the general PIT hypothesis, we compared differences in responding for
Results
Questionnaires
As expected, between-group differences arose in terms of checking behavior,
Background characteristics (mean and standard deviations or raw numbers) per group.
Instrumental conditioning results
Results showed that participants learned to perform the correct response for both

Barplots of mean performance in the instrumental phase per outcome and button response. Error bars denote standard errors.
Specific PIT results
Results showed that participants performed

Barplots of mean performance in the transfer phase per outcome and button response. Error bars denote standard errors.
Given the significant Stimulus × Response × Group interaction, we followed up our analyses with separate repeated measures ANOVAs within each group. Results showed the same pattern of responses across both groups but now the rate of responding was higher for the OC− group, Stimulus × Response interaction,
General PIT results
Regarding our exploratory hypothesis, we found a significant Stimulus × Response interaction,
Follow-up post hoc analysis showed that participants pressed the
Discussion
We compared PIT effects between individuals with low (OC−) and high (OC+) levels of subclinical OCD symptomatology in an avoidance-based PIT. To our knowledge, this is the first time that PIT performance was tested in a population with OCD-related symptomatology. Results showed that both groups exhibited a specific PIT effect, as reflected in the transfer phase, by more frequently pressing the
No between-group differences in terms of trait or state anxiety arose. This may be because the sample had subclinical levels of OCD. Nonetheless, we think it is important to refer to the potential role that anxiety and stress could have played in our results. Specifically, the limited differentiation between the
Although we tested general PIT effects only for exploratory reasons, we acknowledge that our results partially contradict those by Lewis et al. (2013). In that study, healthy individuals underwent an avoidance-based PIT task. Results showed that healthy individuals exhibit both specific and general PIT effects. Although we found clear specific PIT effects, we found only weak evidence for the presence of a general PIT. These differences could be explained by procedural deviations between the different studies. Lewis et al. (2013) used a game-like scenario in which participants had to avoid attacks from different on-screen creatures (e.g., goblins) by using specific shields. In our study, we tailored our task after an impulsive-like checking scenario, where participants had to learn to avoid different house being destroyed. Arguably, the two experiments could be considered only conceptually similar. As such, procedural differences between these studies could have resulted in differences in outcomes for the general PIT.
Our study has limitations. First, we used a relative small sample size, although it was large enough to detect medium to small effects. Second, although we found between-group differences in terms of OCD symptoms, there were no between-group differences in trait anxiety, possibly due to random sample variations. Third, our design allowed us to evaluate PIT during the
All in all, by using an avoidance-related PIT, we explored whether participants with higher levels of OCD symptomatology exhibit higher performance, compared to participants with lower levels of OCD. Our results provide some preliminary evidence that individuals with lower subclinical levels of OCD show somewhat stronger specific PIT than individuals with higher levels. We acquired also preliminary but weak evidence for the presence of a general PIT. We argue that together with other associative learning tasks (e.g., Pavlovian conditioning procedures), the use of PIT could prove useful in further testing how learning processes contribute to OCD symptomatology.
Footnotes
Acknowledgments
The authors would like to thank Dieuwke Sevenster for help with the design of this study and Rosa Ratsma for assisting with data collection as well as for programming parts of the statistical analyses. They would also like to thank Jur M. Kersten, Kubra Simsek, Floor Schijen, Myrthe van Gestel, and Romy Schouten for collecting the experimental data.
Authors’ note
Angelos-Miltiadis Krypotos is now affiliated also with the Health Psychology Research group at KU Leuven.
Declaration of Conflicting Interests
The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding
The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This study was supported by a VICI grant (453-15-005) awarded to Professor Iris M. Engelhard by the Netherlands Organisation for Scientific Research (NWO).
