Abstract
Background and aims
Despite a previously reported connection between compulsive sexual behaviors (CSB), such as problematic pornography use, and heightened cue-reactivity, empirical evidence of the alteration of processes responsible for increased salience attribution to erotic cues remains sparse. Drawing on similarities with addiction models, this study explores the neuronal mechanisms of CSB through the use of appetitive conditioning and extinction with erotic and monetary rewards.
Methods
Thirty-two heterosexual males struggling with CSB (age: 28.9 ± 7.1), and 31 healthy matched participants (age: 27.8 ± 5.6) underwent active appetitive conditioning and extinction tasks in fMRI. The effects of conditioning and extinction towards cues of erotic and monetary rewards were measured via self-assessment (valence and arousal rating towards cues), behavior (reaction times), and brain reactivity.
Results
In conditioning, subjective ratings increased, and reaction times were faster for both erotic and monetary cues among participants with CSB, along with altered activity in ventral striatum (vStr), dorsal anterior cingulate cortex (dACC), and anterior orbitofrontal cortex (aOFC). In extinction, self-assessment ratings remained elevated in the CSB group for both cues in a non-reward-specific fashion, accompanied by altered activity of dACC and vStr.
Discussion and conclusions
These findings suggest enhanced incentive salience attribution to conditioned cues, highlighting a generalized motivational and value-related transfer from rewards to the cues in participants with CSB. Additionally, despite the absence of rewards, the persistence of arousal and valence towards cues underscored the maladaptive extinction process. These insights advance the understanding of CSB's neurobiological underpinnings and its relation to addiction frameworks.
Introduction
Compulsive sexual behavior disorder
Despite the growing body of research (Gola & Potenza, 2018; Kraus, Voon, & Potenza, 2016; Kühn & Gallinat, 2016), and the inclusion of compulsive sexual behavior disorder (CSBD) in the 11th edition of the International Classification of Diseases (ICD-11), many of the neural mechanisms underlying compulsive sexual behaviors (CSB, e.g. problematic pornography use) remain unknown. Numerous studies have drawn parallels between CSB and various forms of addiction (Bőthe et al., 2019; Chatzittofis et al., 2016; Draps et al., 2020; Gola & Draps, 2018; Kor, Fogel, Reid, & Potenza, 2013; Kowalewska et al., 2018; Liberg et al., 2022; Mechelmans et al., 2014; Sinke et al., 2020). A key point of discussion is the dysfunction in the brain reward system, which leads to an ‘incentive salience’ toward stimuli linked with problematic behaviors. This is characterized by an intense craving for the objects of addiction (such as drugs or behaviors like gambling) and heightened sensitivity to cues related to these objects. This increased reactivity is further influenced by the process of associative learning (both Pavlovian and instrumental conditioning), which is vital in the shift from perceiving stimuli as neutral to viewing them as addictive. This shift enhances attention and goal-oriented behavior toward these stimuli, as described in the Incentive Salience Theory (IST; Robinson & Berridge, 2003, 2008). While IST was originally developed to explain substance use disorders, it offers a framework for understanding the neural underpinnings of addictive behaviors, and it is frequently discussed in regard to CSB (Engel et al., 2023; Gola & Draps, 2018; Liberg et al., 2022).
Conditioning
Conditioning is a procedure and a mechanism, leading to the transfer of the subjective value of unconditioned–stimulus (UCS, and an operant or automatic response associated with it) to another, co-occurring, neutral stimulus (conditioned stimulus, CS). There are two main types: classical (Pavlovian) conditioning in which automatic reaction to UCS is transferred to CS after mere pairing of the stimuli; and instrumental conditioning, in which an action by the subject is required to obtain the reward (or avoid punishment) announced by a cue (CS). In appetitive conditioning, UCS is a rewarding stimulus/event of sufficient value to produce the motivation to obtain it. Successful appetitive conditioning results in an emotional/motivational response to the appearance of the CS, which is the cue-reactivity phenomenon posited in IST (Starcke, Antons, Trotzke, & Brand, 2018). Extinction is another important associative learning process. It occurs when the CS-UCS pairing or action-UCS is discontinued and a new rule, i.e. lack of CS-UCS relationship is formed, suppressing the previously developed association (Konorski, 1967; Quirk & Mueller, 2008). Extinction should lead to an inhibition of the motivational response. From a neurobiological perspective, ventral striatum (vStr), amygdala, ventromedial prefrontal cortex (vmPFC), orbitofrontal cortex (OFC), and dorsal anterior cingulate cortex (dACC) control the formation of CS-UCS or action-UCS relationships, and their impairment is responsible for the development of problematic behaviors (Kruse, Klein, Tapia León, Stark, & Klucken, 2020).
Conditioning and CSB
As described in the IST, the development of cue-reactivity due to associative learning may underlie the development of symptoms of CSB. Previous neuroimaging studies of cue-reactivity in a diagnosed sample of individuals with CSB have shown similarities between this disorder and behavioral addictions, reporting increased reactivity of the vStr and OFC during stimulation with cues of erotic rewards (Gola, Wordecha, et al., 2017; Golec, Draps, Stark, Pluta, & Gola, 2021), but in a study on a general male sample researchers found no correlation of the vStr activity and time spent on pornography use or sexual motivation trait (Markert, Klein, Strahler, Kruse, & Stark, 2021).
To our knowledge, the associative learning process in context of CSB has so far been examined in only two neuroimaging studies (Banca et al., 2016; Klucken, Wehrum-Osinsky, Schweckendiek, Kruse, & Stark, 2016) and three behavioral studies (Hoffmann, Goodrich, Wilson, & Janssen, 2014; Snagowski, Laier, Duka, & Brand, 2016; Wells, Krejčová, Binter, Pfaus, & Horsley, 2022). Wells et al. (2022) demonstrated the absence of altered conditioning using only monetary rewards by comparing groups with high and low severity of symptoms in a general male sample. Also on a general male sample, Snagowski et al. (2016), showed that the strength of associative learning of visual erotic cues was related to cybersex addiction tendencies. Hoffman et al. (2014) study found that people with high severity of sexual compulsivity also showed increased conditioned responses to olfactory cues of erotic rewards. These behavioral studies used conditioning tasks that included both Pavlovian and instrumental aspects to investigate the phenomenon of altered associative learning.
To investigate on a neuronal level, a study conducted by Banca et al. (2016) used Pavlovian conditioning during fMRI and a session of Pavlovian and instrumental conditioning beforehand. Behaviorally, the conditioning effect was stronger among individuals diagnosed with CSB for both erotic and monetary cues and there were no differences in brain activity related to the type of cue. Klucken et al. (2016) also used Pavlovian conditioning, but with erotic rewards only and found increased amygdala responses to rewarding cues in the CSB group. They also found decreased vStr connectivity to the vmPFC compared to healthy subjects.
The current understanding of this area of research is limited, with a significant gap in empirical evidence and the absence of a coherent theoretical framework. Given the parallels between CSB and addictive behaviors, the IST, alongside the conditioning process, emerges as a potential framework for explaining the emergence of CSB symptoms. The persistence of these symptoms might be interpreted as an abnormal extinction process. In light of this, we decided to conduct a neuroimaging study aimed at observing the mechanisms of active appetitive conditioning and extinction among individuals with CSB using both erotic and monetary rewards, serving as disorder-specific and general rewarding stimuli. Based on the IST framework (Robinson & Berridge, 2003, 2008) and previous research (Banca et al., 2016; Gola, Wordecha, et al., 2017; Golec et al., 2021; Hoffman et al., 2014; Klucken et al., 2016; Snagowski et al., 2016), we hypothesized that during the conditioning procedure, men struggling with CSB would be characterized by stronger conditioning effects for erotic cues, evident in increased arousal and motivation and reflected by self-assessment, reaction times and brain activity alterations in orbitofrontal and ventromedial prefrontal cortices, dorsal anterior cingulate cortex, ventral striatum, and amygdala. These effects should be more difficult to extinguish for men struggling with CSB, leading to higher persistence during the extinction procedure.
Methods
Participants
Sixty-six right-handed heterosexual males participated in the study, among which 33 self-identified as struggling with CSB and 33 as healthy control (HC) subjects. Recruitment was done via therapist referrals and internet-based and social media advertisements. All participants underwent screening with psychological questionnaires before the fMRI examination [Brief Pornography Screener (BPS, Kraus et al., 2020); Sexual Addiction Screening Test (SAST-R, Gola, Skorko, et al., 2017); South Oaks Gambling Screen (SOGS, Lesieur & Blume, 1987); Criteria for Hypersexual Disorder (HD, Kafka, 2010); Obsessive Compulsive Inventory (OCI-R, Foa et al., 2002); The Hospital Anxiety and Depression Scale (HADS, Zigmond & Snaith, 1983); Hypersexual Behavior Inventory (HBI, Reid, Garos, & Carpenter, 2011); Alcohol Use Disorders Identification Test (AUDIT, Babor, de la Fuente, Saunders, & Grant, 1992); Impulsiveness Scale (IS-12, Kahn et al., 2019; Szczypiński, Jakubczyk, Kopera, Trucco, & Wojnar, 2021)], and were also asked for time spent on pornography consumption in the month prior to the examination. Participants meeting the inclusion criteria were assigned to either the CSB or HC group. The inclusion criteria for the CSB group were: at least 4 or 5 criteria of HD, BPS score 6 or more, SAST-R 6 or more, whereas for the HC group, the criteria were BPS score 3 or less, SAST-R 5 or less, and HD 1 or 0. Additionally, both groups had to score SOGS 4 or less, OCI-R 25 or less and HADS 19 or less. Additionally, general exclusion criteria related to contradiction in taking part in MRI examination, i.e. significant health issues, epilepsy, serious past head traumas, metal objects/implants in the body. Subjects were also informed to abstain from alcohol, caffeinated beverages, and psychoactive substances at least one day prior to the experiments, although they were informed that if caffeine is included in the morning routine, it is advised to follow it on that day. Additionally, subjects were asked to be well rested before the experimental session. Three subjects (two HC and one CSB) were removed from the analysis due to incomplete data. The reliability of used questionnaires are presented in supplementary materials.
Conditioning and extinction tasks
During the fMRI examination, subjects engaged in a conditioning and extinction procedure (extended task used by Kruse, Tapia León, Stark, & Klucken, 2017, see Fig. 1). The conditioning task consisted of two fMRI runs (10 min each). It was followed by the extinction task that had exactly the same structure as the conditioning task, except that no matter how quick the response, subjects could never win any UCS+ and were always presented with UCS- (scrambled picture). Subjects were compensated based on task performance, up to 120 PLN (27 EUR).
Conditioning task design. Each trial began with a fixation cross (6–10 s), followed by 1 of 3 possible simple shapes (6 s), which were cues (CS+) informing about the category of a possible reward. Next, for a randomized length of time (1–3 s), a small circle was presented, followed by a larger circle during which subjects had to quickly react with a button click in order to win a reward. The window of opportunity was between 140 and 500 ms. For fast enough responses, the reward was displayed accordingly to trial type: either a pornographic or erotic picture of women for erotic condition (UCS+erotic), the amount (2–5 PLN) won in the given trial for the monetary condition (UCS+cash), and a scrambled picture for control condition (UCS-). Reactions outside the window of opportunity always resulted in scrambled pictures (UCS-). After the reward presentation (2.5 s), a brief eye pictogram was displayed (3 s) to remind participants to blink during this period. The strength of CS reinforcement was kept at around 70% (7 out of 10 trials of both CS+ condition types in each fMRI run) and was controlled by an adaptive window of opportunity length in which reactions would result in a reward. Details regarding the adaptive procedure can be found in the supplementary materials. The connection between cue shape and reward type was randomized between subjects. Participants were instructed to react as fast as possible in the target period, regardless of cue type
Citation: Journal of Behavioral Addictions 2025; 10.1556/2006.2025.00012
To assess the behavioral effects of conditioning and extinction success, subjects were asked to rate their valence and arousal towards simple shapes (all three CS) in the form of a 7-point Self-Assessment Manikin (Bradley & Lang, 1994) at three time points: before the beginning of conditioning, after conditioning, and after extinction (see Fig. 2).
Experimental procedure protocol. Before entering the MRI room, subjects were asked to rate valence and arousal towards shapes used as the CS in the following tasks. Then, after finishing the conditioning task and after the extinction task, subjects were again asked to rate their CS-related valence and arousal. Conditioning and extinction tasks each lasted 20 min and were divided into early and late phases. To increase sensitivity to effects taking place during the early and late phases of the learning process, the first seven trials were taken into analysis for the early and the last seven for the late phase
Citation: Journal of Behavioral Addictions 2025; 10.1556/2006.2025.00012
Analysis of behavioral and self-assessment data
The effects of conditioning and extinction on subjective arousal and valence were analyzed using a three-way repeated-measures ANOVA with a within-subjects factor of Time (pre-, post-conditioning, and post-extinction), Condition Type (monetary and erotic), and a between-subjects factor of Group (CSB vs. HC). RTs were analyzed in two separate three-way ANOVAs (one for conditioning and second for extinction task): one with the effect of Time (early and late conditioning), Condition Type, and Group. For data reduction purposes and to follow subtractive fMRI analysis logic, we used the difference scores (Δ) of subjective ratings and reaction times between each CS+ relative to the CS-. All post-hoc tests were adjusted for multiple comparisons using Bonferroni correction unless stated otherwise. The generalized eta squared (
Image acquisition and preprocessing
Neuroimaging was performed on a 3T Siemens Prisma MRI scanner using a 64-channel RF head coil. For functional imaging, a multi-band sequence was used with TR = 750 ms and voxel size 2 × 2 × 2 mm. Preprocessing of the MRI data was done using SPM12 (WellcomeTrust Centre for Neuroimaging, UK), FSL (Jenkinson, Beckmann, Behrens, Woolrich, & Smith, 2012), and in-house MATLAB code. Standard SPM preprocessing steps were used to prepare fMRI data, notably using a 6 mm smoothing kernel and 0.004 Hz high-pass filter. A further description of the image acquisition parameters, neuroimaging data preprocessing, and hardware and software used in the experiment can be found in the supplementary materials.
Image analysis
Functional images were analyzed using the general linear model in SPM12. BOLD responses evoked by each cue type (CS+erotic, CS+cash, CS-) and reward type (UCS+erotic, UCS+cash, UCS-) were modeled as separate regressors. Details regarding statistical modeling of the fMRI data can be found in the supplementary materials. For the exploratory whole-brain analysis, we tested the following CSB vs. HC contrasts for each of the four stages: 1) CS+erotic vs. CS-; 2) CS+cash vs. CS-, for a total of 8 contrasts of interest. Additionally, analogous whole-brain analysis was conducted without between-subject factor (no group division) for the purpose of general task activity visualization. Whole-brain group-level analyses used a voxel-level threshold of p < 0.001 and cluster-based correction pFWE < 0.05. The results of this exploratory analysis can be found in the supplementary materials (Figs S1–S3, and Tables S1 and S2), as well as on the online repository: https://neurovault.org/collections/JLXZWOAJ/
For the main fMRI analysis, knowing that the effects of conditioning and reward anticipation in CSB on brain functioning are small (for a review, see Klein et al., 2022), we chose a priori-hypothesized bilateral regions of interest (ROI) to improve statistical test sensitivity. For ROI analysis, we used the following regions: vStr (functionally defined mask from previous studies; Gola, Wordecha, et al., 2017), amygdala (structural mask derived from Harvard-Oxford atlas), anterior and posterior orbitofrontal cortex (aOFC and pOFC, structural masks derived AAL3 atlas; Rolls, Huang, Lin, Feng, & Joliot, 2020), dACC (functionally defined mask from Brainnetome Atlas, label A32p; Fan et al., 2016) and vmPFC (structural mask derived from AAL3 atlas under the name fronto-medial orbitofrontal cortex). ROIs are visualized in Fig. 3. For the conditioning, we analyzed activity of vStr, aOFC, pOFC, amygdala, vmPFC, and dACC; for extinction, we used a reduced set of ROIs: vStr, amygdala, vmPFC, and dACC.
Visualization of ROIs chosen for analysis. The ventral striatum is colored in turquoise, amygdala in pink, dorsal anterior cingulate cortex in yellow, anterior and posterior orbitofrontal cortices in red, and blue and ventromedial prefrontal cortex in green
Citation: Journal of Behavioral Addictions 2025; 10.1556/2006.2025.00012
The averaged contrasts of beta estimates of each CS+ vs. CS- for each condition of each task from the ROIs were extracted. In an analogous fashion to the RT analysis, ROI values were analyzed in two separate three-way ANOVAs for each ROI: one with the effect of Time, Condition Type, and Group and a second identically analyzed one for the extinction task. All post-hoc tests were adjusted for multiple comparisons using Bonferroni correction unless stated otherwise.
Ethics
Before taking part in the study, all subjects gave their written informed consent for participation and were screened for any contraindications to MRI. The research protocol was approved by a local ethical committee and was conducted in accordance with the Declaration of Helsinki.
Results
Psychological profile
Group characteristics in demographic and clinical variables are listed in Table 1.
Demographic and clinical characteristics of the CSB and HC groups. Each variable was compared between the CSB and HC groups using an independent t-test without correction for multiple comparisons
| CSB group | HC group | Group Difference | ||||
| Mean | SD | Mean | SD | t-value | p-value | |
| Age | 28.91 | 7.07 | 27.81 | 5.62 | 0.682 | 0.498 |
| BPS | 8.31 | 1.42 | 1.29 | 1.16 | 21.417 | <0.001 |
| SAST-R | 11.56 | 3.53 | 1.94 | 1.34 | 14.228 | <0.001 |
| HBI | 60.94 | 12.46 | 24.13 | 3.79 | 15.751 | <0.001 |
| HADS–Anxiety | 6.66 | 3.11 | 4.00 | 2.65 | 3.648 | <0.001 |
| HADS–Depression | 4.28 | 3.02 | 2.39 | 1.69 | 3.061 | 0.003 |
| OCI-R | 12.06 | 5.90 | 9.61 | 6.44 | 1.576 | 0.12 |
| IS-12–Cognitive | 11.90 | 2.19 | 10.80 | 2.76 | 1.806 | 0.076 |
| IS-12–Behavioral | 14.22 | 3.53 | 13.97 | 3.58 | 0.279 | 0.781 |
| Pornography consumption (hours/week) | 6.67 | 6.66 | 1.08 | 1.16 | 4.603 | < 0.001 |
CSB—Compulsive Sexual Behaviors; HC—healthy control; BPS—Brief Pornography Screener; SAST-R—Sexual Addiction Screening Test; OCI-R—Obsessive Compulsive Inventory; HBI—Hypersexual Behavior Inventory; IS-12—Impulsiveness Scale. Statistically significant results are highlighted by a bold font.
Analysis of behavioral and self-assessment data
The ANOVA results of the subjective valence rating (Fig. 4), measured between the conditioning and extinction tasks, showed a significant effect of Group (F = 10.25, p < 0.01,
Subjective arousal (left) and valence (right) towards both CS+ (relative to the CS-) before the beginning of the conditioning task, after conditioning, and after the extinction task. The CSB group is denoted with plain bars and the HC with striped bars. The difference between CS+erotic vs. CS- is coded in red, and CS+cash vs. CS- is coded in blue. Error bars represent standard error. CSB—Compulsive Sexual Behaviors, CS—Conditioned Stimulus
Citation: Journal of Behavioral Addictions 2025; 10.1556/2006.2025.00012
Similarly, ANOVA for the arousal rating (Fig. 4) showed a significant effect of Group (F = 10.78, p < 0.001,
General successful conditioning and extinction reflected in the cue preference were shown in both of these ANOVA with a significant Time effect (arousal: F = 20.57, p < 0.001,
The ANOVA results of reaction times during conditioning (Fig. 5) showed a significant effect of Group (F = 6.44, p < 0.05,
Reaction times (ms) for both types of CS+ (relative to the CS-) during (left) conditioning and (right) extinction tasks are divided into early and late phases. The CSB group is denoted with plain bars and the HC with striped bars. The difference between CS+erotic vs. CS- is coded with red, and CS+cash vs. CS- is coded with blue color. Error bars represent standard error. CSB—Compulsive Sexual Behaviors, CS—Conditioned Stimulus
Citation: Journal of Behavioral Addictions 2025; 10.1556/2006.2025.00012
General heightened motivation, reflected by a faster RT in both conditioning and extinction, was shown in both of these ANOVAs with a significant Condition Type effect (conditioning: F = 39.58, p < 0.001,
Neuroimaging results
ROI analysis in conditioning
During conditioning, vStr yielded an interaction for Group x Time effects (F = 4.73, p < 0.05,
Brain activity during both CS+ (relative to the CS-) during conditioning is divided into early and late phases for 3 ROIs: (lower left) ventral striatum, (lower middle) anterior orbitofrontal cortex, and (lower right) dorsal anterior cingulate cortex), with significant Group or interaction with Group factors in the ANOVA model. The CSB group is denoted with plain bars and the HC with striped bars. The difference between CS+erotic vs. CS- is coded with red, and CS+cash vs. CS- is coded with yellow. Error bars represent standard error. The upper panel represents localization of the regions of interest. CSB—Compulsive Sexual Behaviors, CS—Conditioned Stimulus
Citation: Journal of Behavioral Addictions 2025; 10.1556/2006.2025.00012
ROI analysis in extinction
In extinction, vStr yielded an interaction for Group x Time x Condition Type effects (F = 7.76, p < 0.01,
Brain activity during both CS+ (relative to the CS-) during extinction is divided into early and late phases for 2 ROIs: (lower left) ventral striatum and (lower right) dorsal anterior cingulate cortex with significant Group or interaction with Group factors in the ANOVA model. The CSB group is denoted with plain bars and the HC with striped bars. The difference between CS+erotic vs. CS- is coded in red, and CS+cash vs. CS- is coded in blue. Error bars represent standard error. The upper panel represents localization of the regions of interest. CSB—Compulsive Sexual Behaviors, CS—Conditioned Stimulus
Citation: Journal of Behavioral Addictions 2025; 10.1556/2006.2025.00012
Discussion
In this study, we looked for signs of altered appetitive associative learning processes in men struggling with CSB. On the behavioral level, we found that in comparison to the control group, they expressed stronger subjective responses and shorter reaction times to cues of stimuli reinforced by both erotic and monetary rewards. These effects were not reflected in fMRI whole-brain analysis, which is in line with previous studies that reported no robust CSB-specific alterations of activity patterns (for review: Klein et al., 2022). More sensitive ROI analysis indicated specific effects, which we discuss below in detail.
Behavioral effects of conditioning
Previous studies on CSB reported mixed results regarding self-assessed and behavioral reactions during conditioning tasks. Such ambiguity may be related to differences in studied populations (diagnosed, sub-clinical and general), implemented reward modalities (monetary, erotic, or both) and task used (Pavlovian vs. instrumental conditioning). Enhanced transfer of motivational value to an initially neutral CS+ (measured via self-assessment or behaviorally) was observed in three studies, out of which two used Pavlovian conditioning and all three used an erotic reward type (Banca et al., 2016; Hoffman et al., 2014; Snagowski et al., 2016). The study of Banca et al. (2016) was the only study to use both monetary and erotic reward, and, similar to our results, they observed strengthened conditioning to both of them. Our two studies suggest that there might be general, unspecific strengthening of reward-based associative learning in CSB. On the other hand, Snagowski et al. (2016), who (like Banca et al., 2016) used Pavlovian-to-instrumental conditioning using only a CS+ of monetary rewards, did not observe the transfer. One possible explanation for this discrepancy is the fact that Snagowski et al. (2016) studied a general male population sample that was median-split based on Online Sexual Behaviour questionnaire scores, while Banca et al. (2016) and the present study studied men struggling with CSB.
Self-assessment results indicated that subjective motivational (arousal) and value-related (valence) transfer from UCS to CS+ was enhanced in CSB. The motivational transfer was more reward-specific towards erotic CS+, whereas value-related transfer was non-reward-specific. Since our task design included elements of instrumental conditioning (receipt of the reward depended on the speed of performed button press), we were also able to objectively measure motivational aspects of UCS to CS+ transfer with analysis of reaction times. In the late phase of conditioning, the RT to both rewarding CS+ were shorter in the CSB group, but with no bias toward cues of erotic rewards. The latter result is inconsistent with subjective self-assessment of arousal described above and not in line with our expectations.
Attentional biases have been linked to CSB symptoms, with several studies demonstrating a correlation between CSB and increased attentional processing and cue sensitivity for erotic content (Albery et al., 2017; Banca et al., 2016; Draps et al., 2021, 2024; Gola, Wordecha, et al., 2017; Liberg et al., 2022; Mechelmans et al., 2014; Pekal, Laier, Snagowski, Stark, & Brand, 2018; Wang, Chen, & Zhang, 2021). Consequently, we also expected stronger conditioning effects for trials with erotic rewards. However, our results only partially (on the level of self-assessment, but not RTs) corroborate this anticipated effect. This discrepancy can also support the hypothesis that the CSB group might exhibit an non-specific enhancement of appetitive conditioning. The vulnerable individuals, through continual exposure to various experiences, could develop a preference for certain erotic stimuli and, upon repeated exposure to these stimuli, begin to demonstrate specific effects manifesting as attentional biases towards erotic stimuli. Given that our task was designed to assess immediate and transient associative learning, we were unable to detect this process.
Brain activity during conditioning
We expected regions previously documented as functionally altered in CSB and related to motivational (dACC and vStr), value-related (aOFC, pOFC, and vmPFC) and affective processing (amygdala) to be differentially engaged during conditioning in the CSB group. Our fMRI results do not fully corroborate two of the previous neuroimaging studies of conditioning in CSB (Banca et al., 2016; Klucken et al., 2016). These studies used Pavlovian tasks with either erotic or erotic and monetary rewards. In Banca et al. (2016), no group differences in any of the CS+’s processing were observed in the whole-brain analysis, but researchers did not use any hypothesis-driven ROI analysis. In Klucken et al. (2016), researchers used the occipital cortex, insula, OFC, vStr, and amygdala as their ROI, and only in the amygdala they detected increased activity related to erotic CS+ as the group difference. In contrast, we did not observe changes in amygdala activity in the CSB group. However, the conditioning task we used included instrumental (active) elements, and amygdala was documented to be more often engaged in Pavlovian than instrumental conditioning (Chase, Kumar, Eickhoff, & Dombrovski, 2015). Also, in contrast to Klucken et al. (2016), we detected altered activity in aOFC and vStr, further adding to the importance of the task design. The aOFC has previously been implicated in a study on cue-reactivity in the CSB (Golec et al., 2021), in which the authors interpreted its activation as involved in aberrant salience attribution to the stimuli related to the addiction. Corroborating that finding, our results show that the effect is not specific to cues of erotic rewards and may underlay non-specific enhancement of appetitive conditioning. Interestingly, we found that vStr activity was dampened in the CSB group in comparison to the healthy subjects during late conditioning for both types of CS+. Not only do these results suggest that the activity was altered in a non-specific fashion, but importantly, that active conditioning engages these brain regions in a more complex way than the passive Pavlovian counterpart, as well as tasks based on cue-reactivity without conditioning aspects used in previous study on the CSB (Gola, Wordecha, et al., 2017).
The role of the dACC in associative learning, and more specifically in learning goal-directed actions via motivational processing, has been extensively studied in rodents and, to some extent, in humans (Shenhav, Botvinick, & Cohen, 2013; Yee, Crawford, Lamichhane, & Braver, 2021). The dACC plays a crucial role in learning, and it exhibits higher activity during early exploring phases of tasks and is positively related to the learning rate (Heilbronner & Hayden, 2016). The activity of dACC is also involved in general-domain reward monitoring and reward-motivated behaviors, enabling reward-related choices to be transferred into motor actions (Bush et al., 2002; Rushworth & Behrens, 2008). In line with our hypothesis, the activity of dACC was altered in CSB: hyperactive in early conditioning and hypoactive during late conditioning when the cue-reward relationship was already established. The observed results again presented non-reward-specific activity alteration. Interestingly, we expected both dACC and vStr to be hyperactive in late conditioning in the CSB group on the grounds of documented heightened reactivity towards cues of erotic rewards in tasks with explicit cue-reward relationships (Gola, Wordecha, et al., 2017; Voon et al., 2014). However, despite expected similarities of both tasks in that regard (anticipation of already known reward), the context of learning via conditioning influenced the reactivity of dACC in the CSB group such that it activated more strongly during the novelty-driven exploring phase of the conditioning rather than the exploitative phase.
Extinction
The extinction process is considered crucial to clinical approaches and cognitive behavioral therapy of addiction (Goode & Maren, 2019; Lovibond, 2004). In chemical addictions, aberrant associative learning present in both conditioning and extinction translates to a high rate of relapse after therapeutic interventions (Torregrossa & Taylor, 2013; Zhang et al., 2019). As there were previously no studies on behavioral or self-assessment effects of extinction in the CSB, our results provide first insights into this aspect of associative learning disruption in the context of behavioral addiction in men struggling with CSB.
The persistence of subjective arousal and valence towards both CS+ in the CSB group, despite the absence of rewards, suggests a heightened incentive salience attributed to the CS+ in a non-specific fashion. This enduring “wanting” could reflect a maladaptive learning process where individuals continue to assign high motivational value to the CS+, consistent with the Incentive Salience Theory description of addiction's impact on the reward system (Robinson & Berridge, 2003). From a therapeutic perspective, this may mean two things. First, typical therapeutic techniques based on habituation processes, e.g. behavioral experiments in the CBT framework, working on habituation of the response to the trigger, could be less effective or secondly, it could indicate the potential importance of relearning processes and thus require increased exposure to the stimulus, similarly as it has been demonstrated before in the case of nicotine addiction (Conklin & Tiffany, 2002; McClernon, Hiott, Huettel, & Rose, 2005; Waters et al., 2004).
The only previous neuroimaging study on the extinction process in the CSB was by Banca et al. (2016), in which they found no neuronal alteration in CSB, although they used stringent statistical thresholding adequate for whole-brain fMRI analysis. Increased sensitivity granted by the ROI analysis allowed us to find functional alterations in dACC and vStr. The dACC activity in the CSB group was heightened throughout early and late extinction for both types of CS+. The latter effect again suggests non-reward-specific activity alteration. This is consistent with the altered activity observed in the early novelty-driven exploring phase in conditioning and the impaired extinction demonstrated by self-assessment, suggesting prolonged exploration after the reward was no longer attainable. The vStr plays a crucial role in the dopaminergic system, central to the development of incentive salience (Robinson & Berridge, 2003). It exhibited high activity in the early extinction for both types of CS+, but in the late extinction the activity for the erotic CS+ diminished, while for the monetary CS+ it remained elevated. This nuanced pattern may reflect a differential process of salience reduction for different types of rewards over the course of extinction. Indeed, vStr has been demonstrated to be more sensitive to secondary than primary rewards (Sescousse, Caldú, Segura, & Dreher, 2013). We found no activity alteration in the amygdala in the CSB group, despite previous studies suggesting that it might play an important role in the extinction process (Kruse et al., 2020) and documented altered activity in CSB during Pavlovian conditioning (Klucken et al., 2016). Additionally, we did not observe any altered activity in vmPFC, contrary to substance addiction studies (Bechara, 2005; Konova et al., 2019).
Limitations
Several limitations of our study should be considered. First, we recruited only white Caucasian, heterosexual males, which limits our results to this specific subpopulation. We also excluded potential participants based on ongoing problems with alcohol and substance abuse and high OCI-R scores, which measure OCD symptoms. It has been noted that the general CSB population has increased OCI-R scores (Draps et al., 2021); therefore, we have cut off some of the subpopulation. Additionally, this study was planned and conducted before the official introduction of CSBD criteria in ICD-11, hence our sample cannot be considered as clinically diagnosed with CSBD, despite similar CSB symptoms characteristics as measured by BPS, SAST-R and HBI. Secondly, we used an active conditioning task design with only one response possibility. This limits our ability to interpret the results in light of more traditional instrumental conditioning approaches widely studied in animal models. Future studies should focus on studying instrumental conditioning with multiple choices during fMRI examination. A third limitation is related to the fact that the extinction was performed immediately following conditioning. A more ecological approach would be to study the extinction after a consolidation period (Hyman, Malenka, & Nestler, 2006; Kruse et al., 2020).
Conclusions
This study provides new insights into behavioral and brain functioning aspects of appetitive conditioning and extinction in CSB. We included both monetary and erotic rewards to study the specificity of associative learning alterations. Here, the evidence shows that men struggling with CSB are prone to short-term general conditioning and extinction alterations towards cues of both erotic and monetary rewards. These alterations are present in self-assessment, reaction times, and reactivity of the ventral striatum, anterior orbitofrontal cortex, and dorsal anterior cingulate cortex. Further studies should include postponed extinction after a consolidation period.
Funding sources
This study was supported by an NCN grant 2016/21/N/HS6/02635 (to JW) covering data collection and work of JW. Work of MG was supported by an NCN grant 2021/40/Q/HS6/00219 (to MG). The funding body has not participated at any stage in study design, data collection, analysis, or interpretation
Authors' contribution
Study concept and design: JW and MG, data acquisition: JW and PD, analysis and interpretation of data: JW and MD, statistical analysis: JW, obtained funding: JW, study supervision: JW, TW and MG, wrote the manuscript: JW, MD and EK. All authors approved the final manuscript. All authors had full access to all data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis.
Conflict of interest
The authors report no financial or other relationship relevant to the subject of this article.
Acknowledgments
We thank all the participants for their enthusiasm and willingness to participate in the study. We appreciate the help of Tim Klucken and Onno Kruse for helpful inputs on the early stage of the study and sharing their experimental procedure. Additionally, we thank Jan Szczypiński for technical assistance, as well as Alicja Dobrzykowska for aid in data acquisition and participant recruitment.
Supplementary material
Supplementary data to this article can be found online at https://doi.org/10.1556/2006.2025.00012.
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