Neural and behavioral correlates of sexual stimuli anticipation point to addiction-like mechanisms in compulsive sexual behavior disorder

Abstract

Background and aims: Compulsive sexual behavior disorder (CSBD) is characterized by persistent patterns of failure to control sexual impulses resulting in repetitive sexual behavior, pursued despite adverse consequences. Despite previous indications of addiction-like mechanisms and the recent impulse-control disorder classification in the International Classification of Diseases (ICD-11), the neurobiological processes underlying CSBD are unknown.

Methods: We designed and applied a behavioral paradigm aimed at disentangling processes related to anticipation and viewing of erotic stimuli. In 22 male CSBD patients (age: M = 38.7, SD = 11.7) and 20 healthy male controls (HC, age: M = 37.6, SD = 8.5), we measured behavioral responses and neural activity during functional magnetic resonance imaging (fMRI). The main outcomes were response time differences between erotic and non-erotic trials and ventral striatum (VS) activity during anticipation of visual stimuli. We related these outcomes with each other, to CSBD diagnosis, and symptom severity.

Results: We found robust case-control differences on behavioral level, where CSBD patients showed larger response time differences between erotic and non-erotic trials than HC. The task induced reliable main activations within each group. While we did not observe significant group differences in VS activity, VS activity during anticipation correlated with response time differences and self-ratings for anticipation of erotic stimuli.

Discussion and conclusions: Our results support the validity and applicability of the developed task and suggest that CSBD is associated with altered behavioral correlates of anticipation, which were associated with ventral striatum activity during anticipation of erotic stimuli. This supports the idea that addiction-like mechanisms play a role in CSBD.

Keywords: anticipation; compulsive sexual behavior disorder; functional MRI; hypersexual disorder; sex addiction; sexual stimuli.

Fig. 1.

Schematic representation of the sexual incentive delay fMRI task. Two example trials of non-erotic control trials (top) and erotic trials (bottom) are shown. The total number of trials was n = 80 (40 for each trial type) acquired in two sessions. Each session contained 20 erotic and 20 non-erotic control trials. Total task duration was approximately 24 min. The trial order was pseudo-randomized. Event durations are indicated. Event 1 grey screen (determined the inter-trial interval): random duration between 4 and 7 s. Event 2 was the anticipation phase presenting a cue symbol that indicated the type of trial, i.e., the future presentation of either an “erotic” or a “non-erotic” image (main event of interest). The meaning of each symbol was explained to the participants outside the scanner, who also performed a short practice session prior to the experiment. Event 3 (fixation cross) indicated task preparation. Event 4 target square: task requires button press. Participants were instructed to press a button as quick as possible when the square appeared and if they would respond fast enough the outcome image will be presented. The button-press task was included to keep participants alert and to assess reaction times as a proxy measure for ‘motivation to win’. Fail rate was fixed to 20%, where an image of noise was presented instead as visual stimuli (see Supplemental Materials for more details on task design). Event 5 grey screen: waiting period (random duration). In event 6, the image corresponding to the trial type was presented, i.e., either an erotic or non-erotic visual stimulus (secondary event of interest). Acquisition procedure was designed to avoid potential order effects, effects induced by symbol rotation, and habituation/conditioning effects (see Supplemental Materials). Jittering (random presentation times) of inter-stimuli durations was applied to disentangle reward anticipation from receipt or button press-related brain activation. Two contrasts were compared between CSBD patients and controls: Contrast 1 (main): Difference in brain activation between erotic and non-erotic trials during anticipation phase (event 2). Contrast 2 (secondary): Difference in brain activation between erotic and non-erotic trials during image presentation (event 6).

Fig. 2.

Behavioral results from the sexual incentive delay task performed during fMRI. The scheme demonstrated the observed trial-by-group interaction and corresponding ΔRT differences. Mean reaction time for each trial type (erotic vs. non-erotic) and group (HC vs. CSBD) are shown. ΔRT for each group is indicated (vertical arrows). Numerical values are listed in Table 2

Fig. 3.

Within-group task-related fMRI mean activations. Corrected COPE mean activations (erotic > non-erotic) for contrast 1 (anticipation) are displayed for both healthy controls (HC, top) and CSBD patients (bottom). Z values are indicated by color (heat map). Although there are visual regional differences in activation patterns between HC and CSBD, direct group comparisons were not significant after correction (same applied to the reversed contrast HC > CSBD). Note that whole brain analyses were exploratory. Results for contrast 2 (viewing phase) and uncorrected group comparisons at a threshold of P = 0.01 are shown in the Supplemental Materials (Figure S3–S6). Cluster statistics, MNI coordinates of activation maxima, and regional labels are provided in the Supplemental Materials Table S10 and S12

Fig. 4.

A: Correlation between VS activation during anticipation and ΔRT. Patient data is plotted in red, HC data in blue. Supplementary Figure S2 shows the regression plot when excluding the outlier with highest VS and lowest ΔRT. Note that we deem results including the outlier reliable (see main text and Supplemental Materials for reasoning). B: Correlation between VS activity during anticipation phase and rating of how much CSBD patients reported to look forward to viewing erotic images (asked before fMRI experiment) (r = 0.61, P = 0.002). Such correlation was not observed in controls (r = −0.221, P = 0.362; see Supplemental Materials for more details)