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Cited by 137Sexuality, Behavior, and TechnologyGambling Behavior and TreatmentsNeural and Behavioral Psychology Studies

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Novelty, conditioning and attentional bias to sexual rewards

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Banca, Paula, Morris, Laurel S., Mitchell, Simon, Harrison, Neil A., Potenza, Marc N., Voon, Valerie·2016·Journal of Psychiatric Research
DOI 10.1016/j.jpsychires.2015.10.017PMC PMC4683093
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Abstract

The Internet provides a large source of novel and rewarding stimuli, particularly with respect to sexually explicit materials. Novelty-seeking and cue-conditioning are fundamental processes underlying preference and approach behaviors implicated in disorders of addiction. Here we examine these processes in individuals with compulsive sexual behaviors (CSB), hypothesizing a greater preference for sexual novelty and stimuli conditioned to sexual rewards relative to healthy volunteers. Twenty-two CSB males and forty age-matched male volunteers were tested in two separate behavioral tasks focusing on preferences for novelty and conditioned stimuli. Twenty subjects from each group were also assessed in a third conditioning and extinction task using functional magnetic resonance imaging. CSB was associated with enhanced novelty preference for sexual, as compared to control images, and a generalized preference for cues conditioned to sexual and monetary versus neutral outcomes compared to healthy volunteers. CSB individuals also had greater dorsal cingulate habituation to repeated sexual versus monetary images with the degree of habituation correlating with enhanced preference for sexual novelty. Approach behaviors to sexually conditioned cues dissociable from novelty preference were associated with an early attentional bias to sexual images. This study shows that CSB individuals have a dysfunctional enhanced preference for sexual novelty possibly mediated by greater cingulate habituation along with a generalized enhancement of conditioning to rewards. We further emphasize a dissociable role for cue-conditioning and novelty preference on the early attentional bias for sexual cues. These findings have wider relevance as the Internet provides a broad range of novel and potentially rewarding stimuli.

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Graphical abstract CC BY · PubMed Central
Fig. 1 Novelty and conditioning behavioral measures. A. Novelty preference: task and outcomes. Subjects were familiarized with sexual images and two non-sexual control images followed by a choice-discrimination task involving choosing between a familiar or matched novel choice randomly (p = 0.50) associated with winning. The graph shows the proportion of novelty choices across trials in subjects with compulsive sexual behavior (CSB) and healthy volunteers (HV). B. Conditioning: task and outcomes. The sexual conditioning task is shown. During conditioning, two black-and-white visual patterns (CS+Sex and CS−) were followed by sexual or neutral images respectively. During choice discrimination testing, subjects chose between CS+Sex and CS− paired with novel visual-pattern stimuli (A and B). The CS+Sex and CS− stimuli were associated with greater probabilities of winning. The graphs show the proportion of conditioned stimuli choices across trials of CSB and HV for Sexual outcomes (left) and Monetary outcomes (right). *Group-by-Valence interaction: p < 0.05.
Fig. 1 Novelty and conditioning behavioral measures. A. Novelty preference: task and outcomes. Subjects were familiarized with sexual images and two non-sexual control images followed by a choice-discrimination task involving choosing between a familiar or matched novel choice randomly (p = 0.50) associated with winning. The graph shows the proportion of novelty choices across trials in subjects with compulsive sexual behavior (CSB) and healthy volunteers (HV). B. Conditioning: task and outcomes. The sexual conditioning task is shown. During conditioning, two black-and-white visual patterns (CS+Sex and CS−) were followed by sexual or neutral images respectively. During choice discrimination testing, subjects chose between CS+Sex and CS− paired with novel visual-pattern stimuli (A and B). The CS+Sex and CS− stimuli were associated with greater probabilities of winning. The graphs show the proportion of conditioned stimuli choices across trials of CSB and HV for Sexual outcomes (left) and Monetary outcomes (right). *Group-by-Valence interaction: p < 0.05.CC BY · PubMed Central
Fig. 2 Relationship between choice preferences and attentional bias across groups. The left graph shows early attentional bias scores for sexual versus neutral stimuli (higher scores indicated greater bias towards sexual versus neutral stimuli) in subjects who preferred the CS+Sex as compared to CS− as the first choice across both groups. *p < 0.05. The right graph shows early attentional bias scores for sexual versus neutral stimuli in subjects who preferred the novel sexual stimulus as compared to the familiar stimulus.
Fig. 2 Relationship between choice preferences and attentional bias across groups. The left graph shows early attentional bias scores for sexual versus neutral stimuli (higher scores indicated greater bias towards sexual versus neutral stimuli) in subjects who preferred the CS+Sex as compared to CS− as the first choice across both groups. *p < 0.05. The right graph shows early attentional bias scores for sexual versus neutral stimuli in subjects who preferred the novel sexual stimulus as compared to the familiar stimulus.CC BY · PubMed Central
Fig. 3 Conditioning imaging task and habituation. A. Imaging task. During conditioning, subjects viewed six colored patterns followed by a Sexual, Monetary or Neutral image. The extinction phase followed, during which the conditioned stimulus was shown without the unconditioned stimulus. B. Habituation. Habituation of dorsal anterior cingulate (dACC) activity in compulsive sexual behavior (CSB) subjects versus healthy volunteers (HV) to repeated Sexual versus Neutral images. The image shows the comparison of the first and last half of the trials. C. Slope and intercept of dACC habituation. The graphs show the slope or degree of habituation (left graph) of beta values of the dACC in CSB and HV individuals and the intercept or initial activity of CSB versus HV (right graph) of Sexual – Neutral (Sex) and Monetary – Neutral (Money) images. *Valence and Group-by-Valence effects p < 0.05; **Valence effect p < 0.05.
Fig. 3 Conditioning imaging task and habituation. A. Imaging task. During conditioning, subjects viewed six colored patterns followed by a Sexual, Monetary or Neutral image. The extinction phase followed, during which the conditioned stimulus was shown without the unconditioned stimulus. B. Habituation. Habituation of dorsal anterior cingulate (dACC) activity in compulsive sexual behavior (CSB) subjects versus healthy volunteers (HV) to repeated Sexual versus Neutral images. The image shows the comparison of the first and last half of the trials. C. Slope and intercept of dACC habituation. The graphs show the slope or degree of habituation (left graph) of beta values of the dACC in CSB and HV individuals and the intercept or initial activity of CSB versus HV (right graph) of Sexual – Neutral (Sex) and Monetary – Neutral (Money) images. *Valence and Group-by-Valence effects p < 0.05; **Valence effect p < 0.05.CC BY · PubMed Central
Fig. 4 Illustration of conditioning, habituation and extinction. This figure illustrates the phases of the imaging task in which the conditioned stimuli are paired with outcomes (CS+sex shown here; CS+money conditioned to monetary outcomes and CS− conditioned to neutral outcomes were randomly interspersed and are not shown) and extinction phase in which only the conditioned stimuli are shown without the outcome. Two different CS+ for each outcome type or CS− were conditioned over 20 trials per stimulus. Five different sexual images (shown here with differing colours of the female stick image) were randomly paired with the two different CS+sex and were each shown 8 times. For the habituation analysis, the change in time of these repeated outcomes was analyzed. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
Fig. 4 Illustration of conditioning, habituation and extinction. This figure illustrates the phases of the imaging task in which the conditioned stimuli are paired with outcomes (CS+sex shown here; CS+money conditioned to monetary outcomes and CS− conditioned to neutral outcomes were randomly interspersed and are not shown) and extinction phase in which only the conditioned stimuli are shown without the outcome. Two different CS+ for each outcome type or CS− were conditioned over 20 trials per stimulus. Five different sexual images (shown here with differing colours of the female stick image) were randomly paired with the two different CS+sex and were each shown 8 times. For the habituation analysis, the change in time of these repeated outcomes was analyzed. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)CC BY · PubMed Central
Fig. 5 Extinction and functional connectivity. A. Omission of outcome during extinction. Decreased right ventral striatal activity in both groups for unexpected omission of Sexual and Monetary outcomes versus Neutral outcomes during extinction (Valence effect: p < 0.05). B. Functional connectivity with repeated exposure. Psychophysiological interaction of individuals with compulsive sexual behaviours (CSB) and healthy volunteers (HV) individuals comparing early versus late exposure of sexual outcomes with a dorsal cingulate seed showing functional connectivity with right ventral striatum (left) and bilateral hippocampus (right). *p < 0.05; **p < 0.005.
Fig. 5 Extinction and functional connectivity. A. Omission of outcome during extinction. Decreased right ventral striatal activity in both groups for unexpected omission of Sexual and Monetary outcomes versus Neutral outcomes during extinction (Valence effect: p < 0.05). B. Functional connectivity with repeated exposure. Psychophysiological interaction of individuals with compulsive sexual behaviours (CSB) and healthy volunteers (HV) individuals comparing early versus late exposure of sexual outcomes with a dorsal cingulate seed showing functional connectivity with right ventral striatum (left) and bilateral hippocampus (right). *p < 0.05; **p < 0.005.CC BY · PubMed Central

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Metadata

Authors
Banca, P., Morris, L. S., Mitchell, S., Harrison, N. A., Potenza, M. N., & Voon, V.
Affiliations
  • University of Cambridge (GB)
  • Brighton and Sussex Medical School (GB)
  • Yale University (US)
Corresponding author
Voon, Valerie
ORCID
Venue
Journal of Psychiatric Research
Publisher
Elsevier BV
Published
2016-01
Volume
72
Pages
91-101
ISSN
0022-3956 (ISSN-L)
DOI
10.1016/j.jpsychires.2015.10.017
PMC
PMC4683093
OpenAlex
W2173747897
Cited by
137
References
64
Citations by year
2026: 8 · 2025: 5 · 2024: 7 · 2023: 6 · 2022: 4 · 2021: 13 · 2020: 57 · 2019: 10 · 2018: 11 · 2017: 8 · 2016: 8
FWCI
11.16
Type
journal article
Language
en
Open access
Licence
Locations
  • Journal of Psychiatric Research (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • ORCA Online Research @Cardiff (Cardiff University) (submittedVersion)
  • Apollo (University of Cambridge) (submittedVersion, cc-by)
Funders
Wellcome Trust (WT093705/Z/10/Z, 093875)
Topics
  • Social Sciences › Psychology › Clinical Psychology › Sexuality, Behavior, and Technology
  • Social Sciences › Psychology › Clinical Psychology › Gambling Behavior and Treatments
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
Keywords
compulsive sexual behavior, novelty seeking, attentional bias, sexual reward, extinction, approach behavior, sexual imagery, addiction
MeSH terms
Adult, Attention, Brain, Conditioning, Psychological, Cues, Exploratory Behavior, Habituation, Psychophysiologic, Humans, Magnetic Resonance Imaging, Male, Neuropsychological Tests, Pattern Recognition, Visual, Photic Stimulation, Reward, Sexual Behavior

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