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Visual sexual stimuli – cue or reward? A perspective for interpretation of recent and future brain imaging findings on human sexual behaviors.

Authors:
  • University of California, San Diego / Polish Academy of Sciences, Warsaw
  • Institute of Psychology, Polish Academy of Sciences

Abstract and Figures

There is an increasing number of neuroimaging studies using visual sexual stimuli (VSS), especially within the emerging field of research on compulsive sexual behaviors (CSB). A central question in this field is whether behaviors such as excessive pornography consumption share common brain mechanisms with widely studied substance and behavioral addictions. Depending on how VSS are conceptualized, different predictions can be formulated within the frameworks of Reinforcement Learning or Incentive Salience Theory, where a crucial distinction is made between conditioned and unconditioned stimuli (related to reward anticipation vs. reward consumption, respectively). Surveying 40 recent human neuroimaging studies we show existing ambiguity about the conceptualization of VSS. Therefore, we feel that it is important to address the question of whether VSS should be considered as conditioned stimuli (cue) or unconditioned stimuli (reward). Here we present our own perspective, which is that in most laboratory settings VSS play a role of reward, as evidenced by: (1) experience of pleasure while watching VSS, possibly accompanied by genital reaction; (2) reward-related brain activity correlated with these pleasurable feelings in response to VSS; (3) a willingness to exert effort to view VSS similarly as for other rewarding stimuli such as money; and (4) conditioning for cues predictive of VSS. We hope that this perspective article will initiate a scientific discussion on this important and overlooked topic and increase attention for appropriate interpretations of results of human neuroimaging studies using VSS.
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PERSPECTIVE
published: xx August 2016
doi: 10.3389/fnhum.2016.00402
Visual Sexual Stimuli—Cue or
Reward? A Perspective for
Interpreting Brain Imaging Findings
on Human Sexual Behaviors
Mateusz Gola1,2*, Małgorzata Wordecha 2,3 ,Artur Marchewka3and Guillaume Sescousse4
1Swartz Center for Computational Neuroscience, Institute for Neural Computations, University of California San Diego,
San Diego, CA, USA, 2Institute of Psychology, Polish Academy of Sciences, Warsaw, Poland, 3Laboratory of Brain Imaging,
Neurobiology Center, Nencki Institute of Experimental Biology of Polish Academy of Sciences, Warsaw, Poland, 4Donders
Institute for Brain, Cognition and Behavior, Radboud University, Nijmegen, Netherlands
Edited by:
Mikhail Lebedev,
Duke University, USA
Reviewed by:
Rudolf Stark,
University of Giessen, Germany
Tim Klucken,
University of Giessen, Germany
Janniko Georgiadis,
University Medical Center Groningen,
Netherlands
Shane W. Kraus,
Department of Veterans Affairs and
University of Massachusetts, USA
*Correspondence:
Mateusz Gola
mgola@ucsd.edu
Received: 27 April 2016
Accepted: 26 July 2016
Published: xx August 2016
Citation:
Gola M, Wordecha M, Marchewka A
and Sescousse G (2016) Visual
Sexual Stimuli—Cue or Reward? A
Perspective for Interpreting Brain
Imaging Findings on Human Sexual
Behaviors.
Front. Hum. Neurosci. 10:402.
doi: 10.3389/fnhum.2016.00402
There is an increasing number of neuroimaging studies using visual sexual stimuli (VSS),
especially within the emerging field of research on compulsive sexual behaviors (CSB).
A central question in this field is whether behaviors such as excessive pornography
consumption share common brain mechanisms with widely studied substance and
behavioral addictions. Depending on how VSS are conceptualized, different predictions
can be formulated within the frameworks of Reinforcement Learning or Incentive Salience
Theory, where a crucial distinction is made between conditioned and unconditioned
stimuli (related to reward anticipation vs. reward consumption, respectively). Surveying
40 recent human neuroimaging studies we show existing ambiguity about the
conceptualization of VSS. Therefore, we feel that it is important to address the question
of whether VSS should be considered as conditioned stimuli (cue) or unconditioned
stimuli (reward). Here we present our own perspective, which is that in most laboratory
settings VSS play a role of reward, as evidenced by: (1) experience of pleasure while
watching VSS, possibly accompanied by genital reaction; (2) reward-related brain activity
correlated with these pleasurable feelings in response to VSS; (3) a willingness to
exert effort to view VSS similarly as for other rewarding stimuli such as money; and
(4) conditioning for cues predictive of VSS. We hope that this perspective article will
initiate a scientific discussion on this important and overlooked topic and increase
attention for appropriate interpretations of results of human neuroimaging studies
using VSS.
Keywords: visual sexual stimuli, neuroimaging, compulsive sexual behaviors, behavioral addictions, incentive
salience, reinforcement learning, sexual behavior
There is an increasing number of neuroimaging studies using visual sexual stimuli (VSS,
Figure 1A). VSS are often used as pleasant, arousing stimuli that have an intrinsic
positive value (see Wierzba et al., 2015). Brain reactivity triggered by VSS is often
interpreted within popular theoretical frameworks describing learning processes or
motivated behavior such as Reinforcement Learning (Sutton and Barto, 1998; Botvinick
et al., 2009) or Incentive Salience Theory (Robinson and Berridge, 1993; Berridge, 2012).
Importantly, these theories make a key distinction between conditioned stimuli (CS) and
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Gola et al. Visual Sexual Stimuli—Cue or Reward?
FIGURE 1 | (A) Blue bars indicate the number of human studies using neuroscience methods (fMRI, EEG, ERP, PET, MEG or TMS) and visual sexual stimuli (VSS)
published between 2000 and 2016 according to PubMed (accessed on March 31st 2016). Red bars indicate the number of neuroscience studies on compulsive
sexual behaviors (CSB): 1 in 2013 (Steele et al., 2013), 2 in 2014 (Kühn and Gallinat, 2014; Voon et al., 2014), 1 in 2015 (Prause et al., 2015), and 3 in 2016 (Banca
et al., 2016; Brand et al., 2016; Klucken et al., 2016). (B) Number of studies published between 2013 and 2016 interpreting VSS as cue, reward or none of these
labels (unspecified). Note that in Oei et al. (2014) VSS were defined both as “reward cues” and “rewarding stimuli”, so it was counted in both categories “Cue” and
”Reward”.
unconditioned stimuli (UCS), which are related to reward
anticipation/wanting vs. reward consumption/liking,
respectively. Accordingly, it is important to make explicit
whether VSS play a role of CS or UCS, i.e., whether they are
incentive cues predicting an upcoming reward, or whether
they are rewarding by themselves. This issue has been
surprisingly overlooked in past studies, despite its important
implications. We reviewed 40 human studies published
between 2013 and 2016, using VSS in combination with
neuroscience methods (fMRI, EEG, ERP, PET, MEG or TMS;
Figure 1B):
Nine studies described VSS as cues/CS: (Minnix et al., 2013;
Politis et al., 2013; Steele et al., 2013; Kühn and Gallinat, 2014;
Oei et al., 2014; Voon et al., 2014; Wetherill et al., 2014; Prause
et al., 2015; Seok and Sohn, 2015).
Sixteen studies described VSS as rewards/UCS: (Costumero
et al., 2013, 2015a,b; Graf et al., 2013; Klucken et al., 2013, 2015,
2016; Sescousse et al., 2013a; Cassidy et al., 2014; Li et al., 2014;
Mascaro et al., 2014; Oei et al., 2014; Lee et al., 2015; Banca
et al., 2016; Brand et al., 2016; Schöne et al., 2016).
One study described VSS as both as CS and UCS: (Oei et al.,
2014).
Fifteen studies did not use any such labels: (Abler et al.,
2013; Chung et al., 2013; Habermeyer et al., 2013; Hernández-
González et al., 2013; Sylva et al., 2013; Wehrum et al., 2013;
Borg et al., 2014; Prause et al., 2014; Kim and Jeong, 2013, 2014;
Wehrum-Osinsky et al., 2014; Flaisch et al., 2015; Amezcua-
Gutiérrez et al., 2016; Kim et al., 2016; Knott et al., 2016).
The Incentive Salience Theory framework, proposed by
Robinson and Berridge (1993), distinguishes two basic
components of motivated behavior—‘‘wanting’’ and ‘‘liking’’.
The latter is directly linked to the experienced value of the
reward (UCS), while the former is related to the expected value
of the reward, often carried by a predictive cue (CS). Studies on
substance and gambling addiction show that learned cues (CS)
related to addiction evoke increased responses in the ventral
striatum as well as increased motivated behavior (i.e., shorter
reaction times, higher accuracy) among addicted individuals,
while responses to the reward itself remain unchanged or
undergo blunting over time (Berridge, 2012; Robinson et al.,
2015).
Thus, the conceptualization of VSS as cues or rewards
in experimental designs is not just a semantic debate,
because it has important consequences for the interpretation
of neuroimaging results. One important consequence is on
the emerging field of neuroscientific research on compulsive
sexual behaviors (CSB; Love et al., 2015; Kraus et al.,
2016a,b;Figure 1). A central question in this field is whether
CSBs (such as excessive pornography consumption Gola
et al., 2016a,b) share common brain mechanisms with widely
studied substance and behavioral addictions (Love et al., 2015;
Gola and Potenza, 2016; Gola et al., 2016c; Kraus et al.,
2016b). Depending on how VSS are conceptualized, different
predictions can be formulated. If one assumes that VSS
play a role of cue, then increased ventral striatal reactivity
among subjects with CSB (in comparison with controls)
would speak in favor of the addiction hypothesis, while
under the assumption that VSS play a role of reward, it is
the opposite result (decreased ventral striatal reactivity) that
would speak in favor of the same hypothesis. Therefore we
feel that it is important to address the question of whether
VSS should be considered as cues (CS) or rewards (UCS)
in human studies. Here we present our own perspective,
hoping that it will initiate a scientific discussion on this
topic.
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Gola et al. Visual Sexual Stimuli—Cue or Reward?
To answer this question we think it is important to distinguish
the meaning of VSS in real life vs. in the laboratory setting
(Figure 2). In many real life situations, VSS such as the naked
body of a sexually attractive partner increase sexual arousal and
lead to approach behaviors initializing dyadic sexual activity
and ending with orgasm (Georgiadis and Kringelbach, 2012;
Gola et al., 2015a). In this case, we argue that VSS play a
role of cue (CS), while orgasm plays the role of (primary)
reward (UCS). The reasoning is similar in most cases of solitary
sexual activity. Most common VSS are pornographic videos or
photos (cue/CS), which increase sexual arousal, and lead to
masturbation ending with orgasm (reward/UCS). In contrast,
during laboratory experiments, subjects are usually not allowed
to initiate any sexual activity (such as masturbation) and natural
UCS—orgasm—is unavailable. Even if subjects would be allowed
to masturbate during the study, laboratory conditions are far less
comfortable than the usual context of pornography consumption
or dyadic sexual activity. Thus, individuals participating in
laboratory experiments do not expect any other reward than
being exposed to VSS. Therefore, we posit that in laboratory
setting VSS play a role of reward (UCS; Figure 2). The
conceptualization of VSS as rewards in the context of laboratory
experiments comes with several predictions. Among healthy
subjects we should observe: (1) experience of pleasure while
watching VSS, possibly accompanied by genital reaction; (2)
reward-related brain activity correlated with these pleasurable
feelings in response to VSS; (3) a willingness to exert effort to
view VSS similarly as for other rewarding stimuli such as money;
and (4) conditioning of cues (CS) predictive of VSS. Below we
review evidence supporting these predictions.
In studies collecting hedonic ratings of VSS, subjects
consistently report that watching VSS is a subjectively pleasurable
experience when these match the subjects’ sexual preferences
(Chivers and Bailey, 2005; Rupp and Wallen, 2009; Jacob
et al., 2011; Wierzba et al., 2015). In addition, these hedonic
ratings have been shown to be accompanied by genital reactions
as measured by penile plethysmography in male participants
(Stoléru et al., 1999; Redouté et al., 2000; Ferretti et al., 2005).
FIGURE 2 | According to our perspective, in most real life situations (such as sexual activity with partner or solitary pornography consumption) visual
sexual stimuli (VSS; such as naked body of a sexually attractive partner or pornographic content) play a role of cue (CS). VSS increase sexual arousal
and lead to behaviors initializing dyadic or solitary sexual activity and ending with reward—i.e., orgasm (UCS). In contrast, in most laboratory settings sexual activity
and orgasm are unavailable. We claim that VSS then play a role of reward (UCS), similarly to some real life situations such as the visit to a strip club. In such contexts,
individuals do not expect any other reward than being exposed to VSS, and are willing to exert effort or pay money to receive desired VSS, while being susceptible to
conditioning for cues predictive of these VSS. For the purpose of illustration of our ideas this figure presents a simplified representation of real life where other
scenarios of VSS use are possible, i.e., pornography consumption may lead to dyadic sexual activity or vice versa. Credits of sample photos: Lies Thru a Lens; Strip
club in Montreal, Quebec, in Saint Henri borough; Lola Bel Aire, striptease from Miss Exotic World 2008, CC BY 2.0. For license terms see: CC BY 2.0
(https://creativecommons.org/licenses/by/2.0/).
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Gola et al. Visual Sexual Stimuli—Cue or Reward?
Erectile reaction among males takes some time so it is easier
to observe it with long-lasting VSS such as videos or long
presentations of pictures (Ferretti et al., 2005), however even
brief presentations of static sexual photographies are related with
subjective pleasure and arousal (Ferretti et al., 2005; Wierzba
et al., 2015).
Many studies have shown that passive VSS viewing evokes
ventral striatum activity (Arnow et al., 2002; Stark et al., 2005;
Sabatinelli et al., 2007; Demos et al., 2012; Georgiadis and
Kringelbach, 2012; Stoléru et al., 2012; Wehrum-Osinsky et al.,
2014). It is difficult to assess whether striatal activity reflects cue
related wanting or reward related liking in these studies given
that the ventral striatum is known to respond to both appetitive
cues (CS) and rewards (UCS; Flagel et al., 2011; Liu et al., 2011)
However, the observed correlation between striatal activity and
hedonic ratings triggered by VSS in various studies (Walter et al.,
2008; Sescousse et al., 2010, 2013b) favors the hypothesis that VSS
act like rewarding stimuli. In this respect, VSS play a similar role
as monetary rewards: they activate similar brain areas including
the ventral striatum, and trigger comparable hedonic reactions
and motivated behaviors (Sescousse et al., 2010, 2013b, 2015).
The main difference is that VSS are primary rewards (i.e., they
have an intrinsic and innate reward value), whereas money is a
secondary reward (whose value is learned by exchange against
other rewards). This difference leads to a partially different
mapping onto the brain reward system, and different strengths
of activation (Sescousse et al., 2010, 2013b, 2015).
Even though most studies using VSS have used passive
viewing paradigms, a few investigations have employed more
advanced experimental designs aiming to measure participants’
willingness to exert effort towards VSS. In a series of studies, we
have used a modified version of the monetary incentive delay
task (Knutson et al., 2001) to include VSS (Sescousse et al., 2010,
2013a, 2015; Gola et al., 2015b, 2016c). In this task subjects see
two types of cues that are predictive of either VSS or monetary
gains. These cues are followed by a discrimination task in which
subjects have to press the correct button (out of two) within a
time limit of 1 s. The receipt of a monetary gain or VSS is partly
dependent on their performance on this task, such that reaction
times can be interpreted as an indirect measure of the motivation
to obtain these rewards. Importantly, cues predicting VSS elicit
similar reaction times as those predicting monetary rewards,
demonstrating that participants are willing to exert effort to
view VSS, and that their motivation is similar for both rewards
(Sescousse et al., 2010). This willingness to exert effort, which is
a hallmark of reward (Thorndike, 1965), has been observed in
other studies using effort (but also delay) discounting paradigms
with VSS (Prévost et al., 2010). In addition, we have shown that
individual differences in the effort exerted for money vs. VSS
is strongly correlated with the relative brain activity evoked by
corresponding cues in the ventral striatum (Sescousse et al., 2015;
Gola et al., 2016c). This precise fine-tuning of brain activity and
reaction times by VSS predicting cues further confirms that VSS
have intrinsically rewarding properties.
Finally, recent studies have shown that abstract CS (such as
colorful patterns or dots) associated with VSS maintain their
incentive salience even when they are not predictive of VSS
anymore (Banca et al., 2016; Klucken et al., 2016). In the study
by Banca et al. (2016), abstract visual patterns acquired positive
predictive value (CS+) or neutral predictive value (CS) by being
repetitively paired with VSS or neutral stimuli, respectively. In
the following phase of the experiment, subjects had to make
choices between those CS and novel abstract stimuli, while
both CS were now paired with increased chances of monetary
gains (but not VSS anymore). Despite both CS having equal
chances of leading to monetary gains, CS+ were chosen more
frequently than CSon average (mostly by subjects with CSB),
demonstrating the strong rewarding properties of VSS.
As we have shown above, there is a consistent body of
evidence supporting our view that in laboratory settings VSS play
a role of reward rather than cue. Moreover, even in everyday
life VSS do not always play a role of cue for sexual activity
and orgasm. Long before the development of photography
people have liked art such as sculptures and paintings depicting
nudity. Perhaps (similarly to modern times) this type of art
was a source of pleasure rather than cue for sexual activity.
In the era of photography people showed willingness to pay
for pictures and videos with erotic and pornographic content,
then internet technology provided everyone with easy and free
access to a whole variety of VSS (Cooper, 1998). Perhaps most
of contemporary VSS (such as internet pornography) play a role
of cue for solitary or dyadic sexual activity, but in some cases
VSS are sought after for themselves, again demonstrating their
intrinsic rewarding value. A good example in everyday life are
calendars with erotic pictures, that people buy and expose in their
workplace or at home. Similarly, the popularity of strip clubs,
in which people are willing to pay to watch nude dancers with
whom they are not allowed to engage in sexual activity, illustrate
the potency of VSS as hedonic stimuli (Figure 2).
Based on the above arguments, we argue that VSS play a
role of reward—rather than cue—in most experimental setups
in which sexual activity and climax experience are unavailable.
As we outlined above, viewing VSS is a pleasurable experience
that people are willing to work and wait for (Prévost et al., 2010),
and activates the same brain reward regions as monetary gains
(Sescousse et al., 2010, 2013a, 2015; Gola et al., 2015b, 2016c).
Moreover neutral stimuli associated with VSS through Pavlovian
conditioning acquire incentive value (Sescousse et al., 2010,
2013a, 2015; Banca et al., 2016; Gola et al., 2016c; Klucken et al.,
2016). This conceptualization of VSS as rewards rather than cues
calls for the re-examination—and possibly re-interpretation—of
the results reported in earlier studies defining VSS as cues.
Certainly it may have a strong impact on the interpretation of
neuroimaging studies investigating neurobiological similarities
between CSB and addiction; for instance, based on the popular
Incentive Salience Theory framework, one would expect opposite
ventral striatal reactivity for VSS depending on whether they
are conceptualized as a cue or reward (as an example of such
ambiguous interpretation see: Prause et al., 2015, 2016; see also
Gola, 2016 for discussion). If in most of experimental setups, as
we argue, VSS play a role of reward, then diminished (rather
than increased) ventral striatal reactivity to VSS in individuals
with problematic pornography use (Gola et al., 2016a) would
speak in favor of the addiction hypothesis (Robinson et al., 2015).
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We would expect this to be accompanied by increased ventral
striatum activations for CS that are predictive of VSS, as well
as increased effort or shorter reaction times to gain access to
these VSS. In future studies, we hope that the role played by
VSS in the specific protocols that are used will receive increased
attention, and that appropriate interpretations of results will be
made accordingly.
ADDITIONAL INFORMATION
Method of Study Selection
We searched the Pubmed database from 2000 to 2016 to
identify neuroscience publications (key words: fMRI, EEG, ERP,
PET, MEG or TMS) with VSS (keywords: VSS, sexual stimuli,
erotic stimuli, sexual pictures, erotic pictures, sexual images,
erotic images, sexual videos, erotic videos). Only full peer-
reviewed publications were selected (no conference abstracts).
For studies published between 2013 (year of first publication
on problematic pornography use) and 2016 we categorized
them into three categories depending on whether VSS were
described as: (1) ‘‘cue/CS’’; (2) "reward/rewarding stimuli/UCS’’;
and (3) otherwise.
Related Issues
Here we want to highlight several issues which, if properly
investigated, may provide valuable information in the debate on
the interpretation of studies using VSS and help to extend the
significance of future research.
One of the crucial points is to examine the difference in
behavioral and neural responding when VSS are used as cues
vs. rewards. It could be done by comparing two experimental
conditions in which VSS play a role of reward (most of current
experimental settings) or cue (settings allowing subjects to climax
during or after the study).
Another interesting hypothesis is that behavior and brain
activaty elicited by VSS in typical experimental settings may
partly reflect inhibitory control. This inhibitory control may be
removed at the end of the experiment, after which subjects may
start seeking sexual encounters or initiate solitary sexual activity.
For instance, an old behavioral study by Brown et al. (1976)
has shown that among heterosexual males, VSS viewing in the
laboratory induced masturbation in 24.5% of the subjects on the
day of the experiment, while on other days only 12.5% of them
engaged in masturbation. This observation suggests that for a
fraction of the subjects, watching VSS in the laboratory may have
been a cue eliciting sexual motivation that had to be inhibited.
To examine such a possibility it would be important to control
for sexual activity following experimental studies. Furthermore
it raises several questions: does this subgroup differ from other
participants, i.e., in terms of sexual arousability (Gola et al.,
2015a)? And if so, than does it affect brain activity?
We hope that these questions will inspire investigators and
will be addressed in future studies.
AUTHOR CONTRIBUTIONS
All authors discussed the idea. MG prepared figures. MW and
MG did a review of literature. MG and GS wrote the manuscript.
AM and MW commented on the manuscript.
FUNDING
MG was supported by Opus grant from National Science
Centre in Poland (2014/15/B/HS6/03792; MG) and scholarship
of Ministry of Science and Higher Education of Republic of
Poland (469/STYP/10/2015); MW was supported by Opus grant
from National Science Centre in Poland (2014/15/B/HS6/03792;
MG); GS was supported by a Veni grant from the Netherlands
Research Organization (NWO, ref no. 016.155.218).
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Conflict of Interest Statement: The authors declare that the research was
conducted in the absence of any commercial or financial relationships that could
be construed as a potential conflict of interest.
Copyright © 2016 Gola, Wordecha, Marchewka and Sescousse. This is an open-
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... Only one study found conflicting results in a sample of the general population (Kühn & Gallinat, 2014). These findings could be interpreted as signs of brain responses comparable to addiction; however, for sexual stimuli it is unclear whether these are cues or rewards (Gola, Lewczuk, & Skorko, 2016;Gola, Wordecha, Marchewka, & Sescousse, 2016). Watching sexual stimuli can be seen as an unconditioned reward, especially for those who experience and report high sexual desire toward these stimuli. ...
... Interpretation of functional brain imaging data is dependent on this conceptualization of cue vs reward, with data interpreted as supporting or contradicting the addiction hypothesis. Some experts have therefore called for a "reexamination-and possibly reinterpretation-of the results" reported in earlier functional neuroimaging studies that assess cue-reactivity in response to visual sexual stimuli (Gola, Wordecha, et al., 2016). ...
Chapter
The present chapter addresses the many faces of cybersex and describes the mental health challenges of various sexual activities using new technologies. This includes a range of sexual behaviors, from Internet use to sex with robots. In many cases, cybersex use is not problematic and not associated with personal distress or functional impairment. However, in those cases where people lose control over their cybersexual behavior or harm others we discuss diagnostic criteria as well as differential diagnoses and ways to evaluate the given behavior. The chapter also addresses the current state of research regarding the psychobiology as well as pharmacological and psychotherapeutic treatment options of cybersexual behaviors that are associated with mental health issues.
... Why would erotic cues affect learning and decision-making? Erotic cues robustly activate neural structures including ventral striatum and orbitofrontal cortex that receive catecholaminergic projections from midbrain nuclei (Gola et al., 2016;Stark et al., 2005;Wehrum-Osinsky et al., 2014). Via this route, primary reinforcers such as erotic cues are assumed to promote immediate out-of-domain reward preferences (Li, 2008;Yeomans & Grace, 2015) and thus might also promote habitual (model-free) over goal-directed (modelbased) control of behavior. ...
... Why would erotic cues affect learning and decision-making? Erotic cues robustly activate neural structures including ventral striatum and orbitofrontal cortex that receive catecholaminergic projections from midbrain nuclei (Gola et al., 2016;Stark et al., 2005;Wehrum-Osinsky et al., 2014). Via this route, primary reinforcers such as erotic cues are assumed to promote immediate out-of-domain reward preferences (Li, 2008;Yeomans & Grace, 2015) and thus might also promote habitual (model-free) over goal-directed (modelbased) control of behavior. ...
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Computational psychiatry focuses on identifying core cognitive processes that appear altered across a broad range of psychiatric disorders. Temporal discounting of future rewards and model-based control during reinforcement learning have proven as two promising candidates. Despite its trait-like stability, temporal discounting has been suggested to be at least partly under contextual control. For example, highly arousing cues such as erotic pictures were shown to increase discounting, although overall evidence to date remains somewhat mixed. Whether model-based reinforcement learning is similarly affected by arousing cues is unclear. Here we tested cue-reactivity effects (erotic pictures) on subsequent temporal discounting and model-based reinforcement learning in a within-subjects design in n=39 healthy male participants. Self-reported and physiological arousal (cardiac activity and pupil dilation) were assessed before and during cue exposure. Arousal was increased during exposure of erotic vs. neutral cues both on the subjective and autonomic level. Erotic cue exposure nominally increased discounting as reflected by reduced choices of delayed options. Hierarchical drift diffusion modeling (DDM) linked increased discounting to a shift in the starting point bias of evidence accumulation towards immediate options. Model-based control during reinforcement learning was reduced following erotic cues according to model-agnostic analysis. Notably, DDM linked this effect to attenuated forgetting rates of unchosen options, leaving the model-based control parameter unchanged. Our findings replicate previous work on cue-reactivity effects in temporal discounting and for the first time show similar effects in model-based reinforcement learning. Our results highlight how environmental cues can impact core human decision processes and reveal that comprehensive drift diffusion modeling approaches can yield novel insights in reward-based decision processes.
... Among its conceptualisations, problematic Internet pornography use has been defined as a form of obsessive-compulsive disorder (Cooper, Delmonico, Griffin-Shelley, & Mathy, 2004;Young, 2005), as a symptom of hypersexual disorder (Reid, Li, Gilliland, Stein, & Fong, 2011), as a behavioural addiction (Griffiths, 2001;Meerkerk, Van Den Eijnden, & Garretsen, 2006), and, more recently, as a specific Internet-use disorder (Brand, Young, Laier, Wölfling, & Potenza, 2016). Notably, a wide array of evidence (e.g., Brand et al., 2016;Elmquist, Shorey, Anderson, & Stuart, 2016;Gola, Wordecha, Marchewka, & Sescousse, 2016;Love, Laier, Brand, Hatch, & Hajela, 2015;Walsh et al., 2020) shows similarities between problematic Internet pornography use and substance use disorders or other behavioural addictions in terms of neurobiological, cognitive, and behavioural mechanisms. These include the compulsion to achieve a specific desired target, the perception of losing control, the repetitive implementation of maladaptive behaviours despite awareness of the negative consequences, and craving (Brand et al., 2011;Laier, Pawlikowski, Pekal, Schulte, & Brand, 2013;Skinner & Aubin, 2010;Tiffany & Wray, 2012). ...
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Introduction According to the recent adaptation of the I-PACE model, desire thinking and craving might be closely related to problematic Internet pornography use. The overall aim of the present study was to investigate the role of two components of desire thinking (imaginal prefiguration and verbal perseveration) and craving in problematic Internet pornography use. Furthermore, we examined gender differences in the underlying mechanism linking desire thinking to problematic Internet pornography use. Method A total of 414 Italian adults (mean age = 27.55 years, SD = 6.13; age range= 18 – 58; 53.6% men) participated in this study. Participants completed an online survey to assess problematic Internet pornography use, pornography craving, desire thinking and problematic Internet use. Path analyses and a multi-group approach were used to test the relationships among variables and to explore gender differences. Results Imaginal prefiguration was associated to pornography craving which, in turn, was associated to verbal perseveration as proximal antecedent of problematic Internet pornography use, above and beyond the effect of age, relationship status, and problematic Internet use. Two paths significantly differed between men and women: the path between verbal perseveration and problematic Internet pornography, which for women was weaker and did not reach significance; and the path between problematic Internet use and problematic Internet pornography use that was not significant for women. Conclusions In line with the I-PACE model, the present study provided support for the potential role of desire thinking in problematic Internet pornography use as a specific Internet-use disorder and expanded the literature in the field by testing unexplored gender differences. Preventive and clinical implications are discussed.
... widok kobiety w bikini) są zarówno nagrodą pierwotną (jak u zdrowych jednostek), jak i wtórną. Podczas gdy u osób z zaburzeniem grania w gry hazardowe wskazówki związane z graniem (głównie pieniądze) są i nagrodą wtórną (jak u zdrowych jednostek), i pierwotną (Gola, Wordecha, Marchewka i Sescousse, 2016). Oznacza to, że u osób z danym zaburzeniem przedmioty (zwane wskazówkami) z nim związane stają się pierwotną oraz wtórną nagrodą. ...
... behavior was a subjectively pleasurable experience and activity which, in the putamen, could be triggered by visual sexual stimuli, which acted like rewarding stimuli (53)(54)(55). In previous neuroimaging studies, activation in the putamen was found to be associated with male sexual arousal and penile turgidity (56, 57). ...
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Introduction Type 2 diabetes mellitus (T2DM) has been found to be associated with abnormalities of the central and peripheral vascular nervous system, which were considered to be involved in the development of cognitive impairments and erectile dysfunction (ED). In addition, altered brain function and structure were identified in patients with ED, especially psychological ED (pED). However, the similarities and the differences of the central neural mechanisms underlying pED and T2DM with ED (DM-ED) remained unclear. Methods Diffusion tensor imaging data were acquired from 30 T2DM, 32 ED, and 31 DM-ED patients and 47 healthy controls (HCs). Then, whole-brain structural networks were constructed, which were mapped by connectivity matrices (90 × 90) representing the white matter between 90 brain regions parcellated by the anatomical automatic labeling template. Finally, the method of network-based statistic (NBS) was applied to assess the group differences of the structural connectivity. Results Our NBS analysis demonstrated three subnetworks with reduced structural connectivity in DM, pED, and DM-ED patients when compared to HCs, which were predominantly located in the prefrontal and subcortical areas. Compared with DM patients, DM-ED patients had an impaired subnetwork with increased structural connectivity, which were primarily located in the parietal regions. Compared with pED patients, an altered subnetwork with increased structural connectivity was identified in DM-ED patients, which were mainly located in the prefrontal and cingulate areas. Conclusion These findings highlighted that the reduced structural connections in the prefrontal and subcortical areas were similar mechanisms to those associated with pED and DM-ED. However, different connectivity patterns were found between pED and DM-ED, and the increased connectivity in the frontal–parietal network might be due to the compensation mechanisms that were devoted to improving erectile function.
... Within this framework, we here sought to test further the hypothesis that interindividual differences in concerns beyond purely homeostatic needs modulate Pavlovian and instrumental learning along with their influence on reward-seeking behaviors by using sexual stimuli as rewarding outcomes. Sexual stimuli exert strong effects on human behavior (e.g., Gola et al., 2016;Sennwald et al., 2016Sennwald et al., , 2020, rendering them a powerful tool to investigate human reward processing. More importantly, although sexual reward processing relies on some shared neurobiological and psychological mechanisms with food reward processing (Toates, 2014), they differ in some aspects, with sexual rewards being generally relevant to more complex concerns than primarily physiological ones (e.g., Georgiadis & Kringelbach, 2012). ...
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Pavlovian and instrumental conditioning are fundamental processes helping organisms learn about stimuli that predict rewards in the environment and actions that lead to their obtainment. These two forms of learning and their interplay notably exert a strong impact on reward-seeking behaviors. Here, we examined in humans whether Pavlovian and instrumental learning along with their effects on cue-driven behaviors involving sexual rewards are modulated by the reward relevance to the individual’s sexual orientation. In two experiments, we manipulated the concern-relevance of sexual outcomes in a Pavlovian-instrumental transfer paradigm by recruiting heterosexual and homosexual men and selecting sexual stimuli for each sexual orientation. Results showed enhanced instrumental and Pavlovian learning in response to the most relevant sexual outcome to participants’ sexual orientation as well as increased reward-seeking behaviors in response to its associated cue compared to the less relevant sexual outcome and its associated cue, respectively, thereby reflecting that inter-individual differences in sexual concerns modulated these effects. These findings suggest that motivational influence on reward-related learning and behaviors involving sexual stimuli relies on inter-individual differences in concerns and contribute to fostering further insight into the mechanisms underlying human reward-seeking behaviors.
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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.
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Background: Hypersexual behaviours could reflect psychopathology, in part, because they impair interactions with intimate partners. Methods: Hypersexual concerns were measured as: (1) concern about inability to control one's own sexual behaviours; and (2) sexual films viewed. The outcome, sexual arousal, was measured using two indicators: (1) self-reported sexual arousal (before/after); and (2) skin conductance response from the person stimulated (continuously). Two-hundred and fifty participants completed Orgasmic Meditation (OM), a coupled, structured, 15-min manual-genital stroking. Results: Reported difficulty controlling their own sexual behaviours was not related to sexual arousal reports. Participants who viewed more sexual films reported more sexual arousal before starting OM than participants who viewed less sexual films. Strokers who viewed more sexual films were associated with a higher skin conductance response in the stroked partner. Conclusions: Despite statistical power and pre-registration, hypersexual concerns did not predict sexual responses with a partner. Sex film viewing may increase sexual responsiveness in individuals and their partners.
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Humans and many animals devalue future rewards as a function of time (temporal discounting). Increased discounting has been linked to various psychiatric conditions, including substance-use-disorders, behavioral addictions, and obesity. Despite its high intra-individual stability, temporal discounting is partly under contextual control. One prominent manipulation that has been linked to increases in discounting is the exposure to highly arousing appetitive cues. However, results from trial-wise cue exposure studies appear highly mixed, and changes in physiological arousal were not adequately controlled. Here we tested the effects of appetitive (erotic), aversive, and neutral visual cues on temporal discounting in 35 healthy male participants. The contribution of single-trial physiological arousal was assessed using comprehensive monitoring of autonomic activity (pupil size, heart rate, electrodermal activity). Physiological arousal was elevated following aversive and in particular erotic cues. In contrast to our pre-registered hypothesis, steepness of temporal discounting was not significantly affected by emotional cues of either valence. Aversive cues tended to increase decision noise. Computational modeling revealed that trial-wise arousal only accounted for minor variance over and above aversive and erotic condition effects, arguing against a general effect of physiological arousal on temporal discounting.
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Pornography consumption is highly prevalent, particularly among young adult males. For some individuals, problematic pornography use (PPU) is a reason for seeking treatment. Despite the pervasiveness of pornography, PPU appears under-investigated, including with respect to the underlying neural mechanisms. Using functional magnetic resonance imaging (fMRI), we examined ventral striatal responses to erotic and monetary stimuli, disentangling cue-related ‘wanting’ from reward-related ‘liking’ among 28 heterosexual males seeking treatment for PPU and 24 heterosexual males without PPU. Subjects engaged in an incentive delay task in the scanner, in which they received erotic or monetary rewards preceded by predictive cues. BOLD responses to erotic and monetary cues were analyzed and examined with respect to self-reported data on sexual activity collected over the 2 preceding months. Men with and without PPU differed in their striatal responses to cues predicting erotic pictures, but not in their responses to erotic pictures. PPU subjects when compared to control subjects showed increased activation of ventral striatum specifically for cues predicting erotic pictures but not for cues predicting monetary gains. Relative sensitivity to cues predicting erotic pictures versus monetary gains was significantly related to the increased behavioral motivation to view erotic images (suggestive of higher ‘wanting’), severity of PPU, amount of pornography use per week and number of weekly masturbations. Our findings suggest that, similar to what is observed in substance and gambling addictions, the neural and behavioral mechanisms associated with the anticipatory processing of cues specifically predicting erotic rewards relate importantly to clinically relevant features of PPU. These findings suggest that PPU may represent a behavioral addiction and that interventions helpful in targeting behavioral and substance addictions warrant consideration for adaptation and use in helping men with PPU.
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Pornography consumption is highly prevalent, particularly among young adult males. For some individuals, problematic pornography use (PPU) is a reason for seeking treatment. Despite the pervasiveness of pornography, PPU appears under-investigated, including with respect to the underlying neural mechanisms. Using functional magnetic resonance imaging (fMRI), we examined ventral striatal responses to erotic and monetary stimuli, disentangling cue-related ‘wanting’ from reward-related ‘liking’ among 28 heterosexual males seeking treatment for PPU and 24 heterosexual males without PPU. Subjects engaged in an incentive delay task in the scanner, in which they received erotic or monetary rewards preceded by predictive cues. BOLD responses to erotic and monetary cues were analyzed and examined with respect to self-reported data on sexual activity collected over the 2 preceding months. Men with and without PPU differed in their striatal responses to cues predicting erotic pictures, but not in their responses to erotic pictures. PPU subjects when compared to control subjects showed increased activation of ventral striatum specifically for cues predicting erotic pictures but not for cues predicting monetary gains. Relative sensitivity to cues predicting erotic pictures versus monetary gains was significantly related to the increased behavioral motivation to view erotic images (suggestive of higher ‘wanting’), severity of PPU, amount of pornography use per week and number of weekly masturbations. Our findings suggest that, similar to what is observed in substance and gambling addictions, the neural and behavioral mechanisms associated with the anticipatory processing of cues specifically predicting erotic rewards relate importantly to clinically relevant features of PPU. These findings suggest that PPU may represent a behavioral addiction and that interventions helpful in targeting behavioral and substance addictions warrant consideration for adaptation and use in helping men with PPU.
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Background How best to conceptualize problematic pornography use (PPU) and intervene most effectively remain debated, with obsessive–compulsive disorder (OCD) and addiction frameworks. We investigated the efficacy of the serotonin-reuptake inhibitor paroxetine in combination with cognitive-behavioral therapy in the treatment of problematic pornography use (PPU). Case presentation Three heterosexual males with PPU were treated with cognitive-behavioral therapy and paroxetine. Frequency of pornography use, other sexual behaviors, and anxiety were assessed during treatment. Discussion Paroxetine treatment, although seemingly initially effective in reducing pornography use and anxiety, appeared related to new compulsive sexual behaviors after 3 months. Conclusions Paroxetine may hold promise for short-term reduction of PPU and related anxiety, but new potentially distressing sexual behaviors may emerge. The cases suggest that PPU may arise from multiple domains. We propose an explanation of the effects based on recent neuroscientific research on sexual behaviors and alcohol use.
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Introduction: Pornography has become popular with Internet technology. For most people, pornography use (PU) is entertainment; for some, it can result in seeking treatment for out-of-control behavior. Previous studies have suggested that PU can influence sexual behaviors, but the direct relation between frequency of PU and treatment-seeking behaviors has not been examined. Aims: To investigate whether individuals seeking treatment as a consequence of their problematic PU do so because of their quantity of pornography consumption or because of more complex psychological and behavioral factors related to PU, such as the severity of negative symptoms associated with PU and/or subjective feeling of loss of control over one's behavior. Methods: A survey study was conducted of 569 heterosexual Caucasian men 18 to 68 years old, including 132 seeking treatment for problematic PU (referred by psychotherapists after their initial visit). Main outcomes measures: The main outcome measures were self-reported PU, its negative symptoms, and actual treatment-seeking behavior. Results: We tested models explaining sources of seeking treatment for problematic PU with negative symptoms associated with PU and additional factors (eg, onset and number of years of PU, religiosity, age, dyadic sexual activity, and relationship status). Seeking treatment was significantly, yet weakly, correlated solely with the frequency of PU (r = 0.21, P < .05) and this relation was significantly mediated by negative symptoms associated with PU (strong, nearly full mediation effect size; k(2) = 0.266). The relation between PU and negative symptoms was significant and mediated by self-reported subjective religiosity (weak, partial mediation; k(2) = 0.066) in those not seeking treatment. Onset of PU and age appeared to be insignificant. Our model was fairly fitted (comparative fit index = 0.989; root mean square error of approximation = 0.06; standardized root mean square residual = 0.035) and explained 43% of the variance in treatment-seeking behavior (1% was explained by frequency of PU and 42% was explained by negative symptoms associated with PU). Conclusion: Negative symptoms associated with PU more strongly predict seeking treatment than mere quantity of pornography consumption. Thus, treatment of problematic PU should address qualitative factors, rather than merely mitigating the frequency of the behavior, because frequency of PU might not be a core issue for all patients. Future diagnostic criteria for problematic PU should consider the complexity of this issue.
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Objectives: Addictive sexual behaviours are gaining more and more attention from researchers. There are actually 25 different questionnaires for assessing the level of loss of control over sexual. The main aim of this work was to make such an adaptation of the Sexual Addiction Screening Test-Revised (SAST-R; the most popular and questionnaire). behaviours (LoCoSB). None of them have been adapted and validated in a Polish language version. Methods: For the purpose of psychometric features examination and validation of the Polish version of SAST-R (SAST-PL-M), we recruited 116 heterosexual men receiving psychological treatment due to LoCoSB and meeting the criteria for hypersexual disorder. The control group consisted of 442 heterosexual males having never looked for any psychological or psychiatric help due to LoCoSB. Results: SAST-PL-M has high reliability (Cronbach's alpha = 0.904) and good filtering characteristics for identification of people who are potentially experiencing difficulty with control over sexual behaviours (the ROC curve for a threshold of 5 out of a maximum 20 points is characterised by a sensitivity of 99.1% and a specificity of 78.3%). Conclusions: SAST-PL-M can be used as an efficient screening test for symptoms of LoCoSB in clinical and research setups. Results below 5 points indicate a high probability of no problems, while more than 5 points can indicate the need for additional clinical interviews. SAST-PL-M results may be successfully referred to the results of SAST-R when used with heterosexual male populations for research purposes.
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Introduction: There has been growing interest in a better understanding of the etiology of compulsive sexual behavior (CSB). It is assumed that facilitated appetitive conditioning might be an important mechanism for the development and maintenance of CSB, but no study thus far has investigated these processes. Aim: To explore group differences in neural activity associated with appetitive conditioning and connectivity in subjects with CSB and a healthy control group. Methods: Two groups (20 subjects with CSB and 20 controls) were exposed to an appetitive conditioning paradigm during a functional magnetic resonance imaging experiment, in which a neutral stimulus (CS+) predicted visual sexual stimuli and a second stimulus (CS-) did not. Main outcome measures: Blood oxygen level-dependent responses and psychophysiologic interaction. Results: As a main result, we found increased amygdala activity during appetitive conditioning for the CS+ vs the CS- and decreased coupling between the ventral striatum and prefrontal cortex in the CSB vs control group. Conclusion: The findings show that neural correlates of appetitive conditioning and neural connectivity are altered in patients with CSB. The increased amygdala activation might reflect facilitated conditioning processes in patients with CSB. In addition, the observed decreased coupling could be interpreted as a marker for impaired emotion regulation success in this group.
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Sexual arousal affects cognitive processing, which depends on the coordinated functioning among cortical areas. The aim of this research was to determine whether previous observation of videos with sexual content affects the degree of cortical electroencephalographic (EEG) coupling during performance of an executive task. Cortical EEG correlations were calculated in three groups of heterosexual men under three conditions: at rest; during observation of a video with neutral, aggressive, or erotic content; and while performing the Tower of Hanoi task (TOH). Based on self-reports, it was shown that the erotic video induced general and sexual arousal, while the aggressive video affected valence and general arousal. Task performance was similar in all three groups. During performance of TOH, only the erotic group showed a decreased correlation between prefrontal areas with an increased correlation between parietal and prefrontotemporal areas, specifically in the slow bands. It is likely that these changes in the degree of cortical coupling could be associated with the cognitive strategies or functional adaptations that participants require to adequately solve the task during a state of sexual arousal. These data could contribute to improving our understanding of the central nervous mechanisms that underlie the effect of sexual arousal on the cognitive processes involved in tasks like TOH.
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One type of Internet addiction is excessive pornography consumption, also referred to as cybersex or Internet pornography addiction. Neuroimaging studies found ventral striatum activity when participants watched explicit sexual stimuli compared to non-explicit sexual/erotic material. We now hypothesized that the ventral striatum should respond to preferred pornographic compared to non-preferred pornographic pictures and that the ventral striatum activity in this contrast should be correlated with subjective symptoms of Internet pornography addiction. We studied 19 heterosexual male participants with a picture paradigm including preferred and non-preferred pornographic material. Subjects had to evaluate each picture with respect to arousal, unpleasantness, and closeness to ideal. Pictures from the preferred category were rated as more arousing, less unpleasant, and closer to ideal. Ventral striatum response was stronger for the preferred condition compared to non-preferred pictures. Ventral striatum activity in this contrast was correlated with the self-reported symptoms of Internet pornography addiction. The subjective symptom severity was also the only significant predictor in a regression analysis with ventral striatum response as dependent variable and subjective symptoms of Internet pornography addiction, general sexual excitability, hypersexual behavior, depression, interpersonal sensitivity, and sexual behavior in the last days as predictors. The results support the role for the ventral striatum in processing reward anticipation and gratification linked to subjectively preferred pornographic material. Mechanisms for reward anticipation in ventral striatum may contribute to a neural explanation of why individuals with certain preferences and sexual fantasies are at-risk for losing their control over Internet pornography consumption.