Conditioned appetitive stimulus increases extracellular dopamine in the nucleus accumbens of the rat

This study used in vivo microdialysis to examine the release of dopamine (DA) in the nucleus accumbens (nAc) during the performance of a previously learned, signalled sucrose reward task, and during conditioning of a neutral tone stimulus to this reward. Behavioural measures (magazine entries) confirmed that stimuli associated with sucrose presentation became secondary rewarding stimuli, and DA release was also monitored during subsequent presentation of these stimuli alone. Perhaps surprisingly, during magazine entry for consumption of sucrose, i.e. in conditions similar to routine training, dialysate DA levels in the nAc did not increase. In contrast, during conditioning of the tone with light-sucrose, dopamine levels increased consistently and significantly. Interestingly, DA levels were somewhat, but significantly, increased when tone alone was presented in a test session, i.e. two hours after conditioning, and even more so when tone was combined with the light previously associated with sucrose. In this latter case the number of magazine entries increased to a level similar to that seen during conditioning. Presentation of light alone resulted in a similar level of magazine entries to tone alone, but no significant increase in DA. In summary, these studies confirm that a neutral stimulus can acquire the behavioural properties of reward when conditioned. The neurochemical data, on the other hand, suggest that increases of DA in nAc are more likely to be related to new associative learning than to established incentive or consumatory processes. The increase in DA release in the test session may be related either to the secondary reinforcing properties acquired by the stimulus, or to the change in contingencies, or to the aversive effects of the omission of reward.     

Effects of ventral striatal lesions on first‐ and second‐order appetitive conditioning

Rats with bilateral lesions of the ventral striatal nucleus accumbens failed to acquire Pavlovian second‐order conditioning to auditory stimuli paired with visual stimuli that had previously received first‐order pairings with food. This deficit in second‐order conditioning was specific to learning driven by incentive properties of the first‐order cues, and was observed whether the first‐order training had occurred prior to or after lesion surgery. Lesions also produced deficits in the display of conditioned responses to the first‐order conditioned stimulus, but only when they were made after first‐order training. These results suggest a specific role for the ventral striatum in acquiring and expressing incentive properties of conditioned stimuli through second‐order conditioning, as well as a more general role in expressing previously acquired Pavlovian conditioned responses.     

On-line psychophysical data acquisition and event-related fMRI protocol optimized for the investigation of brain activation in response to gustatory stimuli

An experimental method for event-related functional magnetic resonance imaging that allows for the presentation of several chemosensory stimuli in the oral cavity during the same run, the collection of psychophysical measures (intensity or pleasantness) during the presentation of the stimuli, and the analysis of the data in an event-related fashion are described. The automatic pumps used to present taste stimuli allowed for multiple tastes to be delivered in small amounts under computer control. Psychophysical ratings of pleasantness or intensity were collected after each presentation of a taste stimulus and water, with the general labeled magnitude scale, using a joystick that controlled the movement of an arrow on the visual display. Performing these cognitive tasks required that the participant remained focused, and aided in the interpretation of the data collected. The perceived pleasantness differed across stimuli for all conditions; however, pleasantness ratings for the same stimulus displayed consistency, over the duration of the run and before each scan on separate days. Activation in response to sucrose and caffeine while the participant rated pleasantness was found in the insula, frontal operculum, rolandic operculum and orbitofrontal cortex which is consistent with previous taste fMRI studies.     

The hippocampus and appetitive Pavlovian conditioning: effects of excitotoxic hippocampal lesions on conditioned locomotor activity and autoshaping

The hippocampus (HPC) is known to be critically involved in the formation of associations between contextual/spatial stimuli and behaviorally significant events, playing a pivotal role in learning and memory. However, increasing evidence indicates that the HPC is also essential for more basic motivational processes. The amygdala, by contrast, is important for learning about the motivational significance of discrete cues. This study investigated the effects of excitotoxic lesions of the rat HPC and the basolateral amygdala (BLA) on the acquisition of a number of appetitive behaviors known to be dependent on the formation of Pavlovian associations between a reward (food) and discrete stimuli or contexts: (1) conditioned/anticipatory locomotor activity to food delivered in a specific context and (2) autoshaping, where rats learn to show conditioned discriminated approach to a discrete visual CS+. While BLA lesions had minimal effects on conditioned locomotor activity, hippocampal lesions facilitated the development of both conditioned activity to food and autoshaping behavior, suggesting that hippocampal lesions may have increased the incentive motivational properties of food and associated conditioned stimuli, consistent with the hypothesis that the HPC is involved in inhibitory processes in appetitive conditioning.     

Orbitofrontal cortex and representation of incentive value in associative learning.

Clinical evidence indicates that damage to ventromedial prefrontal cortex disrupts goal-directed actions that are guided by motivational and emotional factors. As a consequence, patients with such damage characteristically engage in maladaptive behaviors. Other research has shown that neurons in the corresponding orbital region of prefrontal cortex in laboratory animals encode information regarding the incentive properties of goals or expected events. The present study investigates the effect of neurotoxic orbitofrontal cortex (OFC) lesions in the rat on responses that are normally influenced by associations between a conditioned stimulus (CS) and the incentive value of reinforcement. Rats were first trained to associate a visual CS with delivery of food pellets to a food cup. As a consequence of learning, rats approached the food cup during the CS in anticipation of reinforcement. In a second training phase, injection of LiCl followed consumption of the food unconditioned stimulus (US) in the home cage, a procedure used to alter the incentive value of the US. Subsequently, rats were returned to the conditioning chamber, and their responding to the CS in the absence of the food US was tested. Lesions of OFC did not affect either the initial acquisition of a conditioned response to the light CS in the first training phase or taste aversion learning in the second training phase. In the test for devaluation, however, OFC rats exhibited no change in conditioned responding to the visual CS. This outcome contrasts with the behavior of control rats; after devaluation of the US a significant decrease occurred in approach to the food cup during presentation of the CS. The results reveal an inability of a cue to access representational information about the incentive value of associated reinforcement after OFC damage.     

Psychophysiological and subjective indicators of aversive pavlovian conditioning in generalized social phobia.

Aversive conditioning has been proposed as an important etiologic mechanism in social phobia; however, empirical evidence is scarce and has not relied on a detailed analysis of the acquisition and extinction of the conditioned emotional response.Fourteen men sustaining generalized social phobia and 19 healthy control subjects participated in differential aversive conditioning with two neutral faces as conditioned stimuli and an aversive odor as unconditioned stimulus. Subjective and peripheral physiological responses were obtained.Both groups were successfully conditioned as reflected by differential subjective (valence, arousal, subjective unconditioned stimulus expectancy) and peripheral physiological responses (skin conductance, startle response). There was no evidence for an enhanced conditionability in the social phobics; however, they showed an enhanced unconditioned stimulus expectancy, especially for the nonreinforced conditioned stimuli during acquisition, and a delayed extinction of the conditioned skin conductance response as well as a certain dissociation between subjective and physiological responses.The enhanced unconditioned stimulus expectancy during acquisition and the overall elevated subjective arousal suggest that, under threat, subjects with generalized social phobia may be more prone to associate neutral social cues and an aversive outcome. Furthermore, delayed extinction of the conditioned response seems to contribute to the etiology and maintenance of generalized social phobia.     

The role of dopamine in locomotor activity and learning

The discovery that the brain contains neurons utilizing dopamine (DA) as their transmitter has led to studies of the behavioral function of these neurons. Changes in overall level of activity of DA neurons appear to produce parallel changes in locomotor activity. Additionally, DA neurons seem to mediate in part the effects of biologically significant (reinforcing) stimuli on learning. One way in which reinforcing stimuli produce learning is to increase the incentive motivational (response-eliciting) properties of neutral stimuli associated with them; also, reinforcing stimuli maintain the incentive motivational properties of previously conditioned incentive stimuli. Normal DA functioning appears to be required for the establishment and maintenance of incentive learning in naive animals. Previous incentive learning in trained animals can influence behavior for a time even when the function of DA neurons is disrupted; however, with continued testing in the absence of normal DA functioning, previously established conditioned incentive stimuli cease to influence behavior. From these observations and recent physiological, anatomical and biochemical studies of DA systems it is suggested that the biological substrate of DA-mediated incentive learning is a heterosynaptic facilitation of muscarinic cholinergic synapses. This model has important clinical implications since it has been suggested that DA hyperfunctioning underlies the development of schizophrenia.     

A selective role for right insula—basal ganglia circuits in appetitive stimulus processing

Hemispheric lateralization of hedonic evaluation (‘liking’) and incentive motivation (‘wanting’) in neural networks connecting the basal ganglia and insula (BG-I) in humans was examined. Participants with brain damage restricted to the BG-I of the right (n = 5) or left (n = 5) hemisphere, and 26 healthy participants matched on age, sex and intelligence quotient were tested on positively and negatively valenced pictures drawn from varied stimulus categories (Vijayaraghavan et al., 2008). Liking was assessed with explicit ratings of pleasantness using a nine-point Likert scale. Wanting was quantified as the amount of work (via repeated keypresses) that participants expended to increase (approach) or decrease (withdraw) viewing time. Right-lesion patients showed abnormally low viewing times and liking ratings for positive images. For a subset of positive images depicting sexual content, right-lesion patients exhibited active withdrawal, while the other two groups approached such stimuli. These results suggest that the right basal ganglia–insula complex plays a greater role than the left in supporting hedonic evaluation and motivational approach to positively valenced stimuli. The finding that active avoidance of stimuli that were not ‘liked’ was spared in both right- and left-sided lesion subjects suggests that unilateral damage to insula/basal ganglia circuits may not be sufficient to affect general incentive motivation independent of preference.     

The role of dopamine in conditioning and latent inhibition: what, when, where and how?

It is well established that dopamine is released in the nucleus accumbens (NAC) in animals in rewarding or reinforcing situations, and widely believed that this release is the substrate of, or at least closely related to, the experience of reward. The demonstration of conditioned release of dopamine by stimuli conditioned to primary rewards has reinforced this view. However, a number of observations do not sit comfortably with this interpretation, most notably that dopamine is released equally effectively in NAC by aversive stimuli, and stimuli conditioned to them. Furthermore, additional release of dopamine is seen during conditioning, even if motivational stimuli of either type are not involved. It is suggested here that one important action of NAC dopamine release is to restore the salience of potential conditioned stimuli, when this has been reduced by prior un-reinforced experience. The paradigm of latent inhibition (LI) demonstrates a behavioural effect of this type, and extensive studies on the role of dopamine in LI have been undertaken by us and others. Those studies are reviewed here, together with some previously unpublished data, to demonstrate that (1) amphetamine disruption of LI is indeed a function of calcium-dependant dopamine release in the NAC at the time of conditioning; (2) other drugs acting on LI via changes in dopamine transmission act at the same locus; (3) the disruptive effect of indirect dopamine agonists on LI can be prevented by either D-1 selective receptor antagonists, or D-2 selective receptor antagonists. It is concluded that dopamine release in these very varied behavioural contexts (reward, punishment, conditioning, modulation of salience) must be differentiated in some way, and that this should be investigated. An alternative explanation, if they are not differentiated, would be that the release in fact does have the same functional significance in each case. We suggest that this common significance might be the broadening of attention to take in potentially conditionable stimuli, which have previously been devalued.     

Single unit activity of locus coeruleus neurons in the freely moving cat: II. Conditioning and pharmacologic studies

A series of experiments were carried out in which the single unit activity of presumed noradrenergic (NE) neurons in the area of the locus coeruleus (LC) was examined in freely moving cats during two conditioning paradigms and in response to pharmacologic manipulations relevant to anxiety. LC unit activity was examined during conditioned emotional response (CER) and conditioned food reward (CFR) training. During CER training, LC units showed a large increase in activity in response to a stimulus paired with a noxious air puff, whereas no increase in unit activity was seen in response to a stimulus not paired with the air puff (both comparisons relative to their appropriate control conditions). By contrast, during CFR training, a stimulus paired with a rewarding food delivery did not elicit a significant increase in LC unit activity relative to its appropriate control condition. Therefore, NE units in the LC greatly increase their activity in response to a stimulus that predicts the occurrence of a noxious event, but not in response to a stimulus that predicts the occurrence of a rewarding event. Administration of the anxiolytic drug diazepam (0.25 and 2.0 mg/kg, i.p.) had no significant effect on the spontaneous activity of LC neurons, but significantly reduced the excitatory response of LC neurons to simple stimuli. Administration of the anxiogenic drug yohimbine (2.0 mg/kg, i.p.) significantly increased the spontaneous activity of LC neurons. These results support the hypothesis that LC neurons play a role in aversive but not appetitive conditioning, and are consistent with the hypothesis that these neurons may play a role in anxiety. These data are discussed within the broader context of LC neurons mediating the organism's adaptive response to environmental or physiological challenges.     

Haloperidol does not alter expression of ethanol-induced conditioned place preference

A recent experiment (Risinger et al., Psychopharmacology, 107 (1992) 453-456) has shown that haloperidol does not prevent acquisition of ethanol-induced conditioned place preference, suggesting that dopaminergic mechanisms do not mediate the primary rewarding properties of ethanol. The present experiment examined whether haloperidol would prevent the expression of conditioned reward to ethanol-paired stimuli using the place conditioning paradigm. DBA/2J mice received four pairings of a tactile stimulus with ethanol (2 g/kg, IP). A different stimulus was paired with saline. Before preference testing, different groups received one of three doses of haloperidol (0, 0.05 or 0.1 mg/kg); ethanol was not given. Haloperidol produced a dose-dependent decrease in locomotor activity, but did not affect conditioned place preference. These results suggest that expression of ethanol-induced conditioned place preference is mediated by non-dopaminergic mechanisms.     

Avoidance‐based human Pavlovian‐to‐instrumental transfer

The Pavlovian‐to‐instrumental transfer (PIT) paradigm probes the influence of Pavlovian cues over instrumentally learned behavior. The paradigm has been used extensively to probe basic cognitive and motivational processes in studies of animal learning. More recently, PIT and its underlying neural basis have been extended to investigations in humans. These initial neuroimaging studies of PIT have focused on the influence of appetitively conditioned stimuli on instrumental responses maintained by positive reinforcement, and highlight the involvement of the striatum. In the current study, we sought to understand the neural correlates of PIT in an aversive Pavlovian learning situation when instrumental responding was maintained through negative reinforcement. Participants exhibited specific PIT, wherein selective increases in instrumental responding to conditioned stimuli occurred when the stimulus signaled a specific aversive outcome whose omission negatively reinforced the instrumental response. Additionally, a general PIT effect was observed such that when a stimulus was associated with a different aversive outcome than was used to negatively reinforce instrumental behavior, the presence of that stimulus caused a non‐selective increase in overall instrumental responding. Both specific and general PIT behavioral effects correlated with increased activation in corticostriatal circuitry, particularly in the striatum, a region involved in cognitive and motivational processes. These results suggest that avoidance‐based PIT utilizes a similar neural mechanism to that seen with PIT in an appetitive context, which has implications for understanding mechanisms of drug‐seeking behavior during addiction and relapse.     

Evoked potential conditioning using morphine as the unconditioned stimulus in rats

It is believed that conditioning processes play an important role in the development of narcotic dependence and may be particularly responsible for relapse after treatment. In addition, it was suggested that this conditioning is reflected by altered neural responses to stimuli which were associated with drug administration. To test these hypotheses, evoked potentials were recorded from four regions of rats' brains during a differential classical conditioning procedure. The conditioned and unconditioned effects of morphine on neural responses in each of these regions were studied during both addiction and withdrawal. The conditioning procedure resulted in alterations in the cortical response to the stimulus which was associated with morphine, but no alterations occurred in the response to the differential stimulus. Furthermore, the conditioned cortical response was found to persist after withdrawal from morphine. However, possibly due to state-dependency effects, the conditioned response was expressed only when the subjects were morphine intoxicated. Thus, the conditioned neural response found in this experiment did not reflect the processes postulated to lead to relapse of drug-free addicts.     

Pleasant or Unpleasant: Attentional Modulation of Odor Perception

Using positron emission tomography, we investigated whether regional brain activations differ as a function of attending to pleasant versus unpleasant components of odors. There were two experimental (attention to pleasantness and attention to unpleasantness) and one control (baseline) condition. The stimuli presented during the two experimental conditions were exactly the same (three binary mixtures, each consisting of one pleasant and one unpleasant compound), but the affective property to which participants?? attention was directed was different: They indicated with a mouse click whether each stimulus contained a pleasant (during attention to pleasantness) or unpleasant (during attention to unpleasantness) odor. During baseline, odorless stimuli were presented, and participants pressed the mouse button randomly after each one. Several brain regions were involved in both types of attention, and these included ventral striatum, right orbitofrontal cortex, and anterior cingulate cortex. Subtle differences were also revealed: Attending to pleasantness was associated preferentially with a sensory/perceptual network (piriform cortex and amygdala), whereas attending to unpleasantness engaged a component of the attentional (right parietal) network. Thus, we delineate neural substrates of attending to olfactory pleasantness and unpleasantness, some of which are common to both and others that are specific to pleasantness or to unpleasantness. Our results suggest that the view of the mesolimbic dopaminergic system as the reward network that responds selectively to positive reinforcers is somewhat limited: Our findings are more in keeping with a view of this set of structures as the salience system of the brain.     

Deletion of α5 nicotine receptor subunits abolishes nicotinic aversive motivational effects in a manner that phenocopies dopamine receptor antagonism

Nicotine addiction is a worldwide epidemic that claims millions of lives each year. Genetic deletion of α5 nicotinic acetylcholine receptor (nAChR) subunits has been associated with increased nicotine intake, however, it remains unclear whether acute nicotine is less aversive or more rewarding, and whether mice lacking the α5 nAChR subunit can experience withdrawal from chronic nicotine. We used place conditioning and conditioned taste avoidance paradigms to examine the effect of α5 subunit‐containing nAChR deletion (α5 ?/?) on conditioned approach and avoidance behaviour in nondependent and nicotine‐dependent and ‐withdrawn mice, and compared these motivational effects with those elicited after dopamine receptor antagonism. We show that nondependent α5 ?/? mice find low, non‐motivational doses of nicotine rewarding, and do not show an aversive conditioned response or taste avoidance to higher aversive doses of nicotine. Furthermore, nicotine‐dependent α5 ?/? mice do not show a conditioned aversive motivational response to withdrawal from chronic nicotine, although they continue to exhibit a somatic withdrawal syndrome. These effects phenocopy those observed after dopamine receptor antagonism, but are not additive, suggesting that α5 nAChR subunits act in the same pathway as dopamine and are critical for the experience of nicotine's aversive, but not rewarding motivational effects in both a nondependent and nicotine‐dependent and ‐withdrawn motivational state. Genetic deletion of α5 nAChR subunits leads to a behavioural phenotype that exactly matches that observed after antagonizing dopamine receptors, thus we suggest that modulation of nicotinic receptors containing α5 subunits may modify dopaminergic signalling, suggesting novel therapeutic treatments for smoking cessation.     

Amphetamine selectively enhances avoidance responding to a less salient stimulus in rats

This preclinical study examined the psychological processes affected by amphetamine that contribute to human psychosis. Using a novel avoidance conditioning paradigm involving two conditioned stimuli (CS) with varied salience, we found that acute amphetamine (1.5 mg/kg, i.p.) selectively enhanced avoidance responding to a less salient stimulus, but not to a salient one. These findings suggest that elevated dopaminergic activity selectively enhances the attributions of motivational salience to a less salient stimulus, a process that may bear relevance to the development of human delusional thoughts.     

Dissociations in Hippocampal 5-Hydroxytryptamine Release in the Rat Following Pavlovian Aversive Conditioning to Discrete and Contextual Stimuli

The experiments examined the release of 5-hydroxytryptamine using in vivo microdialysis methods in the hippocampus of freely moving rats following Pavlovian aversive conditioning to discrete and contextual stimuli. Differential conditioning was achieved by manipulating the interval between the offset of a discrete auditory ‘clicker’stimulus and the onset of a mild foot-shock reinforcer (0.5 mA, 0.5 s). Foot-shock occurred either simultaneously with the last second of the discrete auditory stimulus (in short-trace subjects) or 60 s later (long-trace subjects). In this way, subjects were preferentially conditioned to the discrete stimulus and background ‘contextual’stimuli respectively. During conditioning subjects also received two identical unpaired visual stimuli. At test, dialysates were collected and behavioural measures taken as all animals experienced (i) the aversive and two other ‘neutral’environments, and (ii) the discrete unconditioned and conditioned stimuli presented in both aversive and neutral environments. Exposure to the aversive environment, but not to either of the two neutral environments, was associated with significantly increased hippocampal 5-hydroxytryptamine release in long-trace subjects. There was also a small but non-significant increase in 5-hydroxytryptamine release in short-trace animals. In contrast, hippocampal 5-hydroxytryptamine release was unaffected by presentation of either of the discrete stimuli under all conditions. The last result was obtained despite robust behavioural responses (freezing) to the discrete conditioned stimulus. These data do not agree with the hypothesis that aversive cues generally activate 5-hydroxytryptamine function in the hippocampus. Rather, they suggest a degree of specificity whereby 5-hydroxytryptamine release in the hippocampus was determined primarily by other qualitative properties of the conditioned aversive stimulus, namely whether the aversive cue was discrete or contextual, as well as by the magnitude of conditioning.     

The basolateral complex of the amygdala is necessary for acquisition but not expression of CS motivational value in appetitive Pavlovian second-order conditioning

The basolateral complex of the amygdala (ABL) is involved in processing information about stimulus motivational value. However, it is not clear whether the ABL is critical for acquisition, maintenance, or expression of this information. Our previous work has shown that ABL lesions made prior to training, block acquisition of an appetitive Pavlovian second-order conditioning task, in which performance is thought to depend on the acquisition of motivational (conditioned reinforcement) value by the first-order conditioned stimulus (CS). The present experiments examined the effects of ABL lesions made after first-order conditioning, when the CS acquires motivational value, but before second-order conditioning, the test for acquired value of that CS. Rats received pairings of a visual CS with a food reinforcer. They then received bilateral sham or excitotoxic lesions of the ABL. After recovery, they received pairings of a second-order auditory CS with the previously conditioned visual CS. In two experiments, both sham and lesioned rats acquired normal second-order conditioned behaviours. Some of the same rats were then given another round of second-order conditioning with novel CSs. In this case, when first-order training occurred after surgery, some second-order conditioned behaviours were impaired in lesioned rats. Tests of the associative underpinnings of second-order conditioned behaviours showed that those behaviours impaired by ABL lesions were based on stimulus-response associations. The results show that although the ABL is critical for second-order conditioning, this role is limited to acquisition of information about the motivational value of the first-order CS, and it is not critical for maintenance of this information or for its use in forming second-order associations.     

Subthalamic nucleus stimulation affects incentive salience attribution in Parkinson's disease

Deep brain stimulation (DBS) of the subthalamic nucleus (STN) can induce nonmotor side effects such as behavioral and mood disturbances or body weight gain in Parkinson's disease (PD) patients. We hypothesized that some of these problems could be related to an altered attribution of incentive salience (ie, emotional relevance) to rewarding and aversive stimuli. Twenty PD patients (all men; mean age ± SD, 58.3 ± 6 years) in bilateral STN DBS switched ON and OFF conditions and 18 matched controls rated pictures selected from the International Affective Picture System according to emotional valence (unpleasantness/pleasantness) and arousal on 2 independent visual scales ranging from 1 to 9. Eighty‐four pictures depicting primary rewarding (erotica and food) and aversive fearful (victims and threat) and neutral stimuli were selected for this study. In the STN DBS ON condition, the PD patients attributed lower valence scores to the aversive pictures compared with the OFF condition (P < .01) and compared with controls (P < .01). The difference between the OFF condition and controls was less pronounced (P < .05). Furthermore, postoperative weight gain correlated with arousal ratings from the food pictures in the STN DBS ON condition (P < .05 compensated for OFF condition). Our results suggest that STN DBS increases activation of the aversive motivational system so that more relevance is attributed to aversive fearful stimuli. In addition, STN DBS–related sensitivity to food reward stimuli cues might drive DBS‐treated patients to higher food intake and subsequent weight gain. © 2011 Movement Disorder Society     

Novelty,conditioning and attentional bias to sexual rewards

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.