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Kent Berridge - One of the best experts on this subject based on the ideXlab platform.
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Computational Models of Incentive-Sensitization in Addiction: Dynamic Limbic Transformation of Learning into Motivation
Computational Neuroscience of Drug Addiction, 2020Co-Authors: Jun Zhang, Kent Berridge, J. Wayne AldridgeAbstract:Incentive Salience is a motivational magnet property attributed to reward-predicting conditioned stimuli (cues). This property makes the cue and its associated unconditioned reward ‘wanted’ at that moment, and pulls an individual’s behavior towards those stimuli. The Incentive-sensitization theory of addiction posits that permanent changes in brain mesolimbic systems in drug addicts can amplify the Incentive Salience of Pavlovian drug cues to produce excessive ‘wanting’ to take drugs. Similarly, drug intoxication and natural appetite states can temporarily and dynamically amplify cue-triggered ‘wanting’, promoting binge consumption. Finally, sensitization and drug intoxication can add synergistically to produce especially strong moments of urge for reward. Here we describe a computational model of Incentive Salience that captures all these properties, and contrast it to traditional cache-based models of reinforcement and reward learning. Our motivation-based model incorporates dynamically modulated physiological brain states that change the ability of cues to elicit ‘wanting’ on the fly. These brain states include the presence of a drug of abuse and longer-term mesolimbic sensitization, both of which boost mesocorticolimbic cue-triggered signals. We have tested our model by recording neuronal activity from mesolimbic output signals for reward and Pavlovian cues in the ventral pallidum (VP), and a novel technique for analyzing neuronal firing “profile”, presents evidence in support of our dynamic motivational account of Incentive Salience.
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Evolving Concepts of Emotion and Motivation.
Frontiers in Psychology, 2018Co-Authors: Kent BerridgeAbstract:This review takes a historical perspective on concepts in the psychology of motivation and emotion, and surveys recent developments, debates and applications. Old debates over emotion have recently risen again. For example, are emotions necessarily subjective feelings? Do animals have emotions? I review evidence that emotions exist also as core psychological processes, which have objectively detectable features, and which can occur either with subjective feelings or without them. Evidence is offered also that studies of emotion in animals can give new insights into human emotions. Beyond emotion, motivation concepts also have changed over decades, and debates still continue. Motivation was once thought in terms of aversive drives, and reward was thought of in terms of drive reduction. Motivation-as-drive concepts were largely replaced by motivation-as-Incentive concepts, yet aversive drive concepts still occasionally surface in motivation neuroscience today. Among Incentive motivation concepts, Incentive Salience is a core process, mediated by brain mesocorticolimbic systems (dopamine-related systems) and sometimes called ‘wanting’ (in quotation marks), to distinguish it from cognitive forms of desire (wanting without quotation marks). Incentive Salience as ‘wanting’ is separable also from pleasure ‘liking’ for the same reward, which has important implications for several human clinical disorders. Ordinarily, Incentive Salience adds motivational urgency to cognitive desires, but ‘wanting’ and cognitive desires can dissociate in some conditions. Excessive Incentive Salience can cause addictions, in which excessive ‘wanting’ can diverge from cognitive desires. Conversely, lack of Incentive Salience may cause motivational forms of anhedonia in depression or schizophrenia, whereas a negatively-valenced form of ‘fearful Salience’ may contribute to paranoia. Finally, negative ‘fear’ and ‘disgust’ have both partial overlap but also important neural differences.
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current perspectives on Incentive Salience and applications to clinical disorders
Current opinion in behavioral sciences, 2018Co-Authors: Jeffrey J Olney, Shelley M Warlow, Erin E Naffziger, Kent BerridgeAbstract:: Affective neuroscience research has revealed that reward contains separable components of 'liking', 'wanting', and learning. Here we focus on current 'liking' and 'wanting' findings and applications to clinical disorders. 'Liking' is the hedonic impact derived from a pleasant experience, and is amplified by opioid and related signals in discrete sites located in limbic-related brain areas. 'Wanting' refers to Incentive Salience, a motivation process for reward, and is mediated by larger systems involving mesocorticolimbic dopamine. Deficits in Incentive Salience may contribute to avolitional features of depression and related disorders, whereas deficits in hedonic impact may produce true anhedonia. Excesses in Incentive Salience, on the other hand, can lead to addiction, especially when narrowly focused on a particular target. Finally, a fearful form of motivational Salience may even contribute to some paranoia symptoms of schizophrenia and related disorders.
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dorsolateral neostriatum contribution to Incentive Salience opioid or dopamine stimulation makes one reward cue more motivationally attractive than another
European Journal of Neuroscience, 2016Co-Authors: Alexandra G Difeliceantonio, Kent BerridgeAbstract:: Pavlovian cues for rewards can become attractive Incentives: approached and 'wanted' as the rewards themselves. The motivational attractiveness of a previously learned cue is not fixed, but can be dynamically amplified during re-encounter by simultaneous activation of brain limbic circuitry. Here it was reported that opioid or dopamine microinjections in the dorsolateral quadrant of the neostriatum (DLS) of rats selectively amplify attraction toward a previously learned Pavlovian cue in an individualized fashion, at the expense of a competing cue. In an autoshaping (sign-tracking vs. goal-tracking) paradigm, microinjection of the mu opioid receptor agonist (DAMGO) or dopamine indirect agonist (amphetamine) in the DLS of sign-tracker individuals selectively enhanced their sign-tracking attraction toward the reward-predictive lever cue. By contrast, DAMGO or amphetamine in the DLS of goal-trackers selectively enhanced prepotent attraction toward the reward-proximal cue of sucrose dish. Amphetamine also enhanced goal-tracking in some sign-tracker individuals (if they ever defected to the dish even once). That DLS enhancement of cue attraction was due to stronger motivation, not stronger habits, was suggested by: (i) sign-trackers flexibly followed their cue to a new location when the lever was suddenly moved after DLS DAMGO microinjection; and (ii) DAMGO in the DLS also made sign-trackers work harder on a new instrumental nose-poke response required to earn presentations of their Pavlovian lever cue (instrumental conditioned reinforcement). Altogether, the current results suggest that DLS circuitry can enhance the Incentive Salience of a Pavlovian reward cue, selectively making that cue a stronger motivational magnet.
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amphetamine induced sensitization and reward uncertainty similarly enhance Incentive Salience for conditioned cues
Behavioral Neuroscience, 2015Co-Authors: Patrick Anselme, Mike J F Robinson, Kristen Suchomel, Kent BerridgeAbstract:Amphetamine and stress can sensitize mesolimbic dopamine-related systems. In Pavlovian autoshaping, repeated exposure to uncertainty of reward prediction can enhance motivated sign-tracking or attraction to a discrete reward-predicting cue (lever-conditioned stimulus; CS), as well as produce crosssensitization to amphetamine. However, it remains unknown how amphetamine sensitization or repeated restraint stress interact with uncertainty in controlling CS Incentive Salience attribution reflected in sign-tracking. Here rats were tested in 3 successive phases. First, different groups underwent either induction of amphetamine sensitization or repeated restraint stress, or else were not sensitized or stressed as control groups (either saline injections only, or no stress or injection at all). All next received Pavlovian autoshaping training under either certainty conditions (100% CS–UCS association) or uncertainty conditions (50% CS–UCS association and uncertain reward magnitude). During training, rats were assessed for sign-tracking to the CS lever versus goal-tracking to the sucrose dish. Finally, all groups were tested for psychomotor sensitization of locomotion revealed by an amphetamine challenge. Our results confirm that reward uncertainty enhanced sign-tracking attraction toward the predictive CS lever, at the expense of goal-tracking. We also reported that amphetamine sensitization promoted sign-tracking even in rats trained under CS–UCS certainty conditions, raising them to sign-tracking levels equivalent to the uncertainty group. Combining amphetamine sensitization and uncertainty conditions did not add together to elevate sign-tracking further above the relatively high levels induced by either manipulation alone. In contrast, repeated restraint stress enhanced subsequent amphetamine-elicited locomotion, but did not enhance CS attraction.
Terry E. Robinson - One of the best experts on this subject based on the ideXlab platform.
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Incentive Salience attribution sensation seeking and novelty seeking are independent traits in a large sample of male and female heterogeneous stock rats
Scientific Reports, 2019Co-Authors: Alesa R Hughson, Terry E. Robinson, Shelly B Flagel, Leah Solberg C Woods, Aidan P Horvath, Katie Holl, Abraham A PalmerAbstract:There are a number of traits that are thought to increase susceptibility to addiction, and some of these are modeled in preclinical studies. For example, “sensation-seeking” is predictive of the initial propensity to take drugs; whereas “novelty-seeking” predicts compulsive drug-seeking behavior. In addition, the propensity to attribute Incentive Salience to reward cues can predict the propensity to approach drug cues, and reinstatement or relapse, even after relatively brief periods of drug exposure. The question addressed here is the extent to which these three ‘vulnerability factors’ are related; that is, predictive of one another. Some relationships have been reported in small samples, but here a large sample of 1,598 outbred male and female heterogeneous stock rats were screened for Pavlovian conditioned approach behavior (to obtain an index of Incentive Salience attribution; ‘sign-tracking’), and subsequently tested for sensation-seeking and novelty-seeking. Despite the large N there were no significant correlations between these traits, in either males or females. There were, however, novel relationships between multiple measures of Incentive Salience attribution and, based on these findings, we generated a new metric that captures “Incentive value”. Furthermore, there were sex differences on measures of Incentive Salience attribution and sensation-seeking behavior that were not previously apparent.
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dissociating addiction related endophenotypes Incentive Salience attribution sensation seeking and novelty seeking are independent traits in male and female heterogeneous stock rats
bioRxiv, 2018Co-Authors: Alesa R Hughson, Terry E. Robinson, Shelly B Flagel, Leah Solberg C Woods, Aidan P Horvath, Katie Holl, Abraham A PalmerAbstract:Many factors contribute to addiction vulnerability, and isolating these could aid in improving treatment outcomes. Recent studies suggest that the way individuals respond to reward cues can predict the propensity for reinstatement or relapse, even after relatively brief periods of drug exposure. Other phases of addiction have been associated with different behavioral traits. For example, sensation-seeking is predictive of the initial propensity to take drugs; whereas novelty-seeking predicts compulsive drug-seeking behavior. Here we used a large sample of ~1,600 outbred heterogeneous stock rats to determine the relationship between the propensity to attribute Incentive Salience to reward cues and these two other addiction-related traits. Male and female adult rats were screened for Pavlovian conditioned approach behavior to obtain an index of Incentive Salience attribution (sign-tracking), and subsequently tested for sensation-seeking and novelty-seeking. Despite the large N there were no significant correlations between these traits, in either males or females. There were, however, novel relationships between multiple measures of Incentive Salience attribution and, based on these findings, we generated a new metric that captures Incentive value. Furthermore, there were sex differences on measures of Incentive Salience attribution and sensation-seeking behavior that were not previously apparent.
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dynamic encoding of Incentive Salience in the ventral pallidum dependence on the form of the reward cue
eNeuro, 2018Co-Authors: Allison M Ahrens, Terry E. Robinson, Lindsay M Ferguson, Wayne J AldridgeAbstract:Abstract Some rats are especially prone to attribute Incentive Salience to a cue (conditioned stimulus, CS) paired with food reward (sign-trackers, STs), but the extent they do so varies as a function of the form of the CS. Other rats respond primarily to the predictive value of a cue (goal-trackers, GTs), regardless of its form. Sign-tracking is associated with greater cue-induced activation of mesolimbic structures than goal-tracking; however, it is unclear how the form of the CS itself influences activity in neural systems involved in Incentive Salience attribution. Thus, our goal was to determine how different cue modalities affect neural activity in the ventral pallidum (VP), which is known to encode Incentive Salience attribution, as rats performed a two-CS Pavlovian conditioned approach task in which both a lever-CS and a tone-CS predicted identical food reward. The lever-CS elicited sign-tracking in some rats (STs) and goal-tracking in others (GTs), whereas the tone-CS elicited only goal-tracking in all rats. The lever-CS elicited robust changes in neural activity (sustained tonic increases or decreases in firing) throughout the VP in STs, relative to GTs. These changes were not seen when STs were exposed to the tone-CS, and in GTs there were no differences in firing between the lever-CS and tone-CS. We conclude that neural activity throughout the VP encodes Incentive signals and is especially responsive when a cue is of a form that promotes the attribution of Incentive Salience to it, especially in predisposed individuals.
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individual variation in Incentive Salience attribution and accumbens dopamine transporter expression and function
European Journal of Neuroscience, 2016Co-Authors: Bryan F Singer, Terry E. Robinson, Vedran Lovic, Bipasha Guptaroy, Curtis J Austin, Isabella Wohl, Jillian L Seiler, Roxanne A Vaughan, Margaret E Gnegy, Brandon J AragonaAbstract:Cues (conditioned stimuli; CSs) associated with rewards can come to motivate behavior, but there is considerable individual variation in their ability to do so. For example, a lever-CS that predicts food reward becomes attractive and wanted, and elicits reward-seeking behavior, to a greater extent in some rats (‘sign-trackers’; STs) than others (‘goal-trackers’; GTs). Variation in dopamine (DA) neurotransmission in the nucleus accumbens (NAc) core is thought to contribute to such individual variation. Given that the DA transporter (DAT) exerts powerful regulation over DA signaling, we characterized the expression and function of the DAT in the accumbens of STs and GTs. STs showed greater DAT surface expression in ventral striatal synaptosomes than GTs, and ex vivo fast-scan cyclic voltammetry recordings of electrically evoked DA release confirmed enhanced DAT function in STs, as indicated by faster DA uptake, specifically in the NAc core. Consistent with this, systemic amphetamine (AMPH) produced greater inhibition of DA uptake in STs than in GTs. Furthermore, injection of AMPH directly into the NAc core enhanced lever-directed approach in STs, presumably by amplifying the Incentive value of the CS, but had no effect on goal-tracking behavior. On the other hand, there were no differences between STs and GTs in electrically-evoked DA release in slices, or in total ventral striatal DA content. We conclude that greater DAT surface expression may facilitate the attribution of Incentive Salience to discrete reward cues. Investigating this variability in animal sub-populations may help explain why some people abuse drugs while others do not.
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individual variation in the propensity to attribute Incentive Salience to a food cue influence of sex
Behavioural Brain Research, 2015Co-Authors: Kyle K Pitchers, Shelly B Flagel, Elizabeth G Odonnell, Leah Solberg C Woods, Martin Sarter, Terry E. RobinsonAbstract:Abstract There is considerable individual variation in the propensity of animals to attribute Incentive Salience to discrete reward cues, but to date most of this research has been conducted in male rats. The purpose of this study was to determine whether sex influences the propensity to attribute Incentive Salience to a food cue, using rats from two different outbred strains (Sprague-Dawley [SD] and Heterogeneous Stock [HS]). The motivational value of a food cue was assessed in two ways: (i) by the ability of the cue to elicit approach toward it and (ii) by its ability to act as a conditioned reinforcer. We found that female SD rats acquired Pavlovian conditioned approach behavior slightly faster than males, but no sex difference was detected in HS rats, and neither strain showed a sex difference in asymptotic performance of approach behavior. Moreover, female approach behavior did not differ across estrous cycle. Compared to males, females made more active responses during the test for conditioned reinforcement, although they made more inactive responses as well. We conclude that although there are small sex differences in performance on these tasks, these are probably not due to a notable sex difference in the propensity to attribute Incentive Salience to a food cue.
Joshua S Beckmann - One of the best experts on this subject based on the ideXlab platform.
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the role of glutamate signaling in Incentive Salience second by second glutamate recordings in awake sprague dawley rats
Journal of Neurochemistry, 2018Co-Authors: Seth R Batten, Francois Pomerleau, Jorge E Quintero, Greg A Gerhardt, Joshua S BeckmannAbstract:: The attribution of Incentive Salience to reward-predictive stimuli has been shown to be associated with substance abuse-like behavior such as increased drug taking. Evidence suggests that glutamate neurotransmission and sequential N-methyl-D-aspartate (NMDA) activation are involved in the attribution of Incentive Salience. Here, we further explore the role of second-by-second glutamate neurotransmission in the attribution of Incentive Salience to reward-predictive stimuli by measuring sign-tracking behavior during a Pavlovian conditioned approach procedure using ceramic-based microelectrode arrays configured for sensitive measures of extracellular glutamate in awake behaving Sprague-Dawley rats. Specifically, we show that there is an increase in extracellular glutamate levels in the prelimbic cortex (PrL) and the nucleus accumbens core (NAcC) during sign-tracking behavior to a food-predictive conditioned stimulus (CS+) compared to the presentation of a non-predictive conditioned stimulus (CS-). Furthermore, the results indicate greater increases in extracellular glutamate levels in the PrL compared to NAcC in response to the CS+, including differences in glutamate release and signal decay. Taken together, the present research suggests that there is differential glutamate signaling in the NAcC and PrL during sign-tracking behavior to a food-predictive CS+.
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nmda receptor blockade specifically impedes the acquisition of Incentive Salience attribution
Behavioural Brain Research, 2018Co-Authors: Jonathan J Chow, Joshua S BeckmannAbstract:Abstract Glutamatergic signaling plays an important role in learning and memory. Using Pavlovian conditioned approach procedures, the mechanisms that drive stimulus-reward learning and memory have been investigated. However, there are instances where reward-predictive stimuli can function beyond being solely predictive and can be attributed with “motivational value” or Incentive Salience. Using a Pavlovian conditioned approach procedure consisting of two different but equally predictive stimuli (lever vs. tone) we investigated the role NMDA receptor function has in the attribution of Incentive Salience. The results revealed that the administration of MK-801, an NMDA receptor antagonist, during acquisition of Pavlovian conditioned approach promoted goal-tracking to a lever stimulus, while control animals learned to sign-track. Moreover, within the same animals, the use of a tone stimulus elicited goal-tracking responses that were unaffected by MK-801 pretreatments. Furthermore, a lever CS that elicited sign-tracking served as a more robust conditioned reinforcer than a tone CS that elicited goal-tracking or a lever CS that elicited goal-tracking via MK-801 pretreatments. Collectively, these results demonstrate that NMDA receptor antagonism can alter the stimulus-reward relationship learned and prevent the attribution of Incentive Salience, rather than impede general learning.
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suboptimal choice in rats Incentive Salience attribution promotes maladaptive decision making
Behavioural Brain Research, 2017Co-Authors: Jonathan J Chow, Aaron P Smith, George A Wilson, Thomas R Zentall, Joshua S BeckmannAbstract:Abstract Stimuli that are more predictive of subsequent reward also function as better conditioned reinforcers. Moreover, stimuli attributed with Incentive Salience function as more robust conditioned reinforcers. Some theories have suggested that conditioned reinforcement plays an important role in promoting suboptimal choice behavior, like gambling. The present experiments examined how different stimuli, those attributed with Incentive Salience versus those without, can function in tandem with stimulus-reward predictive utility to promote maladaptive decision-making in rats. One group of rats had lights associated with goal-tracking as the reward-predictive stimuli and another had levers associated with sign-tracking as the reward-predictive stimuli. All rats were first trained on a choice procedure in which the expected value across both alternatives was equivalent but differed in their stimulus-reward predictive utility. Next, the expected value across both alternatives was systematically changed so that the alternative with greater stimulus-reward predictive utility was suboptimal in regard to primary reinforcement. The results demonstrate that in order to obtain suboptimal choice behavior, Incentive Salience alongside strong stimulus-reward predictive utility may be necessary; thus, maladaptive decision-making can be driven more by the value attributed to stimuli imbued with Incentive Salience that reliably predict a reward rather than the reward itself.
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toward isolating the role of dopamine in the acquisition of Incentive Salience attribution
Neuropharmacology, 2016Co-Authors: Jonathan J Chow, Justin R Nickell, Mahesh Darna, Joshua S BeckmannAbstract:Stimulus-reward learning has been heavily linked to the reward-prediction error learning hypothesis and dopaminergic function. However, some evidence suggests dopaminergic function may not strictly underlie reward-prediction error learning, but may be specific to Incentive Salience attribution. Utilizing a Pavlovian conditioned approach procedure consisting of two stimuli that were equally reward-predictive (both undergoing reward-prediction error learning) but functionally distinct in regard to Incentive Salience (levers that elicited sign-tracking and tones that elicited goal-tracking), we tested the differential role of D1 and D2 dopamine receptors and nucleus accumbens dopamine in the acquisition of sign- and goal-tracking behavior and their associated conditioned reinforcing value within individuals. Overall, the results revealed that both D1 and D2 inhibition disrupted performance of sign- and goal-tracking. However, D1 inhibition specifically prevented the acquisition of sign-tracking to a lever, instead promoting goal-tracking and decreasing its conditioned reinforcing value, while neither D1 nor D2 signaling was required for goal-tracking in response to a tone. Likewise, nucleus accumbens dopaminergic lesions disrupted acquisition of sign-tracking to a lever, while leaving goal-tracking in response to a tone unaffected. Collectively, these results are the first evidence of an intraindividual dissociation of dopaminergic function in Incentive Salience attribution from reward-prediction error learning, indicating that Incentive Salience, reward-prediction error, and their associated dopaminergic signaling exist within individuals and are stimulus-specific. Thus, individual differences in Incentive Salience attribution may be reflective of a differential balance in dopaminergic function that may bias toward the attribution of Incentive Salience, relative to reward-prediction error learning only.
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isolating the Incentive Salience of reward associated stimuli value choice and persistence
Learning & Memory, 2015Co-Authors: Joshua S Beckmann, Jonathan J ChowAbstract:: Sign- and goal-tracking are differentially associated with drug abuse-related behavior. Recently, it has been hypothesized that sign- and goal-tracking behavior are mediated by different neurobehavioral valuation systems, including differential Incentive Salience attribution. Herein, we used different conditioned stimuli to preferentially elicit different response types to study the different Incentive valuation characteristics of stimuli associated with sign- and goal-tracking within individuals. The results demonstrate that all stimuli used were equally effective conditioned stimuli; however, only a lever stimulus associated with sign-tracking behavior served as a robust conditioned reinforcer and was preferred over a tone associated with goal-tracking. Moreover, the Incentive value attributed to the lever stimulus was capable of promoting suboptimal choice, leading to a significant reduction in reinforcers (food) earned. Furthermore, sign-tracking to a lever was more persistent than goal-tracking to a tone under omission and extinction contingencies. Finally, a conditional discrimination procedure demonstrated that sign-tracking to a lever and goal-tracking to a tone were dependent on learned stimulus-reinforcer relations. Collectively, these results suggest that the different neurobehavioral valuation processes proposed to govern sign- and goal-tracking behavior are independent but parallel processes within individuals. Examining these systems within individuals will provide a better understanding of how one system comes to dominate stimulus-reward learning, thus leading to the differential role these systems play in abuse-related behavior.
Shelly B Flagel - One of the best experts on this subject based on the ideXlab platform.
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the lateral hypothalamus and orexinergic transmission in the paraventricular thalamus promote the attribution of Incentive Salience to reward associated cues
bioRxiv, 2020Co-Authors: Joshua L Haight, Jonathan D Morrow, Paolo Campus, Cristina E Mariarios, Allison M Johnson, Marin S Klumpner, Brittany N Kuhn, Ignacio R Covelo, Shelly B FlagelAbstract:Rationale: Prior research suggests that inputs from the lateral hypothalamic area (LHA) to the paraventricular nucleus of the thalamus (PVT) contribute to the attribution of Incentive Salience to Pavlovian-conditioned reward cues. However, a causal role for the LHA in this phenomenon has not been demonstrated. In addition, it is unknown which hypothalamic neurotransmitter or peptide system(s) are involved in mediating Incentive Salience attribution. Objectives: To examine: 1) the role of the LHA in the propensity to attribute Incentive Salience to reward cues, and 2) the role of orexinergic signaling in the PVT on the expression of Pavlovian conditioned approach (PavCA) behavior, a reflection of Incentive Salience attribution. Methods: Male Sprague-Dawley rats received bilateral excitotoxic lesions of the LHA prior to the acquisition of Pavlovian conditioned approach (PavCA) behavior. A separate cohort of male rats acquired PavCA behavior and were characterized as sign-trackers (STs) or goal-trackers (GTs) based on their conditioned response. The orexin 1 receptor (OX1r) antagonist SB-334867, or the orexin 2 receptor (OX2r) antagonist TCS-OX2-29, were then administered directly into the PVT to assess the effects of these pharmacological agents on the expression of PavCA behavior and on the conditioned reinforcing properties of the Pavlovian reward cue. Results: Lesions of the LHA before training attenuated the development of lever-directed (sign-tracking) behaviors in the PavCA paradigm, without affecting magazine-directed (goal-tracking) behaviors. Administration of the OX1r antagonist into the PVT reduced lever-directed behaviors and increased magazine-directed behaviors in STs; while administration of the OX2r antagonist only reduced lever-directed behaviors. Further, OX2r, but not OX1r, antagonism was able to reduce the Incentive motivational value of the conditioned stimulus on a conditioned reinforcement test in STs. The behavior of GTs was unaffected by orexinergic antagonism in the PVT. Conclusions: The LHA is necessary for the attribution of Incentive Salience to reward cues and, thereby, the development of a sign-tracking conditioned response. Furthermore, blockade of orexin signaling in the PVT attenuates the Incentive value of a Pavlovian reward cue. These data suggest that hypothalamic orexin inputs to the PVT are a key component of the circuitry that encodes the Incentive motivational value of reward cues and promotes maladaptive cue-driven behaviors.
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Incentive Salience attribution sensation seeking and novelty seeking are independent traits in a large sample of male and female heterogeneous stock rats
Scientific Reports, 2019Co-Authors: Alesa R Hughson, Terry E. Robinson, Shelly B Flagel, Leah Solberg C Woods, Aidan P Horvath, Katie Holl, Abraham A PalmerAbstract:There are a number of traits that are thought to increase susceptibility to addiction, and some of these are modeled in preclinical studies. For example, “sensation-seeking” is predictive of the initial propensity to take drugs; whereas “novelty-seeking” predicts compulsive drug-seeking behavior. In addition, the propensity to attribute Incentive Salience to reward cues can predict the propensity to approach drug cues, and reinstatement or relapse, even after relatively brief periods of drug exposure. The question addressed here is the extent to which these three ‘vulnerability factors’ are related; that is, predictive of one another. Some relationships have been reported in small samples, but here a large sample of 1,598 outbred male and female heterogeneous stock rats were screened for Pavlovian conditioned approach behavior (to obtain an index of Incentive Salience attribution; ‘sign-tracking’), and subsequently tested for sensation-seeking and novelty-seeking. Despite the large N there were no significant correlations between these traits, in either males or females. There were, however, novel relationships between multiple measures of Incentive Salience attribution and, based on these findings, we generated a new metric that captures “Incentive value”. Furthermore, there were sex differences on measures of Incentive Salience attribution and sensation-seeking behavior that were not previously apparent.
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dissociating addiction related endophenotypes Incentive Salience attribution sensation seeking and novelty seeking are independent traits in male and female heterogeneous stock rats
bioRxiv, 2018Co-Authors: Alesa R Hughson, Terry E. Robinson, Shelly B Flagel, Leah Solberg C Woods, Aidan P Horvath, Katie Holl, Abraham A PalmerAbstract:Many factors contribute to addiction vulnerability, and isolating these could aid in improving treatment outcomes. Recent studies suggest that the way individuals respond to reward cues can predict the propensity for reinstatement or relapse, even after relatively brief periods of drug exposure. Other phases of addiction have been associated with different behavioral traits. For example, sensation-seeking is predictive of the initial propensity to take drugs; whereas novelty-seeking predicts compulsive drug-seeking behavior. Here we used a large sample of ~1,600 outbred heterogeneous stock rats to determine the relationship between the propensity to attribute Incentive Salience to reward cues and these two other addiction-related traits. Male and female adult rats were screened for Pavlovian conditioned approach behavior to obtain an index of Incentive Salience attribution (sign-tracking), and subsequently tested for sensation-seeking and novelty-seeking. Despite the large N there were no significant correlations between these traits, in either males or females. There were, however, novel relationships between multiple measures of Incentive Salience attribution and, based on these findings, we generated a new metric that captures Incentive value. Furthermore, there were sex differences on measures of Incentive Salience attribution and sensation-seeking behavior that were not previously apparent.
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a food predictive cue attributed with Incentive Salience engages subcortical afferents and efferents of the paraventricular nucleus of the thalamus
Neuroscience, 2017Co-Authors: Joshua L Haight, Zachary L Fuller, Kurt M Fraser, Shelly B FlagelAbstract:Abstract The paraventricular nucleus of the thalamus (PVT) has been implicated in behavioral responses to reward-associated cues. However, the precise role of the PVT in these behaviors has been difficult to ascertain since Pavlovian-conditioned cues can act as both predictive and Incentive stimuli. The “sign-tracker/goal-tracker” rat model has allowed us to further elucidate the role of the PVT in cue-motivated behaviors, identifying this structure as a critical component of the neural circuitry underlying individual variation in the propensity to attribute Incentive Salience to reward cues. The current study assessed differences in the engagement of specific PVT afferents and efferents in response to presentation of a food-cue that had been attributed with only predictive value or with both predictive and Incentive value. The retrograde tracer fluorogold (FG) was injected into the PVT or the nucleus accumbens (NAc) of rats, and cue-induced c-Fos in FG-labeled cells was quantified. Presentation of a predictive stimulus that had been attributed with Incentive value elicited c-Fos in PVT afferents from the lateral hypothalamus, medial amygdala (MeA), and the prelimbic cortex (PrL), as well as posterior PVT efferents to the NAc. PVT afferents from the PrL also showed elevated c-Fos levels following presentation of a predictive stimulus alone. Thus, presentation of an Incentive stimulus results in engagement of subcortical brain regions; supporting a role for the hypothalamic–thalamic–striatal axis, as well as the MeA, in mediating responses to Incentive stimuli; whereas activity in the PrL to PVT pathway appears to play a role in processing the predictive qualities of reward-paired stimuli.
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individual variation in the propensity to attribute Incentive Salience to a food cue influence of sex
Behavioural Brain Research, 2015Co-Authors: Kyle K Pitchers, Shelly B Flagel, Elizabeth G Odonnell, Leah Solberg C Woods, Martin Sarter, Terry E. RobinsonAbstract:Abstract There is considerable individual variation in the propensity of animals to attribute Incentive Salience to discrete reward cues, but to date most of this research has been conducted in male rats. The purpose of this study was to determine whether sex influences the propensity to attribute Incentive Salience to a food cue, using rats from two different outbred strains (Sprague-Dawley [SD] and Heterogeneous Stock [HS]). The motivational value of a food cue was assessed in two ways: (i) by the ability of the cue to elicit approach toward it and (ii) by its ability to act as a conditioned reinforcer. We found that female SD rats acquired Pavlovian conditioned approach behavior slightly faster than males, but no sex difference was detected in HS rats, and neither strain showed a sex difference in asymptotic performance of approach behavior. Moreover, female approach behavior did not differ across estrous cycle. Compared to males, females made more active responses during the test for conditioned reinforcement, although they made more inactive responses as well. We conclude that although there are small sex differences in performance on these tasks, these are probably not due to a notable sex difference in the propensity to attribute Incentive Salience to a food cue.
Mike J F Robinson - One of the best experts on this subject based on the ideXlab platform.
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amphetamine induced sensitization and reward uncertainty similarly enhance Incentive Salience for conditioned cues
Behavioral Neuroscience, 2015Co-Authors: Patrick Anselme, Mike J F Robinson, Kristen Suchomel, Kent BerridgeAbstract:Amphetamine and stress can sensitize mesolimbic dopamine-related systems. In Pavlovian autoshaping, repeated exposure to uncertainty of reward prediction can enhance motivated sign-tracking or attraction to a discrete reward-predicting cue (lever-conditioned stimulus; CS), as well as produce crosssensitization to amphetamine. However, it remains unknown how amphetamine sensitization or repeated restraint stress interact with uncertainty in controlling CS Incentive Salience attribution reflected in sign-tracking. Here rats were tested in 3 successive phases. First, different groups underwent either induction of amphetamine sensitization or repeated restraint stress, or else were not sensitized or stressed as control groups (either saline injections only, or no stress or injection at all). All next received Pavlovian autoshaping training under either certainty conditions (100% CS–UCS association) or uncertainty conditions (50% CS–UCS association and uncertain reward magnitude). During training, rats were assessed for sign-tracking to the CS lever versus goal-tracking to the sucrose dish. Finally, all groups were tested for psychomotor sensitization of locomotion revealed by an amphetamine challenge. Our results confirm that reward uncertainty enhanced sign-tracking attraction toward the predictive CS lever, at the expense of goal-tracking. We also reported that amphetamine sensitization promoted sign-tracking even in rats trained under CS–UCS certainty conditions, raising them to sign-tracking levels equivalent to the uncertainty group. Combining amphetamine sensitization and uncertainty conditions did not add together to elevate sign-tracking further above the relatively high levels induced by either manipulation alone. In contrast, repeated restraint stress enhanced subsequent amphetamine-elicited locomotion, but did not enhance CS attraction.
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initial uncertainty in pavlovian reward prediction persistently elevates Incentive Salience and extends sign tracking to normally unattractive cues
Behavioural Brain Research, 2014Co-Authors: Patrick Anselme, Mike J F Robinson, Adam M Fischer, Kent BerridgeAbstract:Uncertainty is a component of many gambling games and may play a role in Incentive motivation and cue attraction. Uncertainty can increase the attractiveness for predictors of reward in the Pavlovian procedure of autoshaping, visible as enhanced sign-tracking (or approach and nibbles) by rats of a metal lever whose sudden appearance acts as a conditioned stimulus (CS+) to predict sucrose pellets as an unconditioned stimulus (UCS). Here we examined how reward uncertainty might enhance Incentive Salience as sign-tracking both in intensity and by broadening the range of attractive CS+s. We also examined whether initially-induced uncertainty enhancements of CS+ attraction can endure beyond uncertainty itself, and persist even when Pavlovian prediction becomes 100% certain. Our results show that uncertainty can broaden Incentive Salience attribution to make CS cues attractive that would otherwise not be (either because they are too distal from reward or too risky to normally attract sign-tracking). In addition, uncertainty enhancement of CS+ Incentive Salience, once induced by initial exposure, persisted even when Pavlovian CS-UCS correlations later rose toward 100% certainty in prediction. Persistence suggests an enduring Incentive motivation enhancement potentially relevant to gambling, which in some ways resembles Incentive-sensitization. Higher motivation to uncertain CS+s leads to more potent attraction to these cues when they predict the delivery of uncertain rewards. In humans, those cues might possibly include the sights and sounds associated with gambling, which contribute a major component of the play immersion experienced by problematic gamblers.
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reward uncertainty enhances Incentive Salience attribution as sign tracking
Behavioural Brain Research, 2013Co-Authors: Patrick Anselme, Mike J F Robinson, Kent BerridgeAbstract:Abstract Conditioned stimuli (CSs) come to act as motivational magnets following repeated association with unconditioned stimuli (UCSs) such as sucrose rewards. By traditional views, the more reliably predictive a Pavlovian CS–UCS association, the more the CS becomes attractive. However, in some cases, less predictability might equal more motivation. Here we examined the effect of introducing uncertainty in CS–UCS association on CS strength as an attractive motivation magnet. In the present study, Experiment 1 assessed the effects of Pavlovian predictability versus uncertainty about reward probability and/or reward magnitude on the acquisition and expression of sign-tracking (ST) and goal-tracking (GT) responses in an autoshaping procedure. Results suggested that uncertainty produced strongest Incentive Salience expressed as sign-tracking. Experiment 2 examined whether a within-individual temporal shift from certainty to uncertainty conditions could produce a stronger CS motivational magnet when uncertainty began, and found that sign-tracking still increased after the shift. Overall, our results support earlier reports that ST responses become more pronounced in the presence of uncertainty regarding CS–UCS associations, especially when uncertainty combines both probability and magnitude. These results suggest that Pavlovian uncertainty, although diluting predictability, is still able to enhance the Incentive motivational power of particular CSs.
