Papers by J. Wayne Aldridge
The Journal of Neuroscience
eneuro
Some rats are especially prone to attribute incentive salience to a cue (conditioned stimulus, CS... more 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.
Computational Neuroscience of Drug Addiction
Incentive salience is a motivational magnet property attributed to rewardpredicting conditioned s... more Incentive salience is a motivational magnet property attributed to rewardpredicting 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 cachebased 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. Definition Box: Incentive salience: Also called 'wanting', incentive salience represents motivation for reward (UCS), and is typically triggered in anticipation by a reward-related cue (Pavlovian CS) when the cue is encountered by an individual whose brain mesocorticolimbic circuits are in a highly reactive state (determined by a modulation parameter kappa in our model). Attribution of incentive salience to the cue or reward representations make them more attractive, sought after, and likely to be consumed. Brain mesolimbic systems, especially those involving dopamine, are espe
Behav Brain Sci, 2008
Current computational models predict reward based solely on learning. Real motivation involves th... more Current computational models predict reward based solely on learning. Real motivation involves that but also more. Brain reward systems can dynamically generate incentive salience, by integrating prior learned values with even novel physiological states (e.g., natural appetites; drug-induced mesolimbic sensitization) to cause intense desires that were themselves never learned. We hope future computational models may capture this too.
Http Dx Doi Org 10 1521 Soco 2008 26 5 621, Nov 10, 2008
How do brain representations of the utility of a hedonic goal guide decisions about whether to pu... more How do brain representations of the utility of a hedonic goal guide decisions about whether to pursue it? our focus here will be on brain mechanisms of reward utility operating at particular decision moments in life. Moments such as when you encounter an image, sound, scent or other cue associated in your past with a particular reward; or perhaps just vividly imagine that cue. Such a cue can often trigger a sudden motivational urge to pursue that goal, and sometimes a decision to do so. In drug addicts trying to quit, a cue for the addicted drug might trigger urges that rise to compulsive levels of intensity, despite prior commitments to abstain, leading to the decision to relapse into taking the drug again. normal or addicted, the urge and decision may well have been lacking immediately before the cue was encountered. The decision to pursue the cued reward might never have happened if the cue had not been encountered. Why can such cues momentarily dominate decision making? The answer involves brain mesolimbic dopamine mechanisms that amplify the incentive salience of reward cues, selectively elevating decision utility to trigger "wanting" for the goal. We describe affective neuroscience studies of brain limbic generators of "wanting" that shed light on how cues trigger pursuit of their goals, both normally and even under intense conditions of irrational goal pursuit. Why can sudden encounters with cues for a reward suddenly trigger pulses of motivation to pursue that reward as a goal? This question has both psychological and neural answers, and it may be useful to consider them together. In particular we think a full psychological answer involves a particular subtype of reward utility. To help make this answer clear, we will draw on a utility taxonomy that We thank Ran R. Hassin and Timothy D. Wilson for helpful comments on an earlier version of this manuscript. Portions of this article will appear as a chapter in E.
This chapter examines brain mechanisms of reward utility operating at particular decision moments... more This chapter examines brain mechanisms of reward utility operating at particular decision moments in life-moments such as when one encounters an image, sound, scent, or other cue associated in the past with a particular reward or perhaps just when one vividly imagines that cue. Such a cue can often trigger a sudden motivational urge to pursue its reward and sometimes a decision to do so. Drawing on a utility taxonomy that distinguishes among subtypes of reward utility-predicted utility, decision utility, experienced utility, and remembered utility-it is shown how cue-triggered cravings, such as an addict's surrender to relapse, can hang on special transformations by brain mesolimbic systems of one utility subtype, namely, decision utility. The chapter focuses on a particular form of decision utility called incentive salience, a type of "wanting" for rewards that is amplifi ed by brain mesolimbic systems. Sudden peaks of intensity of incentive salience, caused by neurobiological mechanisms, can elevate the decision utility of a particular reward at the moment its cue occurs. An understanding of what happens at such moments leads to a better understanding of the mechanisms at work in decision making in general.
Oxford series in social cognition and social neuroscience, 2009
This chapter examines brain mechanisms of reward utility operating at particular decision moments... more This chapter examines brain mechanisms of reward utility operating at particular decision moments in life-moments such as when one encounters an image, sound, scent, or other cue associated in the past with a particular reward or perhaps just when one vividly imagines that cue. Such a cue can often trigger a sudden motivational urge to pursue its reward and sometimes a decision to do so. Drawing on a utility taxonomy that distinguishes among subtypes of reward utility-predicted utility, decision utility, experienced utility, and remembered utility-it is shown how cue-triggered cravings, such as an addict's surrender to relapse, can hang on special transformations by brain mesolimbic systems of one utility subtype, namely, decision utility. The chapter focuses on a particular form of decision utility called incentive salience, a type of "wanting" for rewards that is amplified by brain mesolimbic systems. Sudden peaks of intensity of incentive salience, caused by neurobi...
The Journal of neuroscience : the official journal of the Society for Neuroscience, Jan 15, 2003
What is the role of dopamine in natural rewards? A genetic mutant approach was taken to examine t... more What is the role of dopamine in natural rewards? A genetic mutant approach was taken to examine the consequences of elevated synaptic dopamine on (1) spontaneous food and water intake, (2) incentive motivation and learning to obtain a palatable sweet reward in a runway task, and (3) affective "liking" reactions elicited by the taste of sucrose. A dopamine transporter (DAT) knockdown mutation that preserves only 10% of normal DAT, and therefore causes mutant mice to have 70% elevated levels of synaptic dopamine, was used to identify dopamine effects on food intake and reward. We found that hyperdopaminergic DAT knockdown mutant mice have higher food and water intake. In a runway task, they demonstrated enhanced acquisition and greater incentive performance for a sweet reward. Hyperdopaminergic mutant mice leave the start box more quickly than wild-type mice, require fewer trials to learn, pause less often in the runway, resist distractions better, and proceed more directly ...
The Journal of neuroscience : the official journal of the Society for Neuroscience, 1998
The neostriatum controls behavioral sequencing, or action syntax, as well as simpler aspects of m... more The neostriatum controls behavioral sequencing, or action syntax, as well as simpler aspects of movement. Yet the precise nature of the neostriatums role in sequencing remains unclear. Here we used a "natural action" approach that combined electrophysiological and neuroethological techniques. We identified neostriatal neurons that code the serial order of natural movement sequences of rats. During grooming behavior, rats emit complex but highly predictable species-specific sequences of movements, termed "syntactic chains." Neuronal activity of 41% of cells in the dorsolateral and ventromedial neostriatum coded the sequential pattern of syntactic chains. Only 14% coded simple motor properties of grooming movements. Neurons fired preferentially during syntactic chains compared with similar grooming movements made in different sequential order or to behavioral resting. Sequential coding differed between the dorsolateral and ventromedial neostriatum. Neurons in the d...
The Behavior of the Laboratory Rat, 2004
Background: Excessive sequential stereotypy of behavioral patterns (sequential super-stereotypy) ... more Background: Excessive sequential stereotypy of behavioral patterns (sequential super-stereotypy) in Tourette's syndrome and obsessive compulsive disorder (OCD) is thought to involve dysfunction in nigrostriatal dopamine systems. In sequential super-stereotypy, patients become trapped in overly rigid sequential patterns of action, language, or thought. Some instinctive behavioral patterns of animals, such as the syntactic grooming chain pattern of rodents, have sufficiently complex and stereotyped serial structure to detect potential production of overlyrigid sequential patterns. A syntactic grooming chain is a fixed action pattern that serially links up to 25 grooming movements into 4 predictable phases that follow 1 syntactic rule. New mutant mouse models allow gene-based manipulation of brain function relevant to sequential patterns, but no current animal model of spontaneous OCDlike behaviors has so far been reported to exhibit sequential super-stereotypy in the sense of a whole complex serial pattern that becomes stronger and excessively rigid. Here we used a hyper-dopaminergic mutant mouse to examine whether an OCD-like behavioral sequence in animals shows sequential super-stereotypy. Knockdown mutation of the dopamine transporter gene (DAT) causes extracellular dopamine levels in the neostriatum of these adult mutant mice to rise to 170% of wild-type control levels. Results: We found that the serial pattern of this instinctive behavioral sequence becomes strengthened as an entire entity in hyper-dopaminergic mutants, and more resistant to interruption. Hyper-dopaminergic mutant mice have stronger and more rigid syntactic grooming chain patterns than wild-type control mice. Mutants showed sequential super-stereotypy in the sense of having more stereotyped and predictable syntactic grooming sequences, and were also more likely to resist disruption of the pattern en route, by returning after a disruption to complete the pattern from the appropriate point in the sequence. By contrast, wild-type mice exhibited weaker forms of the fixed action pattern, and often failed to complete the full sequence. Conclusions: Sequential super-stereotypy occurs in the complex fixed action patterns of hyper-dopaminergic mutant mice. Elucidation of the basis for sequential super-stereotypy of instinctive behavior in DAT knockdown mutant mice may offer insights into neural mechanisms of overly-rigid sequences of action or thought in human patients with disorders such as Tourette's or OCD.
Journal of Neuroscience, 2004
We recorded neural activity in the ventral pallidum (VP) while rats learned a pavlovian reward as... more We recorded neural activity in the ventral pallidum (VP) while rats learned a pavlovian reward association. Rats learned to distinguish a tone that predicted sucrose pellets (CSϩ) from a different tone that predicted nothing (CSϪ). Many VP units became responsive to CSϩ, but few units responded to CSϪ. When two CSϩ were encountered sequentially, the earliest predictor of reward became most potent. Many VP units were also activated when the sucrose reward was received [unconditioned stimulus (UCS)]. These VP units for UCS remained responsive to sucrose reward after learning, even when sucrose was already predicted by CSϩ. Neural representation of reward learning and reward itself was characterized by population codes. The population of units that responded to CSϩ increased with learning, whereas the population that responded to UCS did not change. A relative firing rate code also represented the identities of conditioned stimuli and UCS. Firing rate differences among stimuli were acquired early and remained stable during subsequent training, whereas population codes and behavioral conditioned responses continued to develop during subsequent training. Thus, the VP makes use of dynamic CS population and rate codes to encode pavlovian reward cues in reward learning and uses stable UCS population and firing codes to encode sucrose reward itself.
Journal of Neuroscience, 2009
Pavlovian cues for rewards become endowed with incentive salience, guiding "wanting" to their lea... more Pavlovian cues for rewards become endowed with incentive salience, guiding "wanting" to their learned reward. Usually, cues are "wanted" only if their rewards have ever been "liked," but here we show that mesocorticolimbic systems can recompute "wanting" de novo by integrating novel physiological signals with a cue's preexisting associations to an outcome that lacked hedonic value. That is, a cue's incentive salience can be recomputed adaptively. We demonstrate that this recomputation is encoded in neural signals coursing through the ventral pallidum. Ventral pallidum neurons do not ordinarily fire vigorously to a cue that predicts the previously "disliked" taste of intense salt, although they do fire to a cue that predicts the taste of previously "liked" sucrose. Yet we show that neural firing rises dramatically to the salt cue immediately and selectively when that cue is encountered in a never-before-experienced state of physiological salt depletion. Crucially, robust neural firing to the salt cue occurred the first time it was encountered in the new depletion state (in cue-only extinction trials), even before its associated intense saltiness has ever been tasted as positively "liked" (salt taste had always been "disliked" before). The amplification of incentive salience did not require additional learning about the cue or the newly positive salt taste. Thus dynamic recomputation of cue-triggered "wanting" signals can occur in real time at the moment of cue re-encounter by combining previously learned Pavlovian associations with novel physiological information about a current state of specific appetite.
Synapse, 2000
This study compared the effect of intraventricular administration of dopamine D1 or D2 agonists o... more This study compared the effect of intraventricular administration of dopamine D1 or D2 agonists or of ACTH on the sequential stereotypy of a serial pattern of grooming movements ("syntactic chain"). In a previous study, we showed that peripheral administration of D1 agonists increased the probability of occurrence and enhanced the stereotypy of the already-stereotyped movement pattern. Here we made microinjec
Synapse, 2000
Peripheral administration of D1 dopamine agonists elicits grooming behavior from rodents. The pre... more Peripheral administration of D1 dopamine agonists elicits grooming behavior from rodents. The present study examined grooming behavior and the relative probability and stereotypy of a natural sequence of grooming movements (called a syntactic grooming chain) that follows a predictable fixed pattern of serial order. We compared the amount of grooming behavior vs. the stereotypy of sequential patterns after peripheral administration of either a partial D1 agonist (SKF 38393; 2.5, 5.0, 10, 20 mg/kg), a full D1 agonist (SKF 82958; 0.1, 0.2, 0.5, 1.0 mg/kg; i.p.), a D2 agonist (quinpirole; 5.0, 10 mg/kg), or ACTH (2.0, 5.0 mg/kg). There was a dissociation between the elicited grooming amount, the pattern frequency, and the pattern completion or sequential stereotypy after these drugs. Quinpirole and ACTH both reduced the likelihood that the sequential pattern would be completed in the normal pattern (and reduced the overall amount of grooming). Administration of either SKF 38393 or SKF 82958 increased the tendency to engage in complex stereotyped sequential patterns of grooming (even though only the partial D1 agonist increased the total amount of grooming). In addition, SKF 38393 increased the sequential stereotypy of the already-stereotyped pattern itself (as measured by the probability of completing the stereotyped sequence once it began). Thus, dopamine D1 receptor activation appears to contribute to a kind of sequential super-stereotypy in which a complex, stereotyped behavioral sequence is initiated more frequently and more often goes to completion. Synapse 37:194-204, 2000.
Social Cognition, 2008
How do brain representations of the utility of a hedonic goal guide decisions about whether to pu... more How do brain representations of the utility of a hedonic goal guide decisions about whether to pursue it? our focus here will be on brain mechanisms of reward utility operating at particular decision moments in life. Moments such as when you encounter an image, sound, scent or other cue associated in your past with a particular reward; or perhaps just vividly imagine that cue. Such a cue can often trigger a sudden motivational urge to pursue that goal, and sometimes a decision to do so. In drug addicts trying to quit, a cue for the addicted drug might trigger urges that rise to compulsive levels of intensity, despite prior commitments to abstain, leading to the decision to relapse into taking the drug again. normal or addicted, the urge and decision may well have been lacking immediately before the cue was encountered. The decision to pursue the cued reward might never have happened if the cue had not been encountered. Why can such cues momentarily dominate decision making? The answer involves brain mesolimbic dopamine mechanisms that amplify the incentive salience of reward cues, selectively elevating decision utility to trigger "wanting" for the goal. We describe affective neuroscience studies of brain limbic generators of "wanting" that shed light on how cues trigger pursuit of their goals, both normally and even under intense conditions of irrational goal pursuit. Why can sudden encounters with cues for a reward suddenly trigger pulses of motivation to pursue that reward as a goal? This question has both psychological and neural answers, and it may be useful to consider them together. In particular we think a full psychological answer involves a particular subtype of reward utility. To help make this answer clear, we will draw on a utility taxonomy that We thank Ran R. Hassin and Timothy D. Wilson for helpful comments on an earlier version of this manuscript. Portions of this article will appear as a chapter in E.
Psychological Science, 1993
How does the brain create rule-governed sequences of behavior? An answer to this question may com... more How does the brain create rule-governed sequences of behavior? An answer to this question may come from a surprising source: the neostriatum (caudate nucleus and putamen). Traditionally, the neostriatum has been considered part of the brain's motor system, but its contribution to the preparation or execution of movement is recognized generally to concern high-level motor functions. Recent work implicates the neostriatum in disorders of sequential action and thought, as in the repetition of thoughts or habits in human obsessive-compulsive disorder and movements or speech in Tourette's syndrome. Yet there is no direct evidence to support the idea that the neostriatum controls sequences of behavior. Using ethological and neurophysiological techniques to study neural activity in the rat neostriatum during syntactic grooming sequences, we found that neuronal activity in the anterolateral neostriatum depended on the execution of syntactic sequences of grooming actions. The individ...
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Papers by J. Wayne Aldridge