Dopamine Encoding of Pavlovian Incentive Stimuli Diminishes with Extended Training

Departments of Psychiatry and Behavioral Sciences, and Pharmacology, University of Washington, Seattle, Washington 98195.
The Journal of Neuroscience : The Official Journal of the Society for Neuroscience (Impact Factor: 6.34). 02/2013; 33(8):3526-32. DOI: 10.1523/JNEUROSCI.5119-12.2013
Source: PubMed


Dopamine is highly implicated both as a teaching signal in reinforcement learning and in motivating actions to obtain rewards. However, theoretical disconnects remain between the temporal encoding properties of dopamine neurons and the behavioral consequences of its release. Here, we demonstrate in rats that dopamine evoked by pavlovian cues increases during acquisition, but dissociates from stable conditioned appetitive behavior as this signal returns to preconditioning levels with extended training. Experimental manipulation of the statistical parameters of the behavioral paradigm revealed that this attenuation of cue-evoked dopamine release during the postasymptotic period was attributable to acquired knowledge of the temporal structure of the task. In parallel, conditioned behavior became less dopamine dependent after extended training. Thus, the current work demonstrates that as the presentation of reward-predictive stimuli becomes anticipated through the acquisition of task information, there is a shift in the neurobiological substrates that mediate the motivational properties of these incentive stimuli.

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    • "However, Schultz and colleagues (Fiorillo et al., 2005) subsequently provided evidence for the presence of the variance correlate in the responses of dopamine neurons on individual trials. Studies using fast-scan cyclic voltammetry in the nucleus accumbens core of rats during Pavlovian conditioning or operant tasks in rats have demonstrated that EV and reward-predictionerror correlates are present in the form of phasic dopamine release (Clark et al., 2013; Flagel et al., 2011; Gan et al., 2010; Stuber et al., 2008), but a correlate of variance or uncertainty in the form of phasic dopamine release has not been described. Therefore, in the current study, we recorded dopamine release in the nucleus accumbens core of rats undergoing Pavlovian conditioning with partial reinforcement which allowed for both the examination of signaling on individual trials and a quantitative analysis of signaling profiles across multiple stages of learning. "
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    ABSTRACT: Cue- and reward-evoked phasic dopamine activity during Pavlovian and operant conditioning paradigms is well correlated with reward-prediction errors from formal reinforcement learning models, which feature teaching signals in the form of discrepancies between actual and expected reward outcomes. Additionally, in learning tasks where conditioned cues probabilistically predict rewards, dopamine neurons show sustained cue-evoked responses that are correlated with the variance of reward and are maximal to cues predicting rewards with a probability of 0.5. Therefore, it has been suggested that sustained dopamine activity after cue presentation encodes the uncertainty of impending reward delivery. In the current study we examined the acquisition and maintenance of these neural correlates using fast-scan cyclic voltammetry in rats implanted with carbon fiber electrodes in the nucleus accumbens core during probabilistic Pavlovian conditioning. The advantage of this technique is that we can sample from the same animal and recording location throughout learning with single trial resolution. We report that dopamine release in the nucleus accumbens core contains correlates of both expected value and variance. A quantitative analysis of these signals throughout learning, and during the ongoing updating process after learning in probabilistic conditions, demonstrates that these correlates are dynamically encoded during these phases. Peak CS-evoked responses are correlated with expected value and predominate during early learning while a variance-correlated sustained CS signal develops during the post-asymptotic updating phase.
    Neurobiology of Learning and Memory 08/2014; 117. DOI:10.1016/j.nlm.2014.07.010 · 3.65 Impact Factor
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    • "Such a proposition is supported by recent evidence from a Pavlovian task, which showed that NAc dopamine adapts to the temporal variability of cue-reward pairings over training. More specifically, cue-elicited dopamine decreased after extensive presentation of the cue-reward associations, although was then restored if the cue was unexpectedly presented at a shorter ITI (Clark et al., 2013). A second, related idea is that, while dopamine may preferentially encode the anticipated benefits of a course of action, there may also be an initial boost in dopamine release to any unpredicted, uncertain event to motivate exploration and investigation of that option (Kakade and Dayan, 2002; Phillips et al., 2007; Walton et al., 2011). "
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    ABSTRACT: Dopamine has long been tightly associated with aspects of reinforcement learning and motivation in simple situations where there are a limited number of stimuli to guide behavior and constrained range of outcomes. In naturalistic situations, however, there are many potential cues and foraging strategies that could be adopted, and it is critical that animals determine what might be behaviorally relevant in such complex environments. This requires not only detecting discrepancies with what they have recently experienced, but also identifying similarities with past experiences stored in memory. Here, we review what role dopamine might play in determining how and when to learn about the world, and how to develop choice policies appropriate to the situation faced. We discuss evidence that dopamine is shaped by motivation and memory and in turn shapes reward-based memory formation. In particular, we suggest that hippocampal-striatal-dopamine networks may interact to determine how surprising the world is and to either inhibit or promote actions at time of behavioral uncertainty.
    Frontiers in Neuroscience 10/2013; 7(7):175. DOI:10.3389/fnins.2013.00175 · 3.66 Impact Factor
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    The Journal of Neuroscience : The Official Journal of the Society for Neuroscience 06/2013; 33(25):10191-2. DOI:10.1523/JNEUROSCI.1543-13.2013 · 6.34 Impact Factor
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