Separate Populations of Neurons in Ventral Striatum Encode Value and Motivation

Bissonette, Gregory B.; Burton, Amanda C.; Gentry, Ronny N.; Goldstein, Brandon L.; Taylor, Hearn,; Barnett, Brian R.; Kashtelyan, Vadim; Roesch, Matthew R.

doi:10.1371/journal.pone.0064673

Cited by 31 publications

(46 citation statements)

References 87 publications

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“…S1f). Neurons in the lesioned area are known to fire to reward-predictive cues (Bissonette et al, 2013; O'Doherty et al, 2003; O'Doherty et al, 2004; Oleson et al, 2012; Roesch et al, 2009) and send output to VTA (Bocklisch et al, 2013; Grace and Bunney, 1985; Groenewegen et al, 1990; Mogenson et al, 1980; Voorn et al, 2004; Watabe-Uchida et al, 2012; Xia et al, 2011), supporting the proposal that this part of VS may influence dopaminergic prediction error signaling as proposed in neural instantiations of temporal difference reinforcement learning (TDRL) models (Daw et al, 2006; Joel et al, 2002). …”

Section: Resultssupporting

confidence: 58%

Temporal Specificity of Reward Prediction Errors Signaled by Putative Dopamine Neurons in Rat VTA Depends on Ventral Striatum

Takahashi

Langdon

Niv

et al. 2016

Neuron

104

115

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Summary Dopamine neurons signal reward prediction errors. This requires accurate reward predictions. It has been suggested that the ventral striatum provides these predictions. Here we tested this hypothesis by recording from putative dopamine neurons in the VTA of rats performing a task in which prediction errors were induced by shifting reward timing or number. In controls, the neurons exhibited error signals in response to both manipulations. However, dopamine neurons in rats with ipsilateral ventral striatal lesions exhibited errors only to changes in number and failed to respond to changes in timing of reward. These results, supported by computational modeling, indicate that predictions about the temporal specificity and the number of expected rewards are dissociable, and that dopaminergic prediction-error signals rely on the ventral striatum for the former but not the latter.

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Section: Resultssupporting

confidence: 58%

Temporal Specificity of Reward Prediction Errors Signaled by Putative Dopamine Neurons in Rat VTA Depends on Ventral Striatum

Takahashi

Langdon

Niv

et al. 2016

Neuron

104

115

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“…These data suggest that activity in NAc represents the motivational value associated with chosen actions and might be critical for translating cue-evoked value signals into motivated behavior (Catanese and van der Meer, 2013; McGinty et al, 2013). Consitent with this hypothesis, we and others have shown that firing in NAc is significantly correlated with reaction time (Roesch et al, 2009; Bissonette et al, 2013; McGinty et al, 2013). …”

Section: Nucleus Accumbens Core Versus Dorsal Lateral Striatumsupporting

confidence: 66%

From ventral-medial to dorsal-lateral striatum: Neural correlates of reward-guided decision-making

Burton

Nakamura

Roesch

2015

Neurobiology of Learning and Memory

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192

135

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The striatum is critical for reward-guided and habitual behavior. Anatomical and interference studies suggest a functional heterogeneity within striatum. Medial regions, such as nucleus accumbens core and dorsal medial striatum play roles in goal-directed behavior, while dorsal lateral striatum is critical for control of habitual action. Subdivisions of striatum are topographically connected with different cortical and subcortical structures forming channels that carry information related to limbic, associative, and sensorimotor functions. Here, we describe data showing that as one progresses from ventral-medial to dorsal-lateral striatum, there is a shift from more prominent value encoding to activity more closely related to associative and motor aspects of decision-making. In addition, we will describe data suggesting that striatal circuits work in parallel to control behavior and that regions within striatum can compensate for each other when functions are disrupted.

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“…In these experiments, animals learn that conditioned stimuli (CS) predict potential rewards or the possibility of punishment. Typically, there are three trial types where the CS predicts: (1) a large reward (e.g., sucrose, juice); (2) a neutral condition or a small (or no) reward; and (3) a small (or no) reward with the threat of an aversive outcome, such as delivery of a bitter quinine solution, electric shock, or air puff to the eye (Rolls et al 1989; Roesch and Olson 2004; Roesch et al 2010a; Bissonette et al 2013; Matsumoto and Hikosaka 2009; Brischoux et al 2009; Anstrom et al 2009; Lammel et al 2011). If neurons encode value , neural activity should show a monotonic relationship during appetitive, neutral, and aversive trials (Fig.…”

Section: Value Versus Motivation and Saliencementioning

confidence: 99%

Neurophysiology of Reward-Guided Behavior: Correlates Related to Predictions, Value, Motivation, Errors, Attention, and Action

Bissonette

Roesch

2015

Current Topics in Behavioral Neurosciences

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Many brain areas are activated by the possibility and receipt of reward. Are all of these brain areas reporting the same information about reward? Or are these signals related to other functions that accompany reward-guided learning and decision-making? Through carefully controlled behavioral studies, it has been shown that reward-related activity can represent reward expectations related to future outcomes, errors in those expectations, motivation, and signals related to goal- and habit-driven behaviors. These dissociations have been accomplished by manipulating the predictability of positively and negatively valued events. Here, we review single neuron recordings in behaving animals that have addressed this issue. We describe data showing that several brain areas, including orbitofrontal cortex, anterior cingulate, and basolateral amygdala signal reward prediction. In addition, anterior cingulate, basolateral amygdala, and dopamine neurons also signal errors in reward prediction, but in different ways. For these areas, we will describe how unexpected manipulations of positive and negative value can dissociate signed from unsigned reward prediction errors. All of these signals feed into striatum to modify signals that motivate behavior in ventral striatum and guide responding via associative encoding in dorsolateral striatum.

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Separate Populations of Neurons in Ventral Striatum Encode Value and Motivation

Cited by 31 publications

References 87 publications

Temporal Specificity of Reward Prediction Errors Signaled by Putative Dopamine Neurons in Rat VTA Depends on Ventral Striatum

Temporal Specificity of Reward Prediction Errors Signaled by Putative Dopamine Neurons in Rat VTA Depends on Ventral Striatum

From ventral-medial to dorsal-lateral striatum: Neural correlates of reward-guided decision-making

Neurophysiology of Reward-Guided Behavior: Correlates Related to Predictions, Value, Motivation, Errors, Attention, and Action

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