The Actor/Critic model has been suggested to be the computational solution to optimizing long term gains. In this model, decisions made by the Actor are updated by the Critic when outcomes deviate from what is expected. Past research shows that midbrain dopamine (DA) neurons signal errors in reward prediction;however, it is unknown how these signals are generated or how they impact decision policies in downstream brains areas. According to the Actor/Critic model, midbrain DA neurons compute prediction errors by comparing the predicted value of reward, signaled by ventral striatum (VS), to the actual value of reward received, but this has not been directly tested. Subsequently, prediction errors are thought to modify behavior by updating the action policies of the Actor, dorsal striatum (DS). Neural correlates in DS include policies related to stimuli, responses and outcomes, but how these correlates are modulated by the DA system during learning remains unknown. Here, these issues will be addressed by recording from single neurons in DS and midbrain DA neurons after DA and VS inactivation, respectively. The importance of these interactions will be verified by inactivation techniques. Importantly, this circuit has been shown to be abnormal in addiction, which makes sense, considering that addicts cannot optimize choice behavior in the face of changing consequences. A final experiment will examine neural correlates of reward predictions, prediction errors and decision policies in rats that have chronically self-administered cocaine;the results will help determine how these neural representations are disrupted after long-term drug exposure.

Public Health Relevance

Optimal decision-making is thought to depend on a circuit involving striatum and midbrain dopamine neurons;areas affected by long-term exposure to drugs of abuse. Together, these brain regions are thought to compute errors in reward prediction, which are subsequently used to update policies that guide future decisions. Improving our understanding of the neural mechanisms underlying the decision making process will provide a better working knowledge of how we learn normally and how this circuit is affected by chronic drug use.

Agency
National Institute of Health (NIH)
Institute
National Institute on Drug Abuse (NIDA)
Type
Research Project (R01)
Project #
5R01DA031695-03
Application #
8459880
Study Section
Cognitive Neuroscience Study Section (COG)
Program Officer
Volman, Susan
Project Start
2011-07-01
Project End
2016-04-30
Budget Start
2013-05-01
Budget End
2014-04-30
Support Year
3
Fiscal Year
2013
Total Cost
$314,917
Indirect Cost
$98,917
Name
University of Maryland College Park
Department
Psychology
Type
Schools of Arts and Sciences
DUNS #
790934285
City
College Park
State
MD
Country
United States
Zip Code
20742
Burton, Amanda C; Bissonette, Gregory B; Vazquez, Daniela et al. (2018) Previous cocaine self-administration disrupts reward expectancy encoding in ventral striatum. Neuropsychopharmacology 43:2350-2360
Burton, Amanda C; Bissonette, Gregory B; Zhao, Adam C et al. (2017) Prior Cocaine Self-Administration Increases Response-Outcome Encoding That Is Divorced from Actions Selected in Dorsal Lateral Striatum. J Neurosci 37:7737-7747
Bissonette, G B; Roesch, M R (2017) Neurophysiology of rule switching in the corticostriatal circuit. Neuroscience 345:64-76
Bissonette, Gregory B; Roesch, Matthew R (2016) Editorial: Neural Circuitry of Behavioral Flexibility: Dopamine and Related Systems. Front Behav Neurosci 10:6
Bryden, Daniel W; Burton, Amanda C; Barnett, Brian R et al. (2016) Prenatal Nicotine Exposure Impairs Executive Control Signals in Medial Prefrontal Cortex. Neuropsychopharmacology 41:716-25
Bissonette, G B; Roesch, M R (2016) Development and function of the midbrain dopamine system: what we know and what we need to. Genes Brain Behav 15:62-73
Bissonette, Gregory B; Roesch, Matthew R (2016) Neurophysiology of Reward-Guided Behavior: Correlates Related to Predictions, Value, Motivation, Errors, Attention, and Action. Curr Top Behav Neurosci 27:199-230
Bissonette, Gregory B; Roesch, Matthew R (2015) Neural correlates of rules and conflict in medial prefrontal cortex during decision and feedback epochs. Front Behav Neurosci 9:266
Hernandez, Alex; Burton, Amanda C; O'Donnell, Patricio et al. (2015) Altered basolateral amygdala encoding in an animal model of schizophrenia. J Neurosci 35:6394-400
Bissonette, Gregory B; Schoenbaum, Geoffrey; Roesch, Matthew R et al. (2015) Interneurons are necessary for coordinated activity during reversal learning in orbitofrontal cortex. Biol Psychiatry 77:454-64

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