Abstract

HIGHLIGHTS Blockade of dopamine D1 receptors in ACC suppressed instrumental learning when overt responding was required.Covert learning through observation was not impaired.After treatment with a dopamine antagonist, instrumental learning recovered but not the rat's pretreatment level of effort tolerance.ACC dopamine is not necessary for acquisition of task-relevant cues during learning, but regulates energy expenditure and effort based decision.Dopamine activity in anterior cingulate cortex (ACC) is essential for various aspects of instrumental behavior, including learning and effort based decision making. To dissociate learning from physical effort, we studied both observational (covert) learning, and trial-and-error (overt) learning. If ACC dopamine activity is required for task acquisition, its blockade should impair both overt and covert learning. If dopamine is not required for task acquisition, but solely for regulating the willingness to expend effort for reward, i.e., effort tolerance, blockade should impair overt learning but spare covert learning. Rats learned to push a lever for food rewards either with or without prior observation of an expert conspecific performing the same task. Before daily testing sessions, the rats received bilateral ACC microinfusions of SCH23390, a dopamine D1 receptor antagonist, or saline-control infusions. We found that dopamine blockade suppressed overt responding selectively, leaving covert task acquisition through observational learning intact. In subsequent testing sessions without dopamine blockade, rats recovered their overt-learning capacity but not their pre-treatment level of effort tolerance. These results suggest that ACC dopamine is not required for the acquisition of conditioned behaviors and that apparent learning impairments could instead reflect a reduced level of willingness to expend effort due to cortical dopamine blockade.

Highlights

  • Learning the contingencies between behavior and environmental events through associative learning is a fundamental adaptive capacity that allows animals to predict outcomes of stimuli and actions through conditioning

  • We have shown that blockade of D1 receptors (D1Rs) in anterior cingulate cortex (ACC) completely suppressed overt instrumental responding

  • Using observational learning, where the learner acquired knowledge pertaining to action-outcome associations without exerting any physical behavioral effort, we found that covert learning was left intact by D1Rs blockade

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Summary

Introduction

Learning the contingencies between behavior and environmental events through associative learning is a fundamental adaptive capacity that allows animals to predict outcomes of stimuli and actions through conditioning. Lesions of ACC in rats (Bussey et al, 1996; Parkinson et al, 2000) and monkeys (Rushworth et al, 2003; Walton et al, 2003), or pharmacological manipulations of its activity (Schweimer and Hauber, 2006; McKee et al, 2010), have led to the conclusion that ACC is required for learning instrumental tasks, but is less necessary for their performance once they have been learned Studies using a T-maze cost–benefit task have shown that contrary to control rats which choose more often the high cost—high reward option, ACC-lesioned rats more often select the low cost—low reward option (Walton et al, 2003; Schweimer et al, 2005)

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