Striatopallidal adenosine A2A receptors in the nucleus accumbens confer motivational control of goal-directed behavior

Neuropharmacology. 2020 May 15:168:108010. doi: 10.1016/j.neuropharm.2020.108010. Epub 2020 Feb 13.

Abstract

The ability to learn the reward-value and action-outcome contingencies in dynamic environment is critical for flexible adaptive behavior and development of effective pharmacological control of goal-directed behaviors represents an important challenge for improving the deficits in goal-directed behavior which may underlie seemingly disparate symptoms across psychiatric disorders. Adenosine A2A receptor (A2AR) is emerging as a novel neuromodulatory target for controlling goal-directed behavior for its unique neuromodulatory features: the ability to integrate dopamine and glutamate signaling, the "brake" constraint of various cognitive processes and the balanced control of goal-directed and habit actions. However, the contribution and circuit mechanisms of the striatopallidal A2ARs in nucleus accumbens (NAc) to control of goal-directed behavior remain to be determined. Here, we employed newly developed opto-A2AR and the focal A2AR knockdown strategies to demonstrate the causal role of NAc A2AR in control of goal-directed behavior. Furthermore, we dissected out multiple distinct behavioral mechanisms underlying which NAc A2ARs control goal-directed behavior: (i) NAc A2ARs preferentially control goal-directed behavior at the expense of habit formation. (ii) NAc A2ARs modify the animals' sensitivity to the value of the reward without affecting the action-outcome contingency. (iii) A2AR antagonist KW6002 promotes instrumental actions by invigorating motivation. (iv) NAc A2ARs facilitate Pavlovian incentive value transferring to instrumental action. (v) NAc A2ARs control goal-directed behavior probably not through NAc-VP pathway. These insights into the behavioral and circuit mechanisms for NAc A2AR control of goal-directed behavior facilitate translational potential for A2AR antagonists in reversal of deficits in goal-directed decision-making associated with multiple neuropsychiatric disorders.

Keywords: Adenosine A(2A) receptors; Goal-directed behavior; Instrumental learning; Motivation; Nucleus accumbens; Pavlovian–instrumental transfer.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine A2 Receptor Antagonists / pharmacology
  • Animals
  • Conditioning, Classical / drug effects
  • Conditioning, Classical / physiology
  • Corpus Striatum / drug effects
  • Corpus Striatum / metabolism*
  • Globus Pallidus / drug effects
  • Globus Pallidus / metabolism*
  • Goals*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Motivation / drug effects
  • Motivation / physiology*
  • Nucleus Accumbens / drug effects
  • Nucleus Accumbens / metabolism*
  • Purines / pharmacology
  • Receptor, Adenosine A2A / deficiency
  • Receptor, Adenosine A2A / metabolism*

Substances

  • Adenosine A2 Receptor Antagonists
  • Purines
  • Receptor, Adenosine A2A
  • istradefylline