Wave-like dopamine dynamics as a mechanism for spatiotemporal credit assignment

Cell. 2021 May 13;184(10):2733-2749.e16. doi: 10.1016/j.cell.2021.03.046. Epub 2021 Apr 15.

Abstract

Significant evidence supports the view that dopamine shapes learning by encoding reward prediction errors. However, it is unknown whether striatal targets receive tailored dopamine dynamics based on regional functional specialization. Here, we report wave-like spatiotemporal activity patterns in dopamine axons and release across the dorsal striatum. These waves switch between activational motifs and organize dopamine transients into localized clusters within functionally related striatal subregions. Notably, wave trajectories were tailored to task demands, propagating from dorsomedial to dorsolateral striatum when rewards are contingent on animal behavior and in the opponent direction when rewards are independent of behavioral responses. We propose a computational architecture in which striatal dopamine waves are sculpted by inference about agency and provide a mechanism to direct credit assignment to specialized striatal subregions. Supporting model predictions, dorsomedial dopamine activity during reward-pursuit signaled the extent of instrumental control and interacted with reward waves to predict future behavioral adjustments.

Keywords: agency learning; basal ganglia; credit assignment; decisionmaking; dopamine; motivated behaviors; reinforcement learning; striatum.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Axons / metabolism*
  • Behavior, Animal*
  • Corpus Striatum / metabolism*
  • Dopamine / metabolism*
  • Female
  • Male
  • Mice
  • Mice, Mutant Strains
  • Reward*

Substances

  • Dopamine