Complete representation of action space and value in all dorsal striatal pathways

• Published in: Cell reports (Cambridge) 2021-07, Vol.36 (4), p.109437, Article 109437
• Main Authors: Weglage, Moritz, Wärnberg, Emil, Lazaridis, Iakovos, Calvigioni, Daniela, Tzortzi, Ourania, Meletis, Konstantinos
• Format: Article
• Language: English
• Subjects: Animals; basal ganglia; behavior; Behavior, Animal; Choice Behavior; Corpus Striatum - physiology; Female; imaging; Locomotion - physiology; Male; Medicin och hälsovetenskap; Mice, Transgenic; mouse; Neural Pathways - physiology; Neurons - physiology; opioid; reinforcement; reward; striatum; striosome; Task Performance and Analysis
• ISSN: 2211-1247; 2211-1247
• DOI: 10.1016/j.celrep.2021.109437

The dorsal striatum plays a central role in the selection, execution, and evaluation of actions. An emerging model attributes action selection to the matrix and evaluation to the striosome compartment. Here, we use large-scale cell-type-specific calcium imaging to determine the activity of striatal projection neurons (SPNs) during motor and decision behaviors in the three major outputs of the dorsomedial striatum: Oprm1+ striosome versus D1+ direct and A2A+ indirect pathway SPNs. We find that Oprm1+ SPNs show complex tunings to simple movements and value-guided actions, which are conserved across many sessions in a single task but remap between contexts. During decision making, the SPN tuning profiles form a complete representation in which sequential SPN activity jointly encodes task progress and value. We propose that the three major output pathways in the dorsomedial striatum share a similarly complete representation of the entire action space, including task- and phase-specific signals of action value and choice. [Display omitted] •Striosomal Oprm1+ SPNs are tuned to motor and value-guided actions•SPNs encode moment-by-moment action and value in a choice task•SPN action tuning is stable over many task sessions, but remaps between contexts•The main striatal pathways encode a similarly rich representation of actions and value Weglage et al. record three different types of striatal projection neurons in dorsomedial striatum during movements and decision making, showing that all three projections share complete and context-specific representations of the action space, where neuron activity tracks moment-by-moment the task progress and the value of actions.