A Corticostriatal Path Targeting Striosomes Controls Decision-Making under Conflict

A striking neurochemical form of compartmentalization has been found in the striatum of humans and other species, dividing it into striosomes and matrix. The function of this organization has been unclear, but the anatomical connections of striosomes indicate their relation to emotion-related brain regions, including the medial prefrontal cortex. We capitalized on this fact by combining pathway-specific optogenetics and electrophysiology in behaving rats to search for selective functions of striosomes. We demonstrate that a medial prefronto-striosomal circuit is selectively active in and causally necessary for cost-benefit decision-making under approach-avoidance conflict conditions known to evoke anxiety in humans. We show that this circuit has unique dynamic properties likely reflecting striatal interneuron function. These findings demonstrate that cognitive and emotion-related functions are, like sensory-motor processing, subject to encoding within compartmentally organized representations in the forebrain and suggest that striosome-targeting corticostriatal circuits can underlie neural processing of decisions fundamental for survival. [Display omitted] •A specific fronto-striatal decision circuit is activated by cost-benefit conflict•It primarily targets striatal striosomes, linked to limbic functions of striatum•Its optogenetic control selectively alters decisions under cost-benefit conflict•Its corticostriatal control is exerted through a striatal inhibitory microcircuit Optogenetic manipulation and electrophysiology of a circuit connecting the prefrontal cortex to striosomes—compartmentalized structures of the striatum—reveals that it has a selective role in influencing decision-making for choices with cost-benefit tradeoffs.