Opponent control of behavior by dorsomedial striatal pathways depends on task demands and internal state

Abstract

A classic view of the striatum holds that activity in direct and indirect pathways oppositely modulates motor output. Whether this involves direct control of movement, or reflects a cognitive process underlying movement, has remained unresolved. Here we find that strong, opponent control of behavior by the two pathways of the dorsomedial striatum (DMS) depends on a task's cognitive demands. Furthermore, a latent state model (a hidden markov model with generalized linear model observations) reveals that-even within a single task-the contribution of the two pathways to behavior is state-dependent. Specifically, the two pathways have large contributions in one of two states associated with a strategy of evidence accumulation, compared to a state associated with a strategy of repeating previous choices. Thus, both the cognitive demands imposed by a task, as well as the strategy that mice pursue within a task, determine whether DMS pathways provide strong and opponent control of behavior.

Complementary coding of behaviors in striatal pathways supports a dual selection-suppression function

“…The concurrent activation of specific iSPN ensembles enables the proper filtering of only one action, most likely the most appropriate action in a given context. This mode of organization likely supports efficient shifts in the behavioral strategy depending on an animal’s internal state or task contingencies 40 .…”

Multiple timescales of sensory-evidence accumulation across the dorsal cortex

“…Our simultaneous inactivation experiments ( Figure 3 ) suggest that dorsal cortical activity is unevenly weighted, potentially by downstream structures. Candidate regions include the medial prefrontal cortex or subcortical structures such as the striatum and the cerebellum, which have been shown to be causally involved in evidence accumulation ( Bolkan et al, 2022 ; Deverett et al, 2019 ; Yartsev et al, 2018 ). Other subcortical candidates are midbrain regions shown to have a high incidence of choice signals in a contrast discrimination task ( Steinmetz et al, 2019 ).…”

On the normative advantages of dopamine and striatal opponency for learning and choice

“…However, this body of literature does not consider how increases or decreases of dopamine affect the decision itself, only its latency or speed. Instead, OpAL/OpAL* can capture both shifts in vigor and cost-benefit choice as seen empirically with drug manipulations across species ( Cousins et al, 1996 ; Salamone et al, 2005 ; Treadway et al, 2012 ; Westbrook et al, 2020 ) and more precise optogenetic manipulations of DA and activity of D1 and D2 MSNs ( Doi et al, 2020 ; Bolkan et al, 2022 ; Zalocusky et al, 2016 ; Tai et al, 2012 ; Yartsev et al, 2018 ). Notably, OpAL* suggests that in sparse reward environments, it is adaptive to lower dopaminergic levels and not merely avoiding action altogether (as in classical notions of the direct indirect pathways).…”