A competitive model for striatal action selection

Abstract

The direct and indirect pathway striatal medium spiny neurons (dMSNs and iMSNs) have long been linked to action selection, but the precise roles of these neurons in this process remain unclear. Here, we review different models of striatal pathway function, focusing on the classic "go/no-go" model which posits that dMSNs facilitate movement while iMSNs inhibit movement, and the "complementary" model, which argues that dMSNs facilitate the selection of specific actions while iMSNs inhibit potentially conflicting actions. We discuss the merits and shortcomings of these models and propose a "competitive" model to explain the contribution of these two pathways to behavior. The "competitive" model argues that rather than inhibiting conflicting actions, iMSNs are tuned to the same actions that dMSNs facilitate, and the two populations "compete" to determine the animal's behavioral response. This model provides a theoretical explanation for how these pathways work together to select actions. In addition, it provides a link between action selection and behavioral reinforcement, via modulating synaptic strength at inputs onto dMSNs and iMSNs. Finally, this model makes predictions about how imbalances in the activity of these pathways may underlie behavioral traits associated with psychiatric disorders. Understanding the roles of these striatal pathways in action selection may help to clarify the neuronal mechanisms of decision-making under normal and pathological conditions.

Keywords: Approach; Avoidance; Dopamine; Drug-seeking; Repetitive behavior; Striatum.

Figure 1.. Three models of striatal pathway function.

(A) The GO/NO GO model posits that direct pathway MSNs (d, in blue) activation favors movement (GO) while indirect pathway MSN activation (i, in red) inhibits movement (STOP). (B) In the COMPLEMENTARY model, dMSNs (d) select and facilitate one action while iMSNs (i) concurrently suppress competing motor programs, allowing the selected action to proceed. (C) In the COMPETITIVE model, the balance of direct and indirect pathway output within an ensemble determines whether the animal approaches or avoids a stimulus.

Figure 2.. Behavioral traits associated with altered striatal plasticity.

(A) The enhanced and reduced excitatory drive onto dMSNs and iMSNs observed in diseases such as drug addiction, alcohol exposure and ASD might bias animals toward the repetition of certain actions, such as stimulus approach or self-directed stereotypies. (B) In naturalistic conflicts, the balanced activity of dMSNs and iMSNs ensures optimal decision-making. (C) Heightened excitatory drive onto iMSNs and reduced functionality of dMSNs may underlie animal model of social avoidance, suggesting that increased striatopallidal activity might bias animals toward stimulus avoidance.