From learning to action: the integration of dorsal striatal input and output pathways in instrumental conditioning

Abstract

Considerable evidence suggests that the learning and performance of instrumental actions depend on activity in basal ganglia circuitry; however, these two functions have generally been considered independently. Whereas research investigating the associative mechanisms underlying instrumental conditioning has identified critical cortical and limbic input pathways to the dorsal striatum, the performance of instrumental actions has largely been attributed to activity in the dorsal striatal output pathways, with direct and indirect pathway projection neurons mediating action initiation, perseveration and cessation. Here, we discuss evidence that the dorsal striatal input and basal ganglia output pathways mediate the learning and performance of instrumental actions, respectively, with the dorsal striatum functioning as a transition point. From this perspective, the issue of how multiple striatal inputs are integrated at the level of the dorsal striatum and converted into relatively restricted outputs becomes one of critical significance for understanding how learning is translated into action. So too does the question of how learning signals are modulated by recent experience. We propose that this occurs through recurrent corticostriatothalamic feedback circuits that serve to integrate performance signals by updating ongoing action-related learning.

Striatal direct and indirect pathway neurons differentially control the encoding and updating of goal-directed learning

“…We have previously argued (Peak et al, 2019) that glutmatergic inputs to the dorsal striatum constitute "learning" pathways in the broader basal ganglia circuitry, and striatal output pathways constitute "performance" pathways. Central to that argument is that the dorsal striatum is a point of convergence of these two functions and the current results refine this, suggesting that both goal-directed learning and performance relies specifically on dSPN input and ouptut processes in the pDMS.…”

“…Such goal-directed actions have been found to rely on the ability of animals to encode the relationship between an action and its consequences or outcome, and to integrate that information with the current value of the outcome (Balleine & Dickinson, 1998;Dickinson & Balleine, 1994). It has also become clear that the acquisition of goaldirected actions relies on a corticostriatal circuit centered on the posterior region of dorsomedial striatum (pDMS) where glutamatergic inputs from the prelimbic cortex and dopaminergic inputs from the substantia nigra pars compacta (SNc) interact to influence goal-directed learning and performance via their effect on striatal output (Shiflett & Balleine, 2010;Peak et al, 2019;Balleine, 2019, for reviews). Accordingly, in the past decade there has been intense investigation into how striatal output pathways mediate the expression of actions, goal-directed or otherwise (Poyraz et al, 2016;Freeze et al, 2013;Hikida et al, 2010;Kravitz et al, 2010;Kravitz et al, 2012;Tai et al, 2012;Tecuapetla et al, 2014;Tecuapetla et al, 2016).…”

Chemogenetic inhibition in the dorsal striatum reveals regional specificity of direct and indirect pathway control of action sequencing

“…It has been hypothesized that these variables-temporal certainty of outcomes and action-outcome contiguity-play important roles in determining the goal-directed nature of behavior (DeRusso et al, 2010; see also Garr et al, in press), and it is possible that tasks that maximize these variables, such as the sequence task used here, could prevent goal-directed control from ever being erased (however, see Adams, 1982). On the other hand, it has been emphasized that it is the posterior DMS specifically that participates in goaldirected decision-making (Peak, Hart, & Balleine, 2018), while the virus infusions here were aimed at the anterior DMS. However, there is some evidence that disruption of anterior DMS function does interfere with goal-directed control of instrumental actions (Corbit, Nie, & Janak, 2012).…”

Loss of striatal tyrosine‐hydroxylase interneurons impairs instrumental goal‐directed behavior

“…Striatal THIN lesions impair pre-pulse inhibition of the startle reflex (Assous et al, 2017), suggesting an important role in attention and behavioral inhibition. We examined striatal THIN's role in reward-based learning and decision making, given the striatum's well-described functions in these domains (Balleine, Liljeholm, & Ostlund, 2009;Peak, Hart, & Balleine, 2018;Sharpe et al, 2018). Specifically, we examined instrumental behavior and tests of effortful responding using (a) the progressive ratio test, (b) a choice test following selective-satiety induced outcome devaluation, and (c) an outcome reinstatement test.…”