Monitoring and Updating of Action Selection for Goal-Directed Behavior through the Striatal Direct and Indirect Pathways

Abstract

The basal ganglia play key roles in adaptive behaviors guided by reward and punishment. However, despite accumulating knowledge, few studies have tested how heterogeneous signals in the basal ganglia are organized and coordinated for goal-directed behavior. In this study, we investigated neuronal signals of the direct and indirect pathways of the basal ganglia as rats performed a lever push/pull task for a probabilistic reward. In the dorsomedial striatum, we found that optogenetically and electrophysiologically identified direct pathway neurons encoded reward outcomes, whereas indirect pathway neurons encoded no-reward outcome and next-action selection. Outcome coding occurred in association with the chosen action. In support of pathway-specific neuronal coding, light activation induced a bias on repeat selection of the same action in the direct pathway, but on switch selection in the indirect pathway. Our data reveal the mechanisms underlying monitoring and updating of action selection for goal-directed behavior through basal ganglia circuits.

Choice suppression is achieved through opponent but not independent function of the striatal indirect pathway in mice

“…Our findings are also compatible with computational accounts that predict that lowering tonic dopamine, which facilitates iSPN activity and suppresses dSPN activity (59,60), shifts explore/exploit balance towards exploration (61,62). Finally, if behavioral switching is viewed as exploring action space, our iSPN data may relate to recent studies that report iSPN activity increases in response to outcomes preceding switch trials (25,64).…”

“…The DMS is primarily composed of D1 receptor expressing dSPNs and D2 receptor expressing iSPNs (20), whose activity reflect task features including movement, cues, and value (16,(21)(22)(23)(24)(25)(26). Consistent with predictions from functional neuroanatomy (27)(28)(29) and theoretical work (30,31), optogenetic stimulation of dSPNs promotes movement and reinforces actions ('go' functions) (32)(33)(34) whereas optogenetic stimulation of iSPNs inhibits movement and drives aversion ('no go' functions) (32)(33)(34).…”

“…While many studies have focused on the role of the striatum in selecting rewarded actions (16,18,25) and stimuli (49), fewer have studied its role in avoiding low-value actions (50)(51)(52)(53) and stimuli (54). Here, our goal was to understand how activity in DMS dSPNs and iSPNs influences the ability to suppress an initially encountered low-value choice in order to make a subsequent high-value choice.…”

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

“…Although we found no significant effect on either of these factors alone, the overall impairment by rats with iSPN inhibition appears to be due to their combination. Indeed, there is recent evidence to suggest that both of these forms of response flexibility require iSPNs; Matamales et al (2020) demonstrated that ablating iSPNs in the DMS encourages recurrent responding during the extinction of goal-directed learning (response perseveration), and Nonomura et al (2018) have shown that iSPNs in the DMS encode non-rewarded responses, and, if optogenetically stimulated following a non-rewarded response, promote switching to an alternate response.…”

Corticostriatal synaptic weight evolution in a two-alternative forced choice task

“…A significant body of experimental work has established that corticostriatal synapses represent one site of such plasticity, which is triggered when a behavior followed by an unexpected reward leads to a change in dopamine levels [8,39,44]. Because the corticostriatal synapses represent a key input pathway to the cortico-basal ganglia-thalamic (CBGT) circuits, these dopaminergic changes have been shown to have a critical impact on global network computations related to action selection [2,7,12,15,24,37,51].…”