Direct and indirect pathways for choosing objects and actions

Abstract

A prominent target of the basal ganglia is the superior colliculus (SC) which controls gaze orientation (saccadic eye movement in primates) to an important object. This 'object choice' is crucial for choosing an action on the object. SC is innervated by the substantia nigra pars reticulata (SNr) which is controlled mainly by the caudate nucleus (CD). This CD-SNr-SC circuit is sensitive to the values of individual objects and facilitates saccades to good objects. The object values are processed differently in two parallel circuits: flexibly by the caudate head (CDh) and stably by the caudate tail (CDt). To choose good objects, we need to reject bad objects. In fact, these contrasting functions are accomplished by the circuit originating from CDt: The direct pathway focuses on good objects and facilitates saccades to them; the indirect pathway focuses on bad objects and suppresses saccades to them. Inactivation of CDt deteriorated the object choice, because saccades to bad objects were no longer suppressed. This suggests that the indirect pathway is important for object choice. However, the direct and indirect pathways for 'object choice', which aim at the same action (i.e., saccade), may not work for 'action choice'. One possibility is that circuits controlling different actions are connected through the indirect pathway. Additional connections of the indirect pathway with brain areas outside the basal ganglia may also provide a wider range of behavioral choice. In conclusion, basal ganglia circuits are composed of the basic direct/indirect pathways and additional connections and thus have acquired multiple functions.

Mapping neural dynamics underlying saccade preparation and execution and their relation to reaction time and direction errors

“…Here, we will focus on results from the antisaccade task, where it has been shown that the inhibition signal is not needed for saccadic movement but is needed to improve performance (Coe et al, 2019). The inhibition signal is potentially sourced from the reshaping of automatic signals via voluntary signals in the frontal and parietal cortices or it may be a spatially focused inhibitory signal sent to the SCs from the basal ganglia (Amita, Kim, Smith, Gopal, & Hikosaka, 2019;Hikosaka et al, 2019;Watanabe & Munoz, 2011). Cortical postsaccade activity within the FEF has been proposed to be related to response-evaluation to post-decision outcomes and sensory information of the stimulus (Teichert et al, 2014).…”

Phase of Firing Coding of Learning Variables across Prefrontal Cortex, Anterior Cingulate Cortex and Striatum during Feature Learning

“…Without LPFC, rhesus monkeys fail to recognize when a previously irrelevant object becomes relevant, as if they fail to calculate prediction errors needed for updating their attentional set (Rudebeck et al, 2017). When the anterior STR is lesioned, nonhuman primates tend to stick to previously learned behavior and show a lack of sensitivity to reward outcomes (Hikosaka et al, 2017(Hikosaka et al, , 2019. These behavioral lesion effects are consistent with the important role of each of these brain areas to track the history of recent outcomes, registering newly encountered (current) outcomes, and calculating the unexpectedness of experienced outcomes (prediction error).…”

“…Our findings critically complement these studies by revealing that 10-25 Hz spike-LFP synchronization is prevalent not only during cognitive processing, but also during the processing of outcomes after attention has been deployed and choices have been made. During this post-choice outcome processing, frontostriatal circuits are likely to adjust their synaptic connection strength to minimize future prediction 13 errors and improve performance (Hikosaka et al, 2019;Leong et al, 2017;Oemisch et al, 2019).…”

Translating striatal activity from brain slice to whole animal neurophysiology: A guide for neuroscience research integrating diverse levels of analysis

“…Several research groups are linking components of reward processing or bivalent reward versus punishment outcome updating to specific DA receptor activation (Hikosaka et al, 2018;Hikosaka et al, 2014) in addition to specific pathways coursing through the corticostriatal loops (Proulx et al, 2018;Wickens, 2008). The direct pathway has been the proposed pathway involved in choosing good objects and this could intimately depend upon the simultaneous interaction between DA D 1 and glutamate signaling (Hikosaka et al, 2019). In contrast, the indirect pathway activation mediates the effects of negative stimuli, suppressing unwanted movements, or generating avoidance reactions.…”