Parallel basal ganglia circuits for decision making

Abstract

The basal ganglia control body movements, mainly, based on their values. Critical for this mechanism is dopamine neurons, which sends unpredicted value signals, mainly, to the striatum. This mechanism enables animals to change their behaviors flexibly, eventually choosing a valuable behavior. However, this may not be the best behavior, because the flexible choice is focused on recent, and, therefore, limited, experiences (i.e., short-term memories). Our old and recent studies suggest that the basal ganglia contain separate circuits that process value signals in a completely different manner. They are insensitive to recent changes in value, yet gradually accumulate the value of each behavior (i.e., movement or object choice). These stable circuits eventually encode values of many behaviors and then retain the value signals for a long time (i.e., long-term memories). They are innervated by a separate group of dopamine neurons that retain value signals, even when no reward is predicted. Importantly, the stable circuits can control motor behaviors (e.g., hand or eye) quickly and precisely, which allows animals to automatically acquire valuable outcomes based on historical life experiences. These behaviors would be called 'skills', which are crucial for survival. The stable circuits are localized in the posterior part of the basal ganglia, separately from the flexible circuits located in the anterior part. To summarize, the flexible and stable circuits in the basal ganglia, working together but independently, enable animals (and humans) to reach valuable goals in various contexts.

Neuronal connections of direct and indirect pathways for stable value memory in caudal basal ganglia

“…The next step in elucidating the mechanisms of the stable value memory is to investigate how these structures are interconnected in the caudal basal ganglia. Our previous studies suggest that good objects facilitate saccades through the direct pathway, while bad objects suppress saccades through the indirect pathway (Hikosaka, Ghazizadeh, Griggs, & Amita, ; Kim et al., ). The functional difference between direct and indirect pathways might arise due to the anatomical segregation of these pathways.…”

Direct and indirect pathways for choosing objects and actions

“…The basal ganglia contribute to decision making (Hikosaka et al, 2018). A typical process of decision making is to choose an object (object choice) and then choose an action (action choice) to manipulate the object, which leads to a rewarding outcome .…”

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

“…Current models for BG function highlight parallel circuits each with a specified functional capacity (Kim & Hikosaka, 2015). In addition, current ways of thinking often incorporate the idea that within each circuit there are two main paths, one direct and one indirect that have been proposed to operate in qualitatively distinct ways (Hikosaka et al, 2018;MacPherson, Morita, & Hikida, 2014).…”

“…Another goal is to bring the research forward to contemporary work using in vivo electrophysiology in awake, behaving animals (Cromwell, Tremblay, & Schultz, 2018;Webber, Mankin, & Cromwell, 2016). There is value in linking the diverse levels of analysis on BG function between reduced cellular analysis to a more holistic behavioral level, and several research teams have made these types of leaps productively (Buzsáki & Tingley, 2018;Calabresi, Picconi, Tozzi, & Ghiglieri, 2016;Hikosaka, Ghazizadeh, Griggs, & Amita, 2018). Our recent research focus has been on relative reward valuation (Binkley, Webber, Powers, & Cromwell, 2014;Ricker, Hatch, Powers, & Cromwell, 2016;Cromwell and Ricker, 2018) and incorporating basic information on dopamine modulation of incoming neural signals could provide the information base necessary for rapid plasticity that leads to changes in motivation sensitive to shifts in reward value from trial to trial (Webber, Chambers, Kostek, Mankin, & Cromwell, 2015).…”