Flexible and Stable Value Coding Areas in Caudate Head and Tail Receive Anatomically Distinct Cortical and Subcortical Inputs

Smith

et al. 2018

Eur J of Neuroscience

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Direct and indirect pathways in the basal ganglia work together for controlling behavior. However, it is still a controversial topic whether these pathways are segregated or merged with each other. To address this issue, we studied the connections of these two pathways in the caudal parts of the basal ganglia of rhesus monkeys using anatomical tracers. Our previous studies showed that the caudal basal ganglia control saccades by conveying long-term values (stable values) of many visual objects toward the superior colliculus. In experiment 1, we injected a tracer in the caudate tail (CDt), and found local dense plexuses of axon terminals in the caudal-dorsal-lateral part of substantia nigra pars reticulata (cdlSNr) and the caudal-ventral part of globus pallidus externus (cvGPe). These anterograde projections may correspond to the direct and indirect pathways, respectively. To verify this in experiment 2, we injected different tracers into cdlSNr and cvGPe, and found many retrogradely labeled neurons in CDt and, in addition, the caudal-ventral part of the putamen (cvPut). These cdlSNr-projecting and cvGPe-projecting neurons were found intermingled in both CDt and cvPut (which we call "striatum tail"). A small but significant proportion of neurons (<15%) were double-labeled, indicating that they projected to both cdlSNr and cvGPe. These anatomical results suggest that stable value signals (good vs. bad) are sent from the striatum tail to cdlSNr and cvGPe in a biased (but not exclusive) manner. These connections may play an important role in biasing saccades toward higher valued objects and away from lower valued objects.

Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

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

Amita

Smith

et al. 2018

Eur J of Neuroscience

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“…Yet, CDh and CDt receive inputs from mostly different areas (e.g., frontal cortex to CDh, temporal cortex to CDt; Yeterian & Van Hoesen, 1978). Even when one area projects to both CDh and CDt, each neuron projects to either CDh or CDt (Griggs et al, 2017).…”

Section: Caudate Tail Circuitmentioning

confidence: 99%

Direct and indirect pathways for choosing objects and actions

Hikosaka

Amita

et al. 2018

Eur J of Neuroscience

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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.

“…Supporting the role of the dorsal striatum as the actor, a number of empirical studies have implicated it in the process of action selection . The dorsal striatum is anatomically divided into dorsomedial and dorsolateral subdivisions (corresponding to the caudate and putamen in primates, respectively); the dorsomedial striatum has been assumed to hold working memory that monitors recent actions to anticipate outcomes and reevaluate the action‐contingent outcomes to select appropriate goal‐directed actions in the future; on the other hand, the dorsolateral striatum has been associated with the transition of behavior to habitual decisions that are insensitive to outcome devaluation.…”

Section: Choice Impulsivity and Dorsal Striatummentioning

confidence: 99%

“…A ventral‐to‐dorsal gradient can be anatomically mapped onto the dorsal striatum based on the afferents from various cortical and subcortical regions . Interestingly, accumulated pieces of evidence from human neuroimaging research have indicated that choice impulsivity could be modulated by such a gradient, but in a distinct anatomical organization (Fig.…”

Section: Evidence From Human Neuroimaging Studiesmentioning

confidence: 99%

The role of the dorsal striatum in choice impulsivity

Annals of the New York Academy of Sciences

2018

It has long been recognized that the dorsal striatum is an essential brain region for control of action selection based on action–outcome contingency learning, particularly when the available actions are bound to rewarding outcomes. In principle, intertemporal choice in the delay‐discounting task—a validated measure of choice impulsivity—involves reward‐associated actions that require the recruitment of the dorsal striatum. Here, we conjecture about ways the dorsal striatum is involved in choice impulsivity. Based on a selective body of studies, we begin with a brief history of research on choice impulsivity and the dorsal striatum, and then provide a comprehensive summary of contemporary studies utilizing human neuroimaging and animal models to search for links between choice impulsivity and the dorsal striatum. In particular, we discuss in‐depth the converging evidence for the associations of choice impulsivity with the reward valuation coded by the caudate, a ventral‐to‐dorsal gradient in the dorsal striatum, the origins of striatal afferents, and developmental maturation of frontostriatal connectivity during adolescence.