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

Abstract

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.

Amygdala controls saccade and gaze physically, motivationally, and socially

“…What is the neuronal mechanism of saccadic control by CeA? Anatomically, CeA projects to several structures that contribute to saccadic eye movements, including SNr, the globus pallidus, the striatum, the zona incerta, and the reticular formation (Price and Amaral, 1981;Shinonaga et al, 1992;Fudge et al, 2002;Fudge et al, 2004;Cho et al, 2013;Griggs et al, 2017;Amita et al, 2018). Importantly, most output neurons in CeA are GABAergic and inhibitory (Tovote et al, 2015), and saccades are controlled mainly by SC (Hikosaka et al, 2000).…”

“…Importantly, we found that although neuronal activity differed across subjects, responses of amygdala neurons were correlated with the saccadic reaction time to reward-associated objects within subjects. Anatomical studies have reported that CeA sends output to the basal ganglia, including the caudate tail (CDt), the globus pallidus externus (GPe), and the substantia nigra pars reticulata (SNr), all of which are known to encode stable object values and control saccades through the SNr-superior colliculus (SC) pathway (Shinonaga et al, 1992;Vankova et al, 1992;Fudge and Haber, 2000;Griggs et al, 2017;Amita et al, 2018). These studies suggest that CeA neurons modulate saccadic eye movements by sending contextual information to the basal ganglia circuit.…”

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).…”

Indirect pathway of caudate tail for choosing good objects in periphery

“…To investigate the neuronal mechanisms in the basal ganglia for skills, we focused on the posterior basal ganglia circuits. The posterior basal ganglia circuits originating from the caudate tail (CDt) send signals to the superior colliculus (SC) through the caudal-dorsal-lateral substantia nigra pars reticulata (cdlSNr) and/or the caudal-ventral globus pallidus externus (cvGPe) (23)(24)(25). These areas have two key features: high-capacity/long-term value memory and peripheral vision.…”