Indirect Pathway of Caudal Basal Ganglia for Rejection of Valueless Visual Objects

Abstract

Summary The striatum controls behavior in two ways: facilitation and suppression through the direct and indirect pathways respectively. However, it is still unclear what information is processed in these pathways. To address this question, we studied two pathways originating from the primate caudate tail (CDt). We found that the CDt innervated the caudal-dorsal-lateral part of the substantia nigra pars reticulata (cdlSNr), directly or indirectly through the caudal-ventral part of the globus pallidus externus (cvGPe). Notably, cvGPe neurons receiving inputs from the CDt were mostly visual neurons that encoded stable reward values of visual objects based on long-past experiences. Their dominant response was inhibition by valueless objects, which generated disinhibition of cdlSNr neurons and inhibition of superior colliculus neurons. Our data suggest that low-value signals are sent by the CDt-indirect pathway to suppress saccades to valueless objects, whereas high-value signals are sent by the CDt-direct pathway to facilitate saccades to valuable objects.

Direct and indirect pathways for choosing objects and actions

“…Anatomical studies showed that CDt projects to the cdlSNr and the caudal‐ventral GPe (cvGPe) and does so locally and densely (Saint‐Cyr et al ., ; Kim et al ., ). cvGPe then projects to cdlSNr locally and densely (Kim et al ., ). Electrophysiological studies confirmed that these connections are inhibitory: direct pathway (CDt‐cdlSNr; Yasuda & Hikosaka, ) and indirect pathway (CDt‐cvGPe, cvGPe‐cdlSNr; Kim et al ., ; Fig.…”

“…cvGPe then projects to cdlSNr locally and densely (Kim et al ., ). Electrophysiological studies confirmed that these connections are inhibitory: direct pathway (CDt‐cdlSNr; Yasuda & Hikosaka, ) and indirect pathway (CDt‐cvGPe, cvGPe‐cdlSNr; Kim et al ., ; Fig. ).…”

“…First, a majority of neurons in each region (CDt, cdlSNr, cvGPe) are visually sensitive, responding to many visual (fractal) objects selectively (selectivity higher in CDt than cdlSNr, cvGPe; Yamamoto et al ., ; Yasuda et al ., ; Kim & Hikosaka, ; Kim et al ., ). Furthermore, a majority of these neurons encode stable values based on long‐term object value memories (Kim & Hikosaka, ; Yamamoto et al ., ; Yasuda & Hikosaka, ; Kim et al ., ). These data detail the above statement: The direct and indirect pathways of CDt aim at saccadic eye movement based on the stable values of visual objects.…”

“…Overall, bad objects are encoded by the indirect pathway, whereas good objects are encoded by the direct pathway (Kim et al ., ). Typically, bad objects inhibit cvGPe neurons, disinhibit cdlSNr neurons and then inhibit SC neurons, thus suppressing saccades to the bad objects.…”

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

“…However, the direct and indirect pathways in “caudal basal ganglia” are still unclear. The caudal basal ganglia, which includes the caudate tail (CDt), the caudal‐dorsal‐lateral part of SNr (cdlSNr) and the caudal‐ventral part of GPe (cvGPe), are specifically involved in long‐term value coding of visual objects (i.e., stable value memory) for saccadic eye movements based on historical life experiences (Kim, Amita, & Hikosaka, ; Yamamoto, Kim, & Hikosaka, ; Yasuda, Yamamoto, & Hikosaka, ). Most neurons in CDt, cdlSNr and cvGPe discriminate visual objects based on their historical value: objects previously and consistently associated with a large reward (good objects) and objects associated with a small reward (bad objects) (Kim et al., ).…”