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

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 of caudate tail encode object values in opposite manners•They both control saccades by sending opposite value signals to superior colliculus•Both value signals are mediated by serial point-to-point inhibitory connections•These pathways together can guide good object choice and bad object rejection Kim et al. found a selective role of the indirect pathway in automatic saccades to visual objects. The pathway, originating from the caudate tail, selectively sends stable value information to the superior colliculus, thus suppressing saccades to historically bad objects.