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

Neuron. 2017 May 17;94(4):920-930.e3. doi: 10.1016/j.neuron.2017.04.033.


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.

Keywords: Basal ganglia; Decision-making; Direct pathway; Globus pallidus external segment; Indirect pathway; Long-term memory; Macaque monkey; Reward value; Striatum; Visual object.

MeSH terms

  • Animals
  • Basal Ganglia
  • Caudate Nucleus / physiology*
  • Choice Behavior
  • Globus Pallidus / physiology*
  • Macaca mulatta
  • Neostriatum / physiology
  • Neural Inhibition / physiology*
  • Neural Pathways / physiology
  • Pars Reticulata / physiology*
  • Reward
  • Saccades / physiology*
  • Superior Colliculi / physiology*