Attention-related modulation of caudate neurons depends on superior colliculus activity

Recent work has implicated the primate basal ganglia in visual perception and attention, in addition to their traditional role in motor control. The basal ganglia, especially the caudate nucleus ‘head’ (CDh) of the striatum, receive indirect anatomical connections from the superior colliculus (SC), a midbrain structure that is known to play a crucial role in the control of visual attention. To test the possible functional relationship between these subcortical structures, we recorded CDh neuronal activity of macaque monkeys before and during unilateral SC inactivation in a spatial attention task. SC inactivation significantly altered the attention-related modulation of CDh neurons and strongly impaired the classification of task-epochs based on CDh activity. Only inactivation of SC on the same side of the brain as recorded CDh neurons, not the opposite side, had these effects. These results demonstrate a novel interaction between SC activity and attention-related visual processing in the basal ganglia.