The Primate Striatum: Neuronal Activity in Relation to Spatial Attention Versus Motor Preparation

Abstract

The primate basal ganglia are known to be involved in the initiation and control of visually guided movements. However, the precise role of these structures is not clear, partly because most neurophysiological studies have not dissociated neuronal activity related to visuomotor processing from that reflecting other aspects of behaviour, such as shifts of spatial attention. Moreover, the way the basal ganglia function together with the frontal cortex during movement initiation and execution is still a matter of debate. In an effort to clarify these issues, we recorded single neurons from the striatum (caudate nucleus and putamen) in two rhesus monkeys trained to perform a conditional visuomotor task, and compared their properties with those of the frontal cortex. The experimental paradigm was designed to distinguish neuronal activity associated with shifts of attention from that reflecting motor preparation. In a given trial, an identical visual stimulus could serve as a cue for the reorientation of spatial attention or as a cue for establishing a motor set depending on when it occurred during that trial. Additional aspects of the paradigm were designed to identify neurons whose activity differed when various stimulus configurations instructed the same action (stimulus effect), as well as neurons whose activity differed when two different actions were instructed by the same stimulus (movement effect). The majority of cells (60%) were preferentially active after instructional cues, 38% discharged preferentially after attentional cues, and the remaining 2% of cells discharged equally after both types of cue. Neurons active after instructional cues were further analysed for stimulus and movement effects. During movement preparation, the activity of the vast majority of striatal cells (putamen, 81%; caudate, 76%) varied significantly when different stimuli instructed the same action. Likewise, when different movements were instructed by the same stimulus, preparatory activity of a majority of cells (putamen, 92%; caudate, 82%) changed. Consequently, a substantial proportion of cells showed combined stimulus and movement effects. Comparison of these neuronal properties with those of the dorsal premotor cortex showed significantly higher proportions of cells in the striatum whose activity reflected sensory or sensorimotor processing. These results suggest that the basal ganglia are involved in shifting attentional set and in high-order processes of movement initiation, including the linking of sensory information with behavioural responses.