The basal ganglia are critical for motor behavior, and a well-known deficit of basal ganglia disorders is the loss of voluntary control over movements. Many studies on the role of basal ganglia in saccadic eye movements have focused on the caudate and substantia nigra pars reticulata (SNr). It has remained unclear, however, whether neurons in other nuclei of the basal ganglia are active during oculomotor behavior and, if they are, whether their activity is preferential for voluntary saccades. We ventured beyond the caudate-SNr pathway to study the globus pallidus externa (GPe) and interna (GPi).

First we recorded from neurons in GPe and GPi (and for comparison, in SNr) in monkeys that made memory-guided saccades. Neurons in all three structures had activity synchronized with saccade generation, visual stimulation, or reward. GPe activity was strongly visual-related while GPi activity was more reward-related. The distribution of signals in GPe, but not GPi, resembled that found in SNr. Response fields of neurons in all three structures were more spatially tuned early in trials (during visual and saccadic events) than later in trials (during reward).

In our second study, we examined whether saccade-related activity in GPe and GPi was preferentially active for voluntary saccades as defined in two ways: made in the absence of visual stimulation and made in the absence of instructions. We designed tasks that covered all four permutations of presence or absence of visual stimulation and instruction, and analyzed neuronal activity associated with the same vectors of saccades across all the tasks. For about half of the saccade-related neurons in all three structures, saccade-related activity varied with task context. The most prominent factor accounting for differential saccade-related activity was instructional context. Surprisingly, we found higher activity for instructed saccades. Preferential activity for non-instructed (highly voluntary) tasks was rare in individual neurons and absent at the population level.

We conclude that GPe and GPi, in addition to SNr, may contribute to oculomotor behavior, and that none of these structures are preferentially active for voluntary saccades. Both of these results provide new views on the role of basal ganglia in eye movements.