Neural Activity in the Macaque Putamen Associated with Saccades and Behavioral Outcome

Abstract

It is now widely accepted that the basal ganglia nuclei form segregated, parallel loops with neocortical areas. The prevalent view is that the putamen is part of the motor loop, which receives inputs from sensorimotor areas, whereas the caudate, which receives inputs from frontal cortical eye fields and projects via the substantia nigra pars reticulata to the superior colliculus, belongs to the oculomotor loop. Tracer studies in monkeys and functional neuroimaging studies in human subjects, however, also suggest a potential role for the putamen in oculomotor control. To investigate the role of the putamen in saccadic eye movements, we recorded single neuron activity in the caudal putamen of two rhesus monkeys while they alternated between short blocks of pro- and anti-saccades. In each trial, the instruction cue was provided after the onset of the peripheral stimulus, thus the monkeys could either generate an immediate response to the stimulus based on the internal representation of the rule from the previous trial, or alternatively, could await the visual rule-instruction cue to guide their saccadic response. We found that a subset of putamen neurons showed saccade-related activity, that the preparatory mode (internally- versus externally-cued) influenced the expression of task-selectivity in roughly one third of the task-modulated neurons, and further that a large proportion of neurons encoded the outcome of the saccade. These results suggest that the caudal putamen may be part of the neural network for goal-directed saccades, wherein the monitoring of saccadic eye movements, context and performance feedback may be processed together to ensure optimal behavioural performance and outcomes are achieved during ongoing behaviour.