Role of primate basal ganglia and frontal cortex in the internal generation of movements

Summary

The purpose of these studies was to investigate neuronal activity in the basal ganglia and frontal cortex in relation to the internal generation of goal-directed movements. Monkeys performed goal-directed arm movements at a self-chosen moment in the absence of phasic stimuli providing external temporal reference. They were rewarded with a small morsel of food for each movement, although automatic or repetitive behavior was not re-inforced. For reasons of comparison, animals were also trained in a delayed go no-go task in which visual cues instructed them to perform or refrain from an arm movement reaction to a subsequent trigger stimulus. This report describes the activity of neurons in the head of the caudate nucleus and rostral putamen preceding self-initiated arm movements and compares it with instruction-induced preparatory activity preceding movements in the delay task. A total of 497 caudate and 354 putamen neurons were tested in the delay task. Two types of preparatory activity were observed: (1) transient responses to the instruction cue, and (2) sustained activity preceding the trigger stimulus or movement onset. Transient responses were found in 48 caudate and 50 putamen neurons, occurring twice as often in movement (‘go’) as compared to no-movement (‘no-go’) trials, but rarely in both. These responses may code the information contained in the instruction relative to the forthcoming behavioral reaction. Sustained activity began after instruction onset and lasted until the trigger stimulus or the arm movement occurred, this being for periods of 2–7 s, 12–35 s, or up to 80 s, depending on the task requirements. This activity was seen in 47 caudate and 45 putamen neurons, was largely confined to go trials, and was unrelated to the preparation of saccadic eye movements. In some cases, this activity began as direct responses to the instruction stimulus, but in the majority of cases developed more gradually before the movement. Thus, both transient and sustained activations appear to be related to the preparation of movements. A total of 390 caudate and 293 putamen neurons were tested during self-initiated movements. Activity preceding earliest movement-related muscle activity was found in 32 caudate and 42 putamen neurons. This premovement activity began 0.5–5.0 s before movement onset (median 1160 ms), increased slowly, reached its peak close to movement onset, and subsided rapidly thereafter. It was unrelated to the preparation of saccadic eye movements. Comparisons between the two tasks were made on 53 neurons. Only one third of the task-related neurons showed premovement activity before both self-initiated and instructed movements, whereas in two thirds such activity was restricted to only one of the tasks. Peak premovement activity occurred significantly closer to movement onset with self-initiated as compared to instructed movements, whereas the magnitudes varied insignificantly. These data show that single neurons in caudate and putamen were activated up to a few seconds before self-initiated movements that were performed, within the constraints of the experimental situation, with a considerable degree of temporal choice due to the absence of explicit external instructive or imperative stimuli. Two thirds of these neurons were exclusively activated before self-initiated movements and not when the movement was prepared by explicit external cues. Thus, both caudate and putamen appear to be involved in setting and maintaining central preparatory states related to the internal generation of individual behavioral acts on the basis of information about the environmental situation (task contingencies, position of movement targets, and reward). Since comparable premovement activity occurs simultaneously in frontal cortical areas closely associated with striatum, neuronal processes underlying the internal generation of behavior may engage cortico-basal ganglia loops.