Presetting Basal Ganglia for Volitional Actions

The basal ganglia (BG) have been considered as a key structure for volitional action preparation. Neurons in the striatum, the main BG input stage, increase activity gradually before volitional action initiation. However, because of the diversity of striatal motor commands, such as automatic (sensory driven) and volitional (internally driven) actions, it is still unclear whether an appropriate set of neurons encoding volitional actions are activated selectively for volitional action preparation. Here, using the antisaccade paradigm (look away from a visual stimulus), we dissociated neurons in the caudate nucleus, the oculomotor striatum, encoding predominantly automatic saccades toward the stimulus and volitional saccades in the opposite direction of the stimulus in monkeys. We found that before actual saccade directions were defined by visual stimulus appearance, neurons encoding volitional saccades increased activity with elapsed time from fixation initiation and by a temporal gap between fixation point disappearance and stimulus appearance. Their activity was further enhanced by an antisaccade instruction and correlated with antisaccade behavior. Neurons encoding automatic saccades also increased activity with elapsed time from fixation initiation and by a fixation gap. However, the activity of this type of neuron was not enhanced by an antisaccade instruction nor correlated with antisaccade behavior. We conclude that caudate neurons integrate nonspatial signals, such as elapsed time from fixation initiation, fixation gap, and task instructions, to preset BG circuits in favor of volitional actions to compete against automatic actions even before automatic and volitional commands are programmed with spatial information.