Macaque Dorsolateral Prefrontal Cortex Does not Suppress Saccade-Related Activity in the Superior Colliculus

Of the many functions ascribed to the dorsolateral prefrontal cortex (DLPFC), the ability to override automatic stimulus-driven behavior is one of the most prominent. This ability has been investigated extensively with the antisaccade task, which requires suppression of saccades toward suddenly appearing visual stimuli. Convergent lines of evidence have supported a model in which the DLPFC suppresses unwanted saccades by inhibiting saccade-related activity in the ipsilateral superior colliculus (SC), a midbrain oculomotor structure. Here, we carried out a direct test of this inhibitory model using unilateral cryogenic deactivation of the DLPFC within the caudal principal sulcus (cPS) and simultaneous single-neuron recording of SC saccade-related neurons in monkeys performing saccades and antisaccades. Contrary to the inhibition model, which predicts that attenuation of inhibition effected by unilateral cPS deactivation should result in activity increases in ipsilateral and decreases in contralateral SC, we observed a delayed onset of saccade-related activity in the ipsilateral SC, and activity increases in the contralateral SC. These effects were mirrored by increased error rates of ipsiversive antisaccades, and reaction times of contraversive saccades. These data challenge the inhibitory model and suggest instead that the primary influence of the DLPFC on the SC is excitatory.