Pursuit-related neurons in the supplementary eye fields: discharge during pursuit and passive whole body rotation

The primate frontal cortex contains two areas related to smooth-pursuit: the frontal eye fields (FEFs) and supplementary eye fields (SEFs). To distinguish the specific role of the SEFs in pursuit, we examined discharge of a total of 89 pursuit-related neurons that showed consistent modulation when head-stabilized Japanese monkeys pursued a spot moving sinusoidally in fronto-parallel planes and/or in depth and with or without passive whole body rotation. During smooth-pursuit at different frequencies, 43% of the neurons tested (17/40) exhibited discharge amplitude of modulation linearly correlated with eye velocity. During cancellation of the vestibulo-ocular reflex and/or chair rotation in complete darkness, the majority of neurons tested (91% = 30/33) responded. However, only 17% of the responding neurons (4/30) were modulated in proportion to gaze (eye-in-space) velocity during pursuit-vestibular interactions. When the monkeys fixated a stationary spot, 20% of neurons tested (7/34) responded to motion of a second spot. Among the neurons tested for both smooth-pursuit and vergence tracking (n = 56), 27% (15/56) discharged during both, 62% (35/56) responded during smooth-pursuit only, and 11% (6/56) during vergence tracking only. Phase shifts (relative to stimulus velocity) of responding neurons during pursuit in frontal and depth planes and during chair rotation remained virtually constant (< or =1 Hz). These results, together with the robust vestibular-related discharge of most SEF neurons, show that the discharge of the majority of SEF pursuit-related neurons is quite distinct from that of caudal FEF neurons in identical task conditions, suggesting that the two areas are involved in different aspects of pursuit-vestibular interactions including predictive pursuit.