Activity of smooth pursuit-related neurons in the monkey periarcuate cortex during pursuit and passive whole-body rotation

Smooth pursuit and vestibularly induced eye movements interact to maintain the accuracy of eye movements in space (i.e., gaze). To understand the role played by the frontal eye fields in pursuit-vestibular interactions, we ex amined activity of 110 neurons in the periarcuate areas of head-stabilized Japanese monkeys during pursuit eye movements and passive whole-body rotati on. The majority (92%) responded with the peak of their modulation near pea k stimulus velocity during suppression of the vestibuloocular reflex (VOR) when the monkeys tracked a target that moved with the same amplitude and ph ase and in the same plane as the chair. We classified pursuit-related neuro ns (n = 100) as gaze velocity if their peak modulation occurred for eye (pu rsuit) and head (VOR suppression) movements in the same direction; the ampl itude of modulation during one less than twice that of the other; and modul ation was lower during target-stationary-in-space condition (VOR x1) than d uring VOR suppression. In addition, we examined responses during VOR enhanc ement (x2) in which the target moved with equal amplitude as, but opposite direction to, the chair. Gaze-velocity neurons responded maximally for oppo site directions during VOR x2 and suppression. Based on these criteria, the majority of pursuit-related neurons (66%) were classified as gaze-velocity with preferred directions uniformly distributed. Because the majority of t he remaining cells (32/34) also responded during VOR suppression, they were classified as eye/head-velocity neurons. Thirteen preferred pursuit and VO R suppression in the same direction; 13 in the opposite direction, and 6 sh owed biphasic modulation during VOR suppression. Eye- and gaze-velocity sen sitivity of the two groups of cells were similar; mean (+/- SD) was 0.53 +/ - 0.30 and 0.50 +/- 0.44 spikes/s per degrees/s, respectively. Gaze-velocit y (but not eye/head-velocity) neurons showed significant correlation betwee n eye- and gaze-velocity sensitivity, and both groups maintained their resp onses when the tracking target was extinguished briefly. The majority of pu r suit-related neurons (28/43 = about 65%) responded to chair rotation in c omplete darkness. When the monkeys fixated a stationary target, more than h alf of cells tested (21/40) discharged in proportion to the velocity of ret inal motion of a second laser spot (mean velocity sensitivity = 0.20 +/- 0. 16 spikes/s per degrees/s). Preferred directions of individual cells to the second spot were similar to those during pursuit. Visual responses to the second spot movement were maintained even when it was extinguished briefly. These results indicate that both retinal image- and gaze-velocity signals are carried by single periarcuate pursuit-related neurons, suggesting that these signals can provide target-velocity-in-space and gaze-velocity comman ds during pursuit-vestibular interactions.