NEURAL RESPONSES RELATED TO SMOOTH-PURSUIT EYE-MOVEMENTS AND THEIR CORRESPONDENCE WITH ELECTRICALLY ELICITED SMOOTH EYE-MOVEMENTS IN THE PRIMATE FRONTAL EYE FIELD

1. Intracortical microstimulation of a portion of the monkey frontal eye field (FEF) lying in the floor and posterior bank of the arcuate sulcus evokes smooth, rather than saccadic eye movements. To further explore this region's involvement in pursuit, we recorded from FEF neurons in the vicinity of sites from which smooth eye movements (SEMs) were elicited electrically and studied their responses during smooth-pursuit and saccadic tasks. In this report, we describe the neurons' responses during visually guided smooth pursuit and compare their locations and response properties with those of elicited SEMs. 2. One hundred and ninety-three neurons, recorded from the FEF region in six hemispheres of three rhesus monkeys, were classified as ''pursuit neurons''. These neurons responded during smooth-pursuit tracking of moving visual stimuli but had no, or only minimal, responses in conjunction with visually guided saccades. Pursuit neurons were located in a small region of the arcuate fundus and posterior bank that overlapped, and extended slightly beyond, the region from which SEMs were elicited with microstimulation. 3. All pursuit neurons had a preferred pursuit direction, and all directions were represented with no strong bias toward ipsilateral, contralateral, up, or down. The directional tuning of 80 pursuit cells was measured quantitatively by testing pursuit in several directions and fitting the responses to a Gaussian function. Tuning indices (the sigma parameter of the Gaussian fit) varied between 13 degrees and 136 degrees. The median tuning index, 44.5 degrees, corresponds to a full width at half maximum of 105 degrees. The ubiquity of selectivity for pursuit direction and the wide distribution of preferred directions indicates that pursuit direction uses a place-code type of representation in FEF; however, the broad directional tuning of most neurons suggests that pursuit direction is given by a weighted average of optimal directions across the population of pursuit neurons active at any given time. 4. In general, the responses of pursuit neurons increased with pursuit velocity. Of 13 neurons formally tested with 2 s of constant-velocity tracking in their preferred direction across a range of target speeds, pursuit velocity sensitivity ranged from 0.24 to 1.42 spikes.s(-1).deg(-1).s(-1), with an average sensitivity of 0.70. This relationship suggests that pursuit neurons represent pursuit magnitude using a rate code; this parallels our previous observation that at most SEM sites, the velocity and acceleration of the electrically elicited eye movements increased as a function of the stimulation current. 5. Pursuit responses began at a median latency of 103 ms (n = 69) after target motion began. When latencies were computed relative to the initiation of smooth pursuit, the majority (61%) discharged before pursuit in their preferred direction and the median relative latency was -19 ms (with negative meaning that the discharge preceded pursuit). Thus significant FEF activity could contribute to the early stages of pursuit initiation, consistent with the previous observation that FEF stimulation elicits SEMs from stationary fixation. 6. We recorded pursuit responses and subsequently tested microstimulation at 113 sites. Of these, the electrical stimulation yielded SEMs at 27, saccades at 12, and no eye movements at the remaining 74 sites. The response latencies of neurons at SEM sites did not differ from those at sites yielding no elicited eye movements; however, SEMs were elicited more often from sites where neurons preferred pursuit directed ipsilateral to the recording hemisphere, relative to those with contralateral preferred directions. 7. The direction of elicited SEMs were correlated with the best tracking direction of neurons recorded at the SEM site (r(+) = 0.71). Despite this highly significant overall correlation, however, elicited SEM direction varied by similar to 40 degrees, on average, from the best pursuit direction of the neuron. This discrepancy may reflect the broad directional tuning of pursuit neurons and the relatively large currents, 50-100 mu A, that were often used to obtain these elicited SEMs. 8. The correspondence between the location and direction preferences of pursuit neurons and those of elicited SEMs, as well as the short latencies of the pursuit responses, suggest that FEF pursuit neurons participate in the generation of pursuit eye movements and that microstimulation of this region elicits SEMs by activating these pursuit neurons, and hence their projections to other parts of the smooth pursuit system.