Two-Dimensional Saccade-Related Population Activity in Superior Colliculus in Monkey

Abstract

Anderson, Russell W., Edward L. Keller, Neeraj J. Gandhi, and Sanjoy Das. Two-dimensional saccade-related population activity in superior colliculus in monkey. J. Neurophysiol. 80: 798–817, 1998. The two-dimensional distribution of population activity in the superior colliculus (SC) during saccadic eye movements in the monkey was estimated using radial basis functions. To make these ensemble activity estimates, cells in the deeper layers of the SC were recorded over much of the rostrocaudal (caudal to 3.8 mm from the rostral tip), mediolateral extent of this structure. The dynamic movement field of each cell was determined at 2-ms intervals around the time of saccades for a wide variety of horizontal and oblique movements. Collicular neurons were divided into partially overlapping dorsal and ventral cell layers on the basis of recorded depth in SC. The pattern of presaccadic activity was used as an additional discriminant to sort the cells in the two layers into separate burst (dorsal) and buildup (ventral) cell classes. Rostrocaudal and medioventral cell location on the colliculus was estimated from the optimal target vector for a cell's visual response rather than from the optimal motor vector. The former technique was more reliable for locating some buildup neurons because it produced locations that compared better with the locations suggested by electrical stimulation. From the movement field data and from the estimates of each cell's anatomic location, a similar algorithm was used to compute the two-dimensional population activity in the two layers of the SC during horizontal and oblique saccades. A subset of the sample of neurons, located near the horizontal meridian of the SC, first was used to compute one-dimensional dynamic population activity estimates for horizontal saccades to allow partial comparison to previous studies. Statistical analyses on the one-dimensional data were limited to saccades of ≤20°. The analyses indicated that while there was a small rostrally directed shift in the center of gravity of the distributed activity in the buildup cell layer, there was little support for the theory of a systematic rostrally directed spread of the leading edge of the activity. The two-dimensional results extend the previous one-dimensional estimates of collicular activity during saccades. Discharge in the burst layer was invariant in size for all saccade vectors and symmetrically arranged about a center of gravity that did not move during saccades. The size of the active area in the buildup layer grew modestly with saccade amplitude, whereas the distribution of activity was skewed toward the rostral end of the SC for saccades larger than 10°. There was a small, but consistent shift in the center of gravity of the two-dimensional activity that was directed along the horizontal meridian (for horizontal movements) or an oblique meridian (for oblique movements) of the SC. However, the spread of activity during a saccade was as large or larger in the mediolateral direction as it was in the rostral direction. The results indicate that changes in activity occur in an extended zone on the SC, and in all directions but caudal, in the buildup layer during saccades and do not support the idea of a rostrally directed spread of activity as a dynamic control mechanism for saccades. Our results and those of previous investigators of collicular population activity may be limited by stationarity concerns in that the cells used to estimate population activity were recorded in several monkeys over an extended period of time to obtain a sufficient spatial sample.