Modulation of presaccadic activity in the frontal eye field by the superior colliculus

Abstract

A cascade of neuronal signals precedes each saccadic eye movement to targets in the visual scene. In the cerebral cortex, this neuronal processing culminates in the frontal eye field (FEF), where neurons have bursts of activity before the saccade. This presaccadic activity is typically considered to drive downstream activity in the intermediate layers of the superior colliculus (SC), which receives direct projections from FEF. Consequently, the FEF activity is thought to be determined solely by earlier cortical processing and unaffected by activity in the SC. Recent evidence of an ascending path from the SC to FEF raises the possibility, however, that presaccadic activity in the FEF may also depend on input from the SC. Here we tested this possibility by recording from single FEF neurons during the reversible inactivation of SC. Our results indicate that presaccadic activity in the FEF does not require SC input: we never observed a significant reduction in FEF presaccadic activity when the SC was inactivated. Unexpectedly, in a third of experiments, SC inactivation elicited a significant increase in FEF presaccadic activity. The passive visual response of FEF neurons, in contrast, was virtually unaffected by inactivation of the SC. These findings show that presaccadic activity in the FEF does not originate in the SC but nevertheless may be influenced by modulatory signals ascending from the SC.

FIG. 1.

Example of saccade changes during superior colliculus (SC) inactivation. A: saccade velocities show that the SC deficit field overlaps the frontal eye field (FEF) visuomovement field. Top left inset: the visuomovement field (dotted circle) of the FEF neuron in this experiment, which had presaccadic activity for saccades made from central fixation (crosshair) to each of 5 possible target locations (white circles). For this experiment, the center target was 5° below and 20° to the left of fixation. The other targets were 10° from the center target. The expanded view (large dotted circle) shows the peak eye velocity in degrees per second (y axis) for saccades to each target, plotted as a function of time (x axis). Time zero indicates the beginning of the lidocaine injection. Red lines indicate the beginning and end of the deficit period for each location (see methods). For this experiment, eye velocities were significantly lower during the deficit period than during the preinjection period at all target locations, and the center location was chosen for neuronal analysis due to its strongest presaccadic activity. B: eye movement trajectories from the same example experiment show that the monkey can still make saccades. Trajectories for all locations are shown for the three analysis periods: preinjection, deficit, and recovery. x and y axes represent the horizontal and vertical eye positions in degrees of visual angle.

FIG. 2.

Presaccadic activity in FEF during SC inactivation. A: population spike density plot for all FEF neurons with presaccadic activity (n = 15) shows that activity does not decrease during the deficit period (red line) compared with the preinjection period (blue line). FEF activity in spikes per second (y axis) is shown as a function of time (x axis), aligned on the beginning of the saccadic eye movement (time 0). Thin lines represent standard error. The shaded box indicates the presaccadic epoch used for computing average firing rates in B. B: each dot represents average presaccadic activity in a single experiment for the deficit period (y axis) plotted against the preinjection period (x axis). Solid dots indicate experiments with a significant difference between the 2 periods. C: presaccadic activity of an example neuron with a significant increase in activity during the deficit period compared with both preinjection and recovery periods. Conventions as in A. D: relationship between the inactivation-induced change in FEF activity and the alignment of spatial representations in FEF and SC. Each dot is from a single experiment. The x axis shows the distance in millimeters on the SC map between the SC injection site and the SC site that corresponds to the FEF representation. The y axis shows the percentage change in presaccadic activity during the deficit period compared with the preinjection period. The dashed horizontal line indicates no change in activity during deficit compared with preinjection.

FIG. 3.

Visual activity in FEF during SC inactivation. A: population spike density plot for all FEF neurons with a visual response (n = 8) shows that activity is not strongly modulated during the deficit period (red line) compared with the preinjection period (blue line). B: each dot represents average visual activity in a single experiment for the deficit period (y axis) plotted against the preinjection period (x axis). Conventions for each panel as in Fig. 2.