Saccadic probability influences motor preparation signals and time to saccadic initiation

Abstract

One must be prudent when selecting potential saccadic targets because the eyes can only move to one location at a time, yet movements must occur quickly enough to permit interaction with a rapidly changing world. This process of efficiently acquiring relevant targets may be aided by advanced planning of a movement toward an upcoming target whose location is gathered via environmental cues or situational experience. We studied how saccadic reaction times (SRTs) and early pretarget neuronal activity covaried as a function of saccadic probability. Monkeys performed a saccadic task in which the probability of the required saccade being directed into the response field of a neuron varied systematically between blocks of trials. We recorded simultaneously the early pretarget activity of saccade-related neurons in the intermediate layers of the superior colliculus. We found that, as the likelihood of the saccade being generated into the response field of the neuron increased, the level of neuronal activity preceding target presentation also increased. Our data suggest that this early activity codes motor preparation because its activity was related to not only the metrics but also the timing of the saccade, with 94% (29/31) of the neurons tested having significant negative correlations between discharge rate and SRT. This view is supported by cases in which exceptionally high levels of pretarget activity were associated with anticipatory saccades into the response field of a neuron that occurred in advance of the target being presented. This study demonstrates how situational experience can expedite motor behavior via the advanced preparation of motor programs.

Fig. 1.

A–D, The activity of a buildup neuron (si17) during the 50% ON (A), 50% OFF (B), 100% ON (C), and 100% OFF (D) saccadic probability conditions. Only trials in which saccades are target driven are shown (i.e., initiated between 70 and 300 msec and falling within the computer-controlled window). The individual rasters of neuronal discharge and the spike density function are aligned on both fixation point disappearance (left vertical line of eachpanel) and target appearance (right vertical line of each panel). For each condition, the first trial in the block is at the bottomof the raster plot, and the last trial in the block is at thetop. The shaded region 50–60 msec after target appearance represents the epoch in which discharge was sampled for subsequent analysis. E, Spike density functions of the same neuron superimposed for five saccadic probability conditions: 100% ON, 80% ON, 50% ON, 80% OFF, and 100% OFF.

Fig. 2.

A buildup neuron (sd67) with early, pretarget activity that occurs only when the required saccade was directed into the response field of the neuron was fully predictable (100% ON direction). The format is the same as that described in the Figure 1legend.

Fig. 3.

Comparison of discharge rates between different saccadic probability conditions. A–D, Eachpoint represents the mean of the discharge rate in the epoch from 50 to 60 msec after target presentation from the last 10 trials for a single neuron for the specified saccadic probability condition. The equality line (slope = 1) is shown in each scatter plot. E, The mean sample discharge rate (±SEM) for the sample of neurons in each saccadic probability condition is shown (paired t test, *p < 0.0001).

Fig. 4.

Comparison of SRTs between different saccadic probability conditions for the corresponding neurons and trials shown in Figure 3. The format is the same as that described in the Figure 3legend.

Fig. 5.

Cumulative distribution of anticipatory saccades during the saccadic probability blocks as a percentage of total trials. These saccades were elicited while recording from the population of neurons used in this study in which data for the 50 and 100% ON and the 100% OFF saccadic probability conditions were collected. Saccades were considered anticipations if they were directed toward the location of the eventual target (and also the mirror-image location for the 50% condition) and occurred 0–69 msec after target presentation.

Fig. 6.

Correlations between SRT and discharge rate of the two buildup neurons shown in Figures 1 (si17) and 2 (sd67). Each datapoint was collected from a single trial.A, B, Data in the ON direction were collected from the 50% (squares) and 100% (filled circles) ON conditions. C,D, Data in the OFF direction were collected from the 50% (squares) and 100% (filled circles) OFF conditions.

Fig. 7.

Correlation coefficient distributions of discharge rate versus SRT in the ON and OFF directions from the sample of buildup neurons. Discharge rates were sampled during a pretarget epoch (A, B; 50–60 msec after target presentation), a gap epoch (C, D; 0–10 msec before target presentation), and a fixation epoch (E, F; 0–10 msec before fixation point disappearance. Hatched bars represent statistically significant correlations (p < 0.01). Arrows depict the mean correlation coefficient for each condition.

Fig. 8.

A, C, Covariation of population discharge rate (A) and SRTs (C) during the evolution of blocks of trials in the different saccadic probability conditions. Each datapoint in A and Crepresents the mean discharge rate or mean SRT from 26 buildup neurons on successive correct trials. The gap between datapoints and splines along the x-axis represents switching saccadic probability blocks. Data for the ON direction are plotted as empty circles, and data for the OFF direction are plotted as filled circles. A spline function is fit through the data in each block of trials (de Boor, 1978). B, D, The correlation between mean discharge rate and mean SRT for the 26 neurons for successive trials in the ON (B) and OFF (D) directions for the combined 50% (squares) and 100% (filled circles) conditions.

Fig. 9.

Saccadic metrics and the corresponding activity of a buildup neuron for three types of saccades (anticipatory, express, and regular) in the 100% ON and 100% OFF conditions.A–L, Eye position was sampled at 500 Hz and plotted from 20 msec before saccade initiation to 20 msec after saccade end. The gray circle represents target location. Rasters and spike density functions are aligned on target presentation (solid vertical line). M,N, The spike density functions accompanying the three types of saccades are superimposed.

Fig. 10.

Comparison of the mean spike density functions of anticipatory, express, and regular saccades for the sample of 11 analyzed neurons aligned on target presentation (A) and saccade onset (B) during the 100% ON condition.