An oculomotor continuum from exploration to fixation

Abstract

During visual exploration, saccadic eye movements scan the scene for objects of interest. During attempted fixation, the eyes are relatively still but often produce microsaccades. Saccadic rates during exploration are higher than those of microsaccades during fixation, reinforcing the classic view that exploration and fixation are two distinct oculomotor behaviors. An alternative model is that fixation and exploration are not dichotomous, but are instead two extremes of a functional continuum. Here, we measured the eye movements of human observers as they either fixed their gaze on a small spot or scanned natural scenes of varying sizes. As scene size diminished, so did saccade rates, until they were continuous with microsaccadic rates during fixation. Other saccadic properties varied as function of image size as well, forming a continuum with microsaccadic parameters during fixation. This saccadic continuum extended to nonrestrictive, ecological viewing conditions that allowed all types of saccades and fixation positions. Eye movement simulations moreover showed that a single model of oculomotor behavior can explain the saccadic continuum from exploration to fixation, for images of all sizes. These findings challenge the view that exploration and fixation are dichotomous, suggesting instead that visual fixation is functionally equivalent to visual exploration on a spatially focused scale.

Fig. 1.

A saccadic continuum from exploration to fixation. (Upper) Average saccade rates for the different experimental conditions. Error bars represent SEM across subjects. (Lower) Examples of Natural Scene and Blank Scene stimuli, proportionally scaled down from the sizes presented in the experiment.

Fig. 2.

The saccadic continuum from exploration to fixation extends to saccade magnitude, peak velocity, intersaccadic interval, and direction. (A–D) Saccadic parameters in relation to scene size. (Upper) Distributions of saccadic parameters do not change in shape with decreasing image sizes, but merely shift continuously. Data from the Natural Scene condition (plots) and Blank Scene condition were equivalent. (Lower) Average saccadic parameters during fixation were indistinguishable from those during free-viewing of the smallest scene (t test P values indicated below each plot). Free-viewing regression slopes were significantly different from zero for each saccadic parameter (correlation coefficients and P values for the regression of the parameter and the logarithm of stimulus size indicated below each plot). Error bars represent SEM across subjects.

Fig. 3.

Empirical and simulated saccade magnitude distributions. Dashed lines show the empirical distributions (same data as in Fig. 2A) and solid lines the simulated ones. Distributions are normalized by the maximum value to facilitate direct comparison.

Fig. 4.

Spatial frequency content does not explain decreased saccade magnitudes for natural scenes of diminishing sizes. (A) Each gray line represents the spatial frequency spectrum (rotational average) of each natural scene at the largest size (32°). Color lines indicate the average of the spectrum of all of the images at four different sizes (32°, 16°, 8°, and 4°). The effect of stimulus size on the slope of the spectra is noticeable. The slope variability at the highest stimulus size (32°) encompasses the average slopes from stimuli sizes 4–32°. (B) Images were sorted by spectrum slope (high, middle, and low) and then divided in three groups of 28 images each. Saccade magnitude changes with stimulus size at all spatial frequencies, but it does not change with spatial frequency for any image size. The smallest image sizes (2°, 1°, and 0.5°) were not included in this analysis due to the difficulty of calculating the corresponding spectra. Error bars represent SEM across subjects.

Fig. 5.

The saccadic continuum extends to nonrestrictive viewing conditions. (A) Seven adjacent monitors formed a very wide screen display, encompassing nearly all of a subject’s visual field. (B) Saccadic rate continuum from exploration to fixation. Error bars represent SEM across subjects. (C) Saccadic magnitude continuum from exploration to fixation. (D) Comparison of saccadic rates (Upper) and magnitudes (Lower) in experiments 1 and 2. Different sets of subjects participated in experiments 1 and 2. Some methodological aspects moreover differed between the two experiments, such as the type of display (see Materials and Methods for details). Thus, to compare the shape of the curves from the two experiments, we normalized the data from experiment 2 using experiment 1 as reference (i.e., we subtracted a constant value from all of the data points from experiment 2, so that the average saccadic rates or magnitudes corresponding to the four common image sizes tested in the two experiments were equivalent). Both experiments produced the same saccadic continuum from fixation to exploration, although experiment 2 had an expanded range.