Dark-habituation increases the dark-background-contingent upshift of gaze in macaque monkeys.

What is the effect of prior experience on sensorimotor behavior? We studied the following intriguing behavior: monkeys fixating a small target direct their gaze above the target if the background is dark. Fixating a target once on a bright background, then on a dark background, yields 2 gaze directions, typically one above the other; hence the name, 'dark-background-contingent upshift of gaze', which is abbreviated as 'upshift'. Is the upshift only an attempt to avoid using the fovea in the dark? If it is, we might expect to also observe a downshift and a sideshift. We studied gaze direction in a large group of 10 rhesus monkeys from Tübingen, to which we added published data from 4 cynomolgus monkeys from Rehovot. The upshift was ubiquitous, and there was no systematic sideshift. What is the function of the upshift? Is it related to vision in the dark? Here, we concentrate on the effect of the monkeys' previous training. Seven of the 14 monkeys were accustomed to working in the dark ('dark-habituated'), while the other 7 had worked in bright ambient light ('bright-habituated'). The main result of this study is that the dark-habituated monkeys had a much larger upshift: the mean upshift was 2.2° in the dark-habituated monkeys, versus 0.5° in the bright-habituated. Thus, the upshift depends on habituation; the size of the upshift reflects months-long cumulative experience. These findings suggest that the function of the upshift is indeed related to seeing in the dark.

Persistence of the dark-background-contingent gaze upshift during visual fixations of rhesus monkeys.

During visual fixations, the eyes are directed so that the image of the target (object of interest) falls on the fovea. An exception to this rule was described in macaque monkeys (though not in humans): dark background induces a gaze shift upwards, sometimes large enough to shift the target's image off the fovea. In this article we address an aspect not previously rigorously studied, the time course of the upshift. The time course is critical for determining whether the upshift is indeed an attribute of visual fixation or, alternatively, of saccades that precede the fixation. These alternatives lead to contrasting predictions regarding the time course of the upshift (durable if the upshift is an attribute of fixation, transient if caused by saccades). We studied visual fixations with dark and bright background in three monkeys. We confined ourselves to a single upshift-inducing session in each monkey so as not to study changes in the upshift caused by training. Already at their first sessions, all monkeys showed clear upshift. During the first 0.5 s after the eye reached the vicinity of the target, the upshift was on average larger, but also more variable, than later in the trial; this initial high value 1) strongly depended on target location and was maximal at locations high on the screen, and 2) appears to reflect mostly the intervals between the primary and correction saccades. Subsequently, the upshift stabilized and remained constant, well above zero, throughout the 2-s fixation interval. Thus there is a persistent background-contingent upshift genuinely of visual fixation.