Serial processing in scotopic vision: from upshift to the scotopic band

Abstract

It has been known for decades that haplorrhine primates and other non-mammalian foveate vertebrates explore visual scenes by making fast eye movements that allow them to shift the image of an object of interest into the fovea. High spatial resolution accommodated by the fovea can be used to scrutinize the object of interest during a period of steady foveal fixation of the object’s image, interrupted only briefly by different types of miniature eye movements, too small to jeopardize the image position within the confines of the fovea. In this dissertation I address a peculiar aspect of the object fixation of macaque monkeys observed under conditions of full darkness. Macaque monkeys exhibit an upward shift of gaze (for short, ‘upshift’) when asked to fixate a tiny fixation spot in an otherwise dark environment. Given the advantages of foveal vision, the upshift that moves the fovea away from the object of interest, the fixation point, must appear paradoxical. The upshift was first described by Snodderly (1987) in rhesus monkeys and rediscovered and investigated in detail by Barash et al. (1998) who studied it in cynomolgus macaques. Barash et al. (1998) demonstrated that the upshift depended solely on the background luminance and not on the contrast between target and background. Barash and coworkers could also show that the upshift increased with training on the fixation and typically started within seconds after turning the background from bright to dark. The view that the upshift was a hitherto undescribed illumination-dependent fixation offset not related to known features of the systems controlling saccades and fixation, was put into a question by Goffart et al. (2006). This group claimed that the upshift is nothing but a luminance dependent disbalance of the saccadic system for the vertical. However, based on this hypothesis, the upshift should be abolished soon after the onset of fixation. To critically test this hypothesis, we carried out a first study in which we trained rhesus monkeys to fixate small targets on the screen. The monkeys fixated a target in two conditions: with bright or dark background. We investigated the time course of the difference between fixation in darkness and fixation in bright conditions that is the actual upshift. We showed that dark-background-dependent upshift persisted during at least during two seconds of fixation. Additionally, the size of the upshift depended on fixation location: fixation in the lower visual field resulted in larger upshifts whereas fixation in the upper visual field demonstrated smaller upshifts. These results clearly indicated that the upshift cannot merely be a consequence of a dysbalanced saccadic system causing hypermetric upward and hypometric downward saccades as both should be corrected within a few milliseconds, ultimately establishing foveal fixation. Anecdotal observations seemed to suggest that the upshift might differ between monkeys. In an attempt to consolidate this impression and, moreover, to identify a cause explaining eventual differences, we embarked on study of a very large sample of 14 monkeys from two species. We tested the monkeys in the same task that we had used in the preceding study. The results were very clear: all monkeys in our sample had upshift and the monkeys lacked systematic horizontal deviation during fixation in darkness. However, the monkeys tested exhibited substantial differences as to the size of the upshift. The monkeys in our large sample differed by the level of ‘habituation’: dark habituated (monkeys that had been previously trained in tasks in full darkness with small bright stimuli) and bright-habituated (monkeys that had been trained in tasks with large bright stimuli without control for full darkness of experimental setup). We showed that the size of the upshift largely reflects the extent to which a monkey is habituated to work in the dark. Dark habituated monkeys with mostly belonged to 2 the group with higher upshift whereas bright habituated monkeys were very likely to demonstrate lower upshift. Species differences (cynomolgus vs. rhesus macaques) were not found. In seeking to explain the upshift, we resorted to the geometry of the rod and cone densities, which constitute a hard bound for the resolution of the percept. Cones peak in the fovea; extrafoveally, cone density decreases as eccentricity increases. Rods are absent in the foveola. On going dorsally from the foveola, rod density increases, until reaching a peak in a location called dorsal rod peak, or rod hotspot (Packer et al., 1989; Wickler and Rakic, 1990; Wickler et al., 1990). We therefore started with the hypothesis that if any retinal location replaces the fovea in scotopic vision, it would be the rod hotspot. We therefore expected that the vertical component of the line of gaze would be distributed bimodally, one mode reflecting the fovea and the other the rod hotspot. However, the results did not corroborate this hypothesis. Upshift height varied a lot, from monkey to monkey, from condition to condition, even within session. Eventually we were led to an alternative hypothesis, that of a scotopic band. We now suggest that at any epoch during scotopic vision there might be a scotopic center, located dorsally to the fovea. The scotopic center replaces the fovea. During fixations, target images are projected on the scotopic center, not on the fovea. Saccadic trajectories show that saccades shift the target’s image directly to the scotopic center. Therefore, not all saccades foveate. Scotopic saccades do not foveate. The relative weight of the scotopic center in the evolution of saccades remains open. In any case, scotopic saccades come with their own sensorimotor transformations, as do scotopic fixations. Scotopic center is only the beginning of the scotopic analogy for high-acuity vision. Unlike the close, tight fovea of photopic vision, the scotopic center moves along a line extending dorsally from immediately dorsal to the fovea. We call this the scotopic band. The presence of the band makes scotopic sensorimotor transformations more complex than photopic because they rely on a parameter – the scotopic band setting, the current location of the scotopic center on the band. Scotopic band is set primarily according to the ambient light, reflected in the laboratory as background luminance. Increasing luminance results in lower upshift, or, equivalently, more ventral setting. However, other factors heavily influence the scotopic setting too. To mention but 2: habituation to darkness increases the upshift, that is, makes the setting more dorsal; and so do also threshold task conditions. Thus, we suggest that ultimately, the scotopic band setting reflects the statistics of the scene and the monkey’s task. The computational needs change gradually, and so do the anatomy (and physiology). Therefore, scotopic band setting is not limited to the two endpoints but occupy the points in between.