Dissociation of visual localization and visual detection in rhesus monkeys (Macaca mulatta)

Abstract

Conscious and unconscious cognitive processes contribute independently to human behavior and can be dissociated. For example, humans report failing to see objects clearly in the periphery while simultaneously being able to grasp those objects accurately (Milner in Proc R Soc B Biol Sci 279:2289-2298, 2012). Knowing whether similar dissociations are present in nonverbal species is critical to our understanding of comparative psychology and the evolution of brains. However, such dissociations are difficult to detect in nonhumans because verbal reports of experience are the main way we discriminate putative conscious from unconscious processing. We trained monkeys in a localization task in which they responded to the location where a target appeared, and a matched detection task in which they reported the presence or absence of the same target. We used masking to manipulate the visibility of targets. Accuracy was high in both tasks when stimuli were unmasked and was attenuated by visual masking. At the strongest level of masking, performance in the detection task was at chance, while localization remained significantly above chance. Critically, errors in the detection task were predominantly misses, indicating that the monkeys' behavior remained under stimulus control, but that the monkeys did not detect the target despite above-chance localization. While these results cannot establish the existence of phenomenal vision in monkeys, the dissociation of visually guided action from detection parallels the dissociation of conscious and unconscious vision seen in humans.

Fig. 1

The presentation sequence in the localization experiment. Trials were initiated by touching the green square, followed by a delay of 500 ms. Then, a target stimulus appeared in one of the four corners, followed by the four annuli that served as both masks and response buttons. The targets and masks were positioned such that they would share their outer and inner contours. Trials were separated by intertrial intervals (ITIs) of 5,000 ms (color figure online)

Fig. 2

Localization accuracy decreased as a function of shortened SOAs. Error bars are one standard error of the mean. For all SOAs, performance was above chance (dashed line)

Fig. 3

The presentation sequence for the detection task. In this example, a target is shown, although this was the case on only half of trials. A green response button and a red response button were used to report presence or absence of the target, respectively. The green and red response buttons were always placed between two adjacent masks (i.e., left-middle, right-middle, top-center, bottom-center) and were placed pseudorandomly such that each appeared equally often in each of the four possible locations (color figure online)

Fig. 4

Detection accuracy, expressed as d′, as a function of SOA. Accuracy was lower at shorter SOAs, and at chance at the 16.7 ms SOA (d′ = −0.06). Error bars are one standard error of the mean

Fig. 5

Proportions of false alarms (trials on which monkeys reported “there” when no target had appeared) and misses (trials on which monkeys reported “not-there” when a target had appeared) at the tested SOAs. Error bars represent one standard error of the mean. The proportion of misses increased as a function of shorter SOAs, whereas the proportion of false alarms was not related to SOA