Lawful tracking of visual motion in humans, macaques, and marmosets in a naturalistic, continuous, and untrained behavioral context

Significance We characterize spatiotemporal integration of naturalistic, continuous visual motion of three primate species (humans, macaques, and marmosets). All three species volitionally, but naturally, track the center of expansion of a dynamic optic flow field. Detailed analysis of this flow-tracking behavior reveals lawful and repeatable dependencies of the behavior on nuances in the stimulus, revealing that even unconstrained and continuous behavior can exhibit the sort of precise dependencies typically studied only in artificial and constrained tasks. Much study of the visual system has focused on how humans and monkeys integrate moving stimuli over space and time. Such assessments of spatiotemporal integration provide fundamental grounding for the interpretation of neurophysiological data, as well as how the resulting neural signals support perceptual decisions and behavior. However, the insights supported by classical characterizations of integration performed in humans and rhesus monkeys are potentially limited with respect to both generality and detail: Standard tasks require extensive amounts of training, involve abstract stimulus–response mappings, and depend on combining data across many trials and/or sessions. It is thus of concern that the integration observed in classical tasks involves the recruitment of brain circuits that might not normally subsume natural behaviors, and that quantitative analyses have limited power for characterizing single-trial or single-session processes. Here we bridge these gaps by showing that three primate species (humans, macaques, and marmosets) track the focus of expansion of an optic flow field continuously and without substantial training. This flow-tracking behavior was volitional and reflected substantial temporal integration. Most strikingly, gaze patterns exhibited lawful and nuanced dependencies on random perturbations in the stimulus, such that repetitions of identical flow movies elicited remarkably similar eye movements over long and continuous time periods. These results demonstrate the generality of spatiotemporal integration in natural vision, and offer a means for studying integration outside of artificial tasks while maintaining lawful and highly reliable behavior.