Head movement allocation in freely-moving macaques learning object-context sequences

Abstract

Flexible learning and long-term memory are hallmark features of primate cognition that are shaped by interactions with changing environments. A comprehensive understanding of these brain-body-environment interactions requires minimal constraints on behavior, and environments rich with conditional cues that encourage diverse behavioral dynamics. In this study, we introduce a multi-level enclosure (Treehouse) that allows for independent control of spatially distributed touchscreens for studying cognition in freely moving macaques. To test flexible learning, two monkeys completed trials consisting of a regular sequence of conditional object choices (targets) across four distinct spatiotemporal contexts (screens). Both monkeys acquired numerous unique, conditional object-context sequences without detriment to new learning as memoranda accumulated. They also successfully recalled their correct choices after weeks without exposure. To assess how monkeys allocate movement during learning and memory-guided decision making, we tracked their head kinematics and used recurrent neural networks to decode different aspects of their engagement with the environment during the choice epoch of the task. One such model predicted the position of the object about to be touched, including on error trials, tracking overt gaze towards objects. Separate models decoded sequence corner, the ordinal step, and the individual screen stations the monkeys occupied, despite identical stimulus layouts and behavioral demands at each station. Head movements also showed efficiencies that the task did not require: under conditions of uncertainty, monkeys were biased in their initial search locations to the targets that were closest to reach, and across days they made smoother head movements as training progressed, with no change in accuracy. These results demonstrate the potential of immersive 3-D environments, in which body kinematics can shed light on animals' goals, and reveal that situated learning in primates can be rapid, capacious, durable, and flexible.