Sensory Evidence Accumulation Using Optic Flow in a Naturalistic Navigation Task

• Published in: The Journal of neuroscience Vol. 42; no. 27; pp. 5451 - 5462
• Main Authors: Alefantis, Panos, Lakshminarasimhan, Kaushik, Avila, Eric, Noel, Jean-Paul, Pitkow, Xaq, Angelaki, Dora E.
• Format: Journal Article
• Language: English
• Published: United States Society for Neuroscience 06.07.2022
• Subjects: Accumulation; Animals; Computer applications; Decision making; Female; Humans; Joysticks; Male; Males; Mammals; Mental task performance; Movement; Navigation behavior; Optic Flow; Perception; Perturbation; Sensory integration; Virtual reality; navigation; virtual reality; nonhuman primates; sensory accumulation; naturalistic; closed loop
• ISSN: 0270-6474; 1529-2401; 1529-2401
• DOI: 10.1523/JNEUROSCI.2203-21.2022

Sensory evidence accumulation is considered a hallmark of decision-making in noisy environments. Integration of sensory inputs has been traditionally studied using passive stimuli, segregating perception from action. Lessons learned from this approach, however, may not generalize to ethological behaviors like navigation, where there is an active interplay between perception and action. We designed a sensory-based sequential decision task in virtual reality in which humans and monkeys navigated to a memorized location by integrating optic flow generated by their own joystick movements. A major challenge in such closed-loop tasks is that subjects' actions will determine future sensory input, causing ambiguity about whether they rely on sensory input rather than expectations based solely on a learned model of the dynamics. To test whether subjects integrated optic flow over time, we used three independent experimental manipulations, unpredictable optic flow perturbations, which pushed subjects off their trajectory; gain manipulation of the joystick controller, which changed the consequences of actions; and manipulation of the optic flow density, which changed the information borne by sensory evidence. Our results suggest that both macaques (male) and humans (female/male) relied heavily on optic flow, thereby demonstrating a critical role for sensory evidence accumulation during naturalistic action-perception closed-loop tasks. The temporal integration of evidence is a fundamental component of mammalian intelligence. Yet, it has traditionally been studied using experimental paradigms that fail to capture the closed-loop interaction between actions and sensations inherent in real-world continuous behaviors. These conventional paradigms use binary decision tasks and passive stimuli with statistics that remain stationary over time. Instead, we developed a naturalistic visuomotor visual navigation paradigm that mimics the causal structure of real-world sensorimotor interactions and probed the extent to which participants integrate sensory evidence by adding task manipulations that reveal complementary aspects of the computation.