Summary This proposal will investigate the neural dynamics underlying three-dimensional foraging behavior, with three overarching goals. The first is to evaluate the neural computations of foraging in dynamic environments in naturalistic settings. The second is to compare the algorithmic behavioral computations and their neural substrates under naturalistic versus traditional laboratory settings. Most neuroscience studies assume that laboratory behavior has real-world implications, so any differences we observe would have remarkable consequences for the future of neuroscience. The third goal is to test the role of hippocampal formation, frontal, and parietal areas in the different components of foraging. We will compare three behaviors in two experimental setups. The behaviors are free-foraging for unpredictable, random rewards, a goal-driven foraging task with navigation among three resource patches under visual uncertainty and stochastic reward presentation, and foraging among three resource patches without navigation. The latter two tasks involve the formation and maintenance of internal models, memories, time-dependent sensory and reward contingencies, the costs of an animal’s own actions, and dynamically changing beliefs about the state of the world. The former two tasks will be performed during head-free navigation in a foraging room, and during head-fixed navigation in virtual reality. In both environments, we will record simultaneously from several mutually interconnected areas involved in visual navigation, spatial memory, path integration, and decision-making. Target areas include posterior parietal cortex, prefrontal cortex, retrosplenial cortex, entorhinal cortex, and hippocampus. We will use advanced behavioral models and theory to infer internal states and to identify their neural representation and interactions across a broad network of interconnected brain areas. In addition, we will regress neuronal activity against task-relevant variables to identify neural subspaces that encode them. Collectively, we expect that these experiments will rigorously illuminate the neural dynamics of foraging and spatial navigation behaviors and critically interrogate whether and how constrained laboratory conditions with head-fixed, restrained animals differ from ecological and naturalistic environments—a critical but still untested assumption of contemporary systems neuroscience.

Project Narrative This proposal applies a transformative approach to understanding the ability to navigate spatial environments and forage, using advanced behavioral models and theory to infer internal states during macaque ethologically relevant foraging behavior. While animals build and maintain an internal model of the environment, we will identify the neural representation of these internal variables and their interactions across a broad network of interconnected brain areas. The results will help to interpret dynamic neural computation and reveal general strategies for naturalistic tasks that could inform both psychiatry and artificial intelligence.