The Versatile Wayfinder: Prefrontal Contributions to Spatial Navigation

Navigation is a behavior fundamental to all mobile animals, and incorporates various cognitive functions, including memory, planning, decision-making, and updating models of the world. Historically, the neural underpinnings of flexible navigation have focused on the hippocampal formation, but recent evidence suggests that regions of the prefrontal cortex (PFC) are crucial to many aspects of navigation, especially when environments are complex or dynamic. This review summarizes what we know from recent human, non-human primate, and rodent studies, proposing a novel perspective that incorporates our knowledge across species and brain regions seeking to avoid tunnel vision in understanding the multifaceted behavior in navigation. The prefrontal cortex (PFC) supports decision-making, goal tracking, and planning. Spatial navigation is a behavior that taxes these cognitive processes, yet the role of the PFC in models of navigation has been largely overlooked. In humans, activity in dorsolateral PFC (dlPFC) and ventrolateral PFC (vlPFC) during detours, reveal a role in inhibition and replanning. Dorsal anterior cingulate cortex (dACC) is implicated in planning and spontaneous internally-generated changes of route. Orbitofrontal cortex (OFC) integrates representations of the environment with the value of actions, providing a ‘map’ of possible decisions. In rodents, medial frontal areas interact with hippocampus during spatial decisions and switching between navigation strategies. In reviewing these advances, we provide a framework for how different prefrontal regions may contribute to different stages of navigation. The prefrontal cortex (PFC) supports decision-making, goal tracking, and planning. Spatial navigation is a behavior that taxes these cognitive processes, yet the role of the PFC in models of navigation has been largely overlooked. In humans, activity in dorsolateral PFC (dlPFC) and ventrolateral PFC (vlPFC) during detours, reveal a role in inhibition and replanning. Dorsal anterior cingulate cortex (dACC) is implicated in planning and spontaneous internally-generated changes of route. Orbitofrontal cortex (OFC) integrates representations of the environment with the value of actions, providing a ‘map’ of possible decisions. In rodents, medial frontal areas interact with hippocampus during spatial decisions and switching between navigation strategies. In reviewing these advances, we provide a framework for how different prefrontal regions may contribute to different stages of navigation. a theoretical construct describing the neural representation that underlies our ability to remember the layout of the environment and store information about events occurring in places. a set of brain regions, including the medial prefrontal cortex, hippocampus, and precuneus/posterior cingulate cortex, which are more active when thought is directed internally, as opposed to towards the external environment. a location-modulated neuron that fires at regular intervals as an animal navigates an open area. Grid cells have been most commonly found in the entorhinal cortex and are thought to form an essential part of the brain’s navigation system by allowing it to understand its position in space by storing and integrating information about location, distance, and direction. a collection of information relevant to a given decision that is difficult to distinguish based on sensory input alone and is therefore ‘hidden’. neurons that become active when an animal enters a particular location within an environment, which are most commonly reported in the hippocampus. during ‘replay’, temporally compressed sequences of place cells reactivate spatial trajectories in explored environments in either forward or reverse order. Replay is associated with high-frequency sharp-wave ripple (SWR) events prevalent during offline periods in both sleep and nonexploratory waking states (‘awake replay’). the set of all possible states of the environment that are relevant for a given task, which for navigation might be the possible paths or enclosed spaces available to navigate. a behaviour considered an overt marker of ‘mental planning/exploration’ or deliberation, observed in rodents at a choice point in a maze, where it frequently pauses and alternately faces towards its potential goal, before deciding.