Theta oscillations support active exploration in human spatial navigation

Abstract

Active navigation seems to yield better spatial knowledge than passive navigation, but it is unclear how active decision-making influences learning and memory. Here, we examined the contributions of theta oscillations to memory-related exploration while testing theories about how they contribute to active learning. Using electroencephalography (EEG), we tested individuals on a maze-learning task in which they made discrete decisions about where to explore at each choice point in the maze. Half the participants were free to make active decisions at each choice point, and the other half passively explored by selecting a marked choice (matched to active exploration) at each intersection. Critically, all decisions were made when stationary, decoupling the active decision-making process from movement and speed factors, which is another prominent potential role for theta oscillations. Participants were then tested on their knowledge of the maze by traveling from object A to object B within the maze. Results show an advantage for active decision-making during learning and indicate that the active group had greater theta power during choice points in exploration, particularly in midfrontal channels. These findings demonstrate that active exploration is associated with theta oscillations during human spatial navigation, and that these oscillations are not exclusively related to movement or speed. Results demonstrating increased theta oscillations in prefrontal regions suggest communication with the hippocampus and integration of new information into memory. We also found evidence for alpha oscillations during active navigation, suggesting a role for attention as well. This study finds support for a general mnemonic role for theta oscillations during navigational learning.

Keywords

• Memory
• Virtual reality
• Encoding
• Reinforcement learning
• Alpha oscillations
• Beta oscillations