Agency Modulation of Hippocampal Activity During Spatial Navigation

TL;DR

The paper shows that when people navigate actively, their hippocampus encodes spatial information more efficiently, leading to better map formation.

Contribution

The study demonstrates that agentic navigation leads to sparse hippocampal encoding and better spatial memory performance.

Findings

Agency lowers hippocampal activity during spatial traversal and improves retrieval navigation performance.

Agentic navigation increases frontal and temporal dissociation of map nodes from non-nodes.

Sparse hippocampal encoding correlates with more accurate cognitive map formation.

Abstract

The role of navigational agency during hippocampal cognitive map formation remains unclear. To examine this, we measured functional brain activity as participants learned landmarks and paths in virtual mazes either through agentic self-generated movements or guided video tours. Anterior hippocampal responses were generally lower at objective nodes (landmarks and junctions) than non-nodes (traversals). Agency lowered hippocampal traversal activity and subsequently resulted in faster and more successful retrieval navigation behavior. Moreover, agency decreased hippocampal functional autocorrelations suggesting lowered responses stemmed from sparse encoding. Finally, hippocampal node encoding corresponded to the extent frontal and temporal responses dissociated nodes from non-nodes. These findings show that agentic spatial navigation affords subjective movement decisions during spatial traversal that drive hippocampal sparse encoding of plain space into structured node maps.

To code spatial environments, hippocampal (HC) cells 1,2 engage selective and topological activities at different places, which constitute cognitive maps 3–6. However, while HC activity is modulated by navigational repetition and motivation 7–10, how these factors drive HC cognitive map formation remains difficult to validate in the non-human animal studies above. Here, we show that agency in human navigation in humans induces sparse HC activity during map-learning and enhances retrieval navigation. Functional magnetic resonance imaging during agentic spatial navigation detected that the formation of map node states was coded by lower, sparser anterior HC ensemble responses, particularly when traversing between landmarks. Higher activity reflected poorer map encoding instead. Moreover, agency increased frontal and temporal node vs. non-node state dissociations that corresponded with lower HC responses. Our findings link repetitive map exposures and goal processing by demonstrating that subjective agentic movement processes in cortical regions drive hippocampal sparse encoding of more accurate cognitive maps. Amongst other inquiries, this framework lays groundwork for examining the role of volition in technology use (e.g. GPS, passive content viewing) on human brain development and aging. Also, a definition of agency in intelligent systems artificial or otherwise might also be developed.

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