A Unique Role for the Hippocampus in Cue Integration During Human Spatial Navigation

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Abstract

A central question in cognitive neuroscience is how the brain integrates distinct sensory and perceptual inputs to improve cognitive performance. This study investigated this question in the context of human spatial navigation by combining high-field 3T fMRI and desktop virtual reality. Participants encoded and retrieved spatial locations using either landmarks alone (landmark condition), visual self-motion cues alone (i.e., optic flow; self-motion condition), or both cues together (combination condition). Participants behaviorally benefited from cue integration. fMRI analyses revealed a cue integration effect in the hippocampus, which displayed positional coding only in the combination condition, and only in participants who showed behavioral benefits from cue integration. Furthermore, hippocampal positional coding was more strongly associated with actual than self-reported locations, indicating it integrates sensory-perceptual inputs from spatial cues. Our findings suggest that the hippocampus’s fundamental function is to integrate diverse sensory-perceptual inputs to support memory-guided navigation, rather than representing space per se, thereby challenging the dominant cognitive map theory in spatial navigation (O’Keefe & Nadel, 1978).

Significance Statement

The hippocampus is traditionally viewed as a cognitive map representing spatial environments. However, our findings challenge this longstanding view by demonstrating that hippocampal involvement in spatial navigation lies in integrating multiple sensory-perceptual inputs to enhance the precision of spatial representations, rather than spatial representation per se. Using high-resolution fMRI and a novel immersive virtual navigation task, we showed that positional coding in the hippocampus emerges only in participants who successfully integrated different spatial cues to enhance spatial memory precision. Our findings also offers a unifying framework for understanding the hippocampal function across domains, including spatial navigation, cue integration, episodic memory, and relational memory.

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