Successful retrieval of competing spatial environments in humans involves hippocampal pattern separation mechanisms

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Abstract

The rodent hippocampus represents different spatial environments distinctly via changes in the pattern of "place cell" firing. It remains unclear, though, how spatial remapping in rodents relates more generally to human memory. Here participants retrieved four virtual reality environments with repeating or novel landmarks and configurations during high-resolution functional magnetic resonance imaging (fMRI). Both neural decoding performance and neural pattern similarity measures revealed environment-specific hippocampal neural codes. Conversely, an interfering spatial environment did not elicit neural codes specific to that environment, with neural activity patterns instead resembling those of competing environments, an effect linked to lower retrieval performance. We find that orthogonalized neural patterns accompany successful disambiguation of spatial environments while erroneous reinstatement of competing patterns characterized interference errors. These results provide the first evidence for environment-specific neural codes in the human hippocampus, suggesting that pattern separation/completion mechanisms play an important role in how we successfully retrieve memories.

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Colin T Kyle

Center for Neuroscience, University of California, Davis, Davis, United States

Competing interests
The authors declare that no competing interests exist.
Jared D Stokes

Department of Psychology, University of California, Davis, Davis, United States

Competing interests
The authors declare that no competing interests exist.
Jennifer S Lieberman

Center for Neuroscience, University of California, Davis, Davis, United States

Competing interests
The authors declare that no competing interests exist.
Abdul S Hassan

Center for Neuroscience, University of California, Davis, Davis, United States

Competing interests
The authors declare that no competing interests exist.
Arne D Ekstrom

Department of Psychology, University of California, Davis, Davis, United States

For correspondence
adekstrom@ucdavis.edu

Competing interests
The authors declare that no competing interests exist.

Ethics

Human subjects: This study was approved by the Institutional Review Board at the University of California at Davis. Written informed consent was obtained from each participant before the experiment.

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This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.