Edited by Gyorgy Buzsáki, New York University Neuroscience Institute, New York, NY, and approved October 16, 2019 (received for review April 19, 2019)
The medial temporal lobe (MTL) plays a role in both spatial navigation and memory, but how these 2 cognitive processes are linked remains unclear. In particular, theta oscillations (4 to 8 Hz) appear prominently in the hippocampus in rodents and humans as they move through spatial environments, but there is mixed evidence as to whether this signal also emerges while animals search memory for previously acquired information. Using electrodes implanted in human neurosurgical patients, we showed that hippocampal theta oscillations reflect representational distances between word items in memory. This suggests there is a fundamental theta-based mechanism that supports the creation and retrieval of “cognitive maps” in the MTL, for explicitly nonspatial information.
The medial temporal lobe (MTL) is known to support episodic memory and spatial navigation, raising the possibility that its true function is to form “cognitive maps” of any kind of information. Studies in humans and animals support the idea that the hippocampal theta rhythm (4 to 8 Hz) is key to this mapping function, as it has been repeatedly observed during spatial navigation tasks. If episodic memory and spatial navigation are 2 sides of the same coin, we hypothesized that theta oscillations might reflect relations between explicitly nonspatial items, such as words. We asked 189 neurosurgical patients to perform a verbal free-recall task, of which 96 had indwelling electrodes placed in the MTL. Subjects were instructed to remember short lists of sequentially presented nouns. We found that hippocampal theta power and connectivity during item retrieval coded for semantic distances between words, as measured using word2vec-derived subspaces. Additionally, hippocampal theta indexed temporal distances between words after filtering lists on recall performance, to ensure adequate dynamic range in time. Theta effects were noted only for semantic subspaces of 1 dimension, indicating a substantial compression of the possible semantic feature space. These results lend further support to our growing confidence that the MTL forms cognitive maps of arbitrary representational spaces, helping to reconcile longstanding differences between the spatial and episodic memory literatures.
Author contributions: E.A.S., B.C.L., M.R.S., and M.J.K. designed research; E.A.S., B.C.L., and M.R.S. performed research; E.A.S. and M.J.K. contributed new reagents/analytic tools; E.A.S. analyzed data; and E.A.S. and M.J.K. wrote the paper.
The authors declare no competing interest.
This article is a PNAS Direct Submission.
Data deposition: Raw electrophysiogical data used in this study are available at http://memory.psych.upenn.edu/Electrophysiological_Data. Analysis code and processed data have been deposited in a public interactive Jupyter Notebook, https://notebooks.azure.com/esolo/projects/theta-semantics.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1906729116/-/DCSupplemental.
Published under the PNAS license.
