Hippocampal theta codes for distances in semantic and temporal spaces

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 116; no. 48; pp. 24343 - 24352
• Main Authors: Solomon, Ethan A., Lega, Bradley C., Sperling, Michael R., Kahana, Michael J.
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 26.11.2019
• Series: PNAS Plus
• Subjects: Animal behavior; Biological Sciences; Cluster Analysis; Cognitive ability; Cognitive maps; Cognitive models; Compression; Electroencephalography; Hippocampus; Hippocampus - physiology; Humans; Mapping; Memory; Memory tasks; Memory, Episodic; Mental Recall; Navigation; Navigation behavior; Neural networks; Neurosurgery; Nontherapeutic Human Experimentation; Parahippocampal Gyrus - physiology; PNAS Plus; Recall; Semantics; Spatial memory; Subspaces; Temporal lobe; Temporal Lobe - physiology; Theta Rhythm; Theta rhythms; Words (language); episodic memory; hippocampus; theta; cognitive map; recall
• DOI: 10.1073/pnas.1906729116
• ISSN: 0027-8424; 1091-6490

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.