Hippocampal theta codes for distances in semantic and temporal spaces

Abstract

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 (4-8 Hz) is key to this mapping function, as it has been repeatedly observed during spatial navigation tasks. If episodic memory and spatial navigation are two sides of the same coin, we hypothesized that theta oscillations would also 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 only noted 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, reconciling longstanding differences between the spatial and episodic memory literatures.

Multiple spatial codes for navigating 2-D semantic spaces

“…A final additional aspect that demands discussion is the absence of distance coding in the hippocampus and entorhinal cortex. This result is surprising because previous studies reported such effect (Theves et al 2019;Solomon et al 2019;Viganò & Piazza 2020). Several discrepancies between these studies and the current one might account for this putative contradiction.…”

“…A more parsimonious explanation might be the fact that the entorhinal cortex, given its anatomical position, is more prone to signal loss, and effects of this kind might be too subtle to be reliably detected and replicated using 3 or 4T magnets. This argument might well also apply to the hippocampus, specifically in light of the results of Solomon et al 2019, that showed a distance effect between words using intracranial electrophysiology, thus with a significantly higher spatial resolution compared to our current one. A more carefully designed experiment addressing this specific question with an ROI approach, in combination with high-field magnets, might be the more accurate way to experimentally solve the issue.…”

Hippocampal theta oscillations support successful associative memory formation

“…Understanding different connectivity relationships for these two oscillations using the associative recognition paradigm may help illuminate separate slow and fast theta networks that explicate regions involved in familiarity versus recollection, especially during retrieval. Certainly, a comprehensive understanding of these oscillations requires further characterization, including contrasts between spatial navigation and verbal memory and updated models of theta generation and propagation accounting for possible slow versus fast theta differences Solomon, Lega, Sperling, & Kahana, 2019). However, our findings support a model by which slow theta oscillatory power increases are necessary for associative memory during item retrieval and as such they constitute direct evidence of a role for these oscillations in recollection.…”

Dynamic activity patterns in the anterior temporal lobe represents object semantics

“…Chen et al, 2016;Clarke et al, 2018). In particular, recent evidence suggests theta activity in the ATL might be particularly important for coding semantic representations of basic-level objects , which is consistent with evidence that theta activity in the MTL dissociates between different object categories (Kraskov et al, 2007) and tracks the access of semantic knowledge (Ackeren et al, 2014;Bastiaansen et al, 2005;Fuentemilla et al, 2014;Halgren et al, 2015;Solomon et al, 2019;Watrous & Ekstrom, 2014).…”