Navigating memories: Space as an organizing principle in episodic memory
Human Cognitive and Systems Neuroscience
Final Report Abstract
The medial temporal lobe (MTL) plays a key role in spatial navigation and in our ability to remember events from our past. However, few studies have directly investigated how these functions relate to each other. Here, we used an established spatial-episodic memory task in which subjects navigate to a series of target stores in a virtual city and later attempt to recall objects that they encoded during navigation. We find that over time subjects get more efficient at navigating to the target stores. During recall, subjects organize their memories according to both temporal and spatial encoding context, recalling items successively that were encoded in temporal or spatial proximity. This suggests that both temporal and spatial context information are reinstated during object recall and then act as a cue for items encoded in a similar context. We developed a formal model to capture these effects, building on the class of temporal context models. Our model acquires a spatial map of the environment and produces temporal and a spatial contiguity effects during recall, similar to those observed in our subjects’ data. We analyzed intracranial EEG and micro-wire data from patients undergoing clinical seizure monitoring to assess learning-related changes in neural representations of space and to study the neural signature of contextual memory retrieval. Using a multinomial-logistic regression classifier, we successfully decoded the subjects’ instantaneous position in the environment from local field potentials (LFPs) in the MTL. Using the classifiers’ predictions, we show that the LFP represents the subjects’ location in semantic and in virtual space, and that both types of representations strengthen over time. We further show that the MTL predicts upcoming locations on the subjects’ trajectories and that these predictions likewise strengthen over time. Our results provide crucial support for the conceptualization of the MTL as a memory space, building semantic knowledge, spatial and non-spatial, from episodic experience to predict the future. During navigation, theta oscillations prominently appear in the local field potential of the medial temporal lobe and they have also been linked to declarative memory encoding and retrieval. Here, we asked how human theta oscillations affect the firing of individual neurons. In a dataset of 1233 neurons recorded from the medial temporal lobe and more sparsely sampled neocortical regions, we found that 29.4% of the recorded neurons fired phase locked to the hippocampal LFP. This effect was most prevalent in the theta band, suggesting that human hippocampal theta oscillations orchestrate neuronal firing. We further asked how theta oscillations relate to memory retrieval. We found that retrieval of contextual information specifically, is associated with an increase in medial temporal theta power. This increase in theta is accompanied by a decrease in hippocampal firing rates, suggesting a sparse code for retrieved information in hippocampal neurons. Together, our results suggest that medial temporal theta oscillations provide access to a “cognitive map” of the environment that can be used to predict the future and that influences how we remember the past.
Publications
- (2020). Reactivated spatial context guides episodic recall. Journal of Neuroscience, 40(10), 2119-2128
Herweg, N. A., Sharan, A. D., Sperling, M. R., Brandt, A., Schulze-Bonhage, A., & Kahana, M. J.
(See online at https://doi.org/10.1523/JNEUROSCI.1640-19.2019) - (2020). Theta oscillations in human memory. Trends in Cognitive Sciences, 24(3), 208-227
Herweg, N. A., Solomon, E. A., & Kahana, M. J.
(See online at https://doi.org/10.1016/j.tics.2019.12.006)
