Lateralized hippocampal oscillations underlie distinct aspects of human spatial memory and navigation

Jonathan Miller,Sang Ah Lee,Joel M Stein,Cory S Inman,Bradley Lega,Joshua Jacobs,Elliot H Smith,Catherine A Schevon,Kathryn A Davis,Michael R Sperling,Ashwini Sharan,Stephen Meisenhelter,Sandhitsu R Das,Ali A Asadi‐Pooya ,Sameer A Sheth,Gregory A Worrell,Andrew J Watrous,Richard Gorniak,Paul A Wanda,Melina Tsitsiklis

doi:10.1038/s41467-018-04847-9

Abstract

The hippocampus plays a vital role in various aspects of cognition including both memory and spatial navigation. To understand electrophysiologically how the hippocampus supports these processes, we recorded intracranial electroencephalographic activity from 46 neurosurgical patients as they performed a spatial memory task. We measure signals from multiple brain regions, including both left and right hippocampi, and we use spectral analysis to identify oscillatory patterns related to memory encoding and navigation. We show that in the left but not right hippocampus, the amplitude of oscillations in the 1–3-Hz “low theta” band increases when viewing subsequently remembered object–location pairs. In contrast, in the right but not left hippocampus, low-theta activity increases during periods of navigation. The frequencies of these hippocampal signals are slower than task-related signals in the neocortex. These results suggest that the human brain includes multiple lateralized oscillatory networks that support different aspects of cognition.

Highlights

The hippocampus plays a vital role in various aspects of cognition including both memory and spatial navigation
Theta oscillations correlate with movement during spatial navigation in rodents[9,10] and humans[11,12], and theta underlies the representation of location by entorhinal grid cells[13]
Our analyses characterized neural signals during the learning of object–location pairs and during traversals to treasure chests to reveal the neural basis of spatial memory encoding and navigation

Summary

Introduction

The hippocampus plays a vital role in various aspects of cognition including both memory and spatial navigation. In a separate line of inquiry, neuroimaging research suggested that the two hippocampi have separate functional roles[17,18] and, in particular, the notion has emerged that activity in the left and right hemispheres separately correlate with verbal and spatial processing, respectively[19,20] Drawing on this diverse body of work, we considered that human hippocampal theta oscillations consist of lateralized signals across left and right hemispheres that each support different behavioral and cognitive processes. By analyzing the relation between task behavior and oscillatory power at various frequencies, we sought to elucidate the electrophysiological basis of human spatial navigation and memory, including understanding functional differences between the hippocampus and neocortex, and between the left and right hemispheres. Our findings indicate that multiple oscillatory networks support different aspects of cognition throughout the brain

Methods

Results

Conclusion