Role of Low- and High-Frequency Oscillations in the Human Hippocampus for Encoding Environmental Novelty During a Spatial Navigation Task

Abstract

The hippocampus plays a key role in the encoding and retrieval of information related to novel environments during spatial navigation. However, the neural basis for these processes in the human hippocampus remains unknown because it is difficult to directly mea- sure neural signals in the human hippocampus. This study investigated hippocampal neural oscillations involved in encoding novel environ- ments during spatial navigation in a virtual environment. Seven epilep- tic patients with implanted intracranial hippocampal depth electrodes performed three sessions of virtual environment navigation. Each session consisted of a navigation task and a location-recall task. The navigation task consisted of eight blocks, and in each block, the participant navi- gated to the location of four different objects and was instructed to remember the location of the objects. After the eight blocks were com- pleted, a location-recall task was performed for each of the four objects. Intracranial electroencephalography data were monitored dur- ing the navigation tasks. Theta (5–8 Hz) and delta (1–4 Hz) oscillations were lower in the first block (novel environment) than in the eighth block (familiar environment) of the navigation task, and significantly increased from block one to block eight. By contrast, low-gamma (31– 50 Hz) oscillations were higher in the first block than in the eighth block of the navigation task, and significantly decreased from block one to block eight. Comparison of sessions with high recall performance (low error between identified and actual object location) and low recall performance revealed that high-gamma (51–100 Hz) oscillations signifi- cantly decreased from block one to block eight only in sessions with high recall performance. These findings suggest that delta, theta, and low-gamma oscillations were associated with encoding of environmen- tal novelty and high-gamma oscillations were important for the success- ful encoding of environmental novelty. V C 2014 Wiley Periodicals, Inc. KEY WORDS: environmental novelty; low-fre- quency oscillations; high-frequency oscillations; hip- pocampus; intracranial electro-encephalography