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 measure neural signals in the human hippocampus. This study investigated hippocampal neural oscillations involved in encoding novel environments during spatial navigation in a virtual environment. Seven epileptic 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 navigated to the location of four different objects and was instructed to remember the location of the objects. After the eight blocks were completed, a location-recall task was performed for each of the four objects. Intracranial electroencephalography data were monitored during 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 significantly 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 environmental novelty and high-gamma oscillations were important for the successful encoding of environmental novelty.

Bidirectional Modulation of Recognition Memory

“…Another possibility is that one of these functions is coded by firing rates and the other by oscillatory or synchronized neuronal activity. Consistent with this idea, depth recordings in the human hippocampus showed that the power of brain oscillations in high-frequency bands, particularly low-gamma frequency bands, decreased as novel environments became familiar (Park et al, 2014). In rodents, exploration of novel objects was accompanied by increased power in the lowgamma frequency range (Lapray et al, 2009).…”

“…Increased gamma power is also associated with increases of attention in humans (Herrmann and Knight, 2001;Debener et al, 2003;Fries, 2009) and exposure to novelty has been shown to increase attention (Lee et al, 2007;Marco-Pallarés et al, 2015). Depth recordings in humans also showed that the power of lower-frequency oscillations increased as novel environments become more familiar (Park et al, 2014). This is consistent with a prior rodent study in which spontaneous local field potentials (LFPs) in the PER showed a prominent oscillation in the 10 -12 Hz (low-beta) frequency band in rats foraging in a familiar environment (Nerad and Bilkey, 2005).…”

Intracranial recordings and human memory

“…[22]). Importantly, ECoG studies demonstrate that low- and high-frequency activity often share an inverse relationship [5,20,24,25,38,39,40]. Likewise, while measures of high-frequency amplitude show overlap with the BOLD measures of fMRI, low-frequency activity is anatomically dissociated with BOLD measures [41].…”

“…Kucewicz et al [38] reported that encoding images induces oscillations from 50-500 Hz within the primary visual cortex as well as limbic and higher cortical regions, consistent with the visual processing stream (also [5]), and successful recall is linked with increased 50-500 Hz oscillatory activity in widespread higher cortical regions. Within the hippocampus, Park et al [40] revealed a role for high-gamma (51-100 Hz) but not low-gamma, delta, or theta, in successful encoding during navigation. Axmacher et al [14] found that 70-90 Hz high-gamma power is selectively increased during processing of unexpected items at multiple points during encoding in preparation for a recognition test.…”

Changes of EEG Spectra and Functional Connectivity during an Object-Location Memory Task in Alzheimer’s Disease

“…Theta band oscillatory in post-rhinal cortex and gamma band in CA3 of hippocampus were correlated with objects place memory in rats (Lu et al, 2011; Furtak et al, 2012). Delta, theta, gamma bands oscillations were correlated with spatial navigation in human (Snider et al, 2013; Park et al, 2014). P300, N200, N300 were the factors in an integrated object-location task in event-related potentials (ERPs) study (Simon-Thomas et al, 2003; van Hoogmoed et al, 2012).…”