Human Hippocampal Neural Oscillations in Novelty Detection during Spatial Navigation

Abstract

Neural oscillations are the fundamental component of cognitive function in normal brain. At the level of neural ensembles, synchronized activity of large numbers of neurons can give rise to macroscopic oscillations, which can be observed in the electroencephalogram (EEG). Neural oscillations can be measured by non-invasive recordings of large cortical regions from the surface of the scalp and invasive recordings of neuronal populations. In particular, intracranial EEG (iEEG) recorded neural oscillations by electrodes implanted directly inside the brain. Since these recordings measure brain activity with higher spatial and temporal resolution than other recording techniques, it is suitable to understand the neural basis of cognitive function. In humans iEEG recordings were possible with exceptional patients such as epilepsy. Spatial navigation and novelty detection are crucial cognitive function to the daily living of all mammals. In particular, novelty detection is prerequisite for the efficient encoding of events into memory. The hippocampus has long been linked with spatial navigation and novelty detection. The human hippocampal neural oscillations related to novelty detection during spatial navigation have not been reported yet. The purpose of this study was to examine the unknown mechanisms related to novelty detection during spatial navigation in human hippocampus. In this study virtual reality (VR) was used to present totally novel environment. VR task was divided into three sessions with completely different environment to look at novelty detection effects. Participant could grow familiar with novelty of environment and object while they grab objects around VR environment. Four epilepsy patients with depth electrodes in left and right hippocampal regions participated in this experiment and performed 3 sessions. All of participants were instructed to grab objects on the ground as quick as possible. Since it is necessary to confirm novel condition (NC) and familiar condition (FC) of virtual environment, navigation performance was analyzed first. There was a significant linear trend (p = 0.008) of performance improvement. And then neural oscillations between NC and FC were compared about environmental and objective novelty detection. Repeated measures analysis with two-way ANOVA of the mean of Pepisode with session (3 different environments) and environmental novelty condition (NC and FC) was performed to determine whether oscillatory episode at hippocampus significantly changed as a result of environmental novelty or session effect. It performed at five frequency bands of interesting to confirm that what oscillations play functional role of novelty detection. The results showed that theta, alpha and gamma oscillations of left hippocampus and gamma of right hippocampus were statistically significant between NC and FC. And then to determine whether event related spectral perturbation at hippocampus significantly changed as a result of environmental novelty, paired-t test was performed with significance level at 0.05 to compare the distributions of paired mean event-related shifts in the power spectrum value corresponding to NC and FC in VR environment. In the left hippocampus, the results showed that power of theta oscillations in NC was higher than in FC, and the power of beta oscillations in NC was lower than in FC. In the right hippocampus, power of delta, theta and gamma oscillations in NC was lower than in FC. These results showed that there was difference function between bilateral hippocampus to process novel object. In conclusion two major findings about novelty detection function of human hippocampus should be highlighted. First finding about environmental novelty detection was that gamma oscillations in both hippocampi are predominant in novel environment, on the other word these oscillations enhanced to encode new environment’s spatial layout. As a result gamma was dominant neural oscillations in environmental novelty detection. Second finding was that right hippocampal delta, theta and gamma oscillations are involved in objective novelty. The results of this study may therefore come to the conclusion that there are different functions in left and right hippocampus to environmental and objective novelty detection. These results are the first report for human iEEG study to examine the function of novelty detection in human hippocampus for aught I know. Thus, this study lays the foundation for future work on human hippocampal oscillations to novelty detection during spatial navigation.