A comparative study of human and rat hippocampal low-frequency oscillations during spatial navigation

Abstract

Rhythmic oscillations within the 3-12 Hz theta frequency band manifest in the rodent hippocampus during a variety of behaviors and are particularly well characterized during spatial navigation. In contrast, previous studies of rhythmic hippocampal activity in primates under comparable behavioral conditions suggest it may be less apparent and possibly less prevalent, or even absent, compared with the rodent. We compared the relative presence of low-frequency oscillations in rats and humans during spatial navigation by using an oscillation detection algorithm ("P-episode" or "BOSC") to better characterize their presence in microelectrode local field potential (LFP) recordings. This method quantifies the proportion of time the LFP exceeds both a power and cycle duration threshold at each frequency, characterizing the presence of (1) oscillatory activity compared with background noise, (2) the peak frequency of oscillatory activity, and (3) the duration of oscillatory activity. Results demonstrate that both humans and rodents have hippocampal rhythmic fluctuations lasting, on average, 2.75 and 4.3 cycles, respectively. Analyses further suggest that human hippocampal rhythmicity is centered around ∼3 Hz while that of rats is centered around ∼8 Hz. These results establish that low-frequency rhythms relevant to spatial navigation are present in both the rodent and human hippocampus, albeit with different properties under the behavioral conditions tested.

Keywords: delta; hippocampus; human; rodent; spatial navigation; theta.

Figure 1

Theta is present in humans at a lower frequency compared to rodents during spatial navigation. A) Examples of human hippocampal raw LFP traces, each from a separate patient, during virtual navigation, showing prominent low frequency oscillations. B) Examples of raw LFP traces, each from a different rat, during the Barnes Maze, also showing prominent low frequency oscillations. C) Example power spectral density plots for a human electrode (red) and a rodent electrode (blue) during navigation. D) Proportion of time oscillatory activity was detected as a function of frequency for 284 human hippocampal recordings (top) and 30 rodent recordings (bottom). Black vertical lines (humans) and dots (rats) indicate the peak frequency at which oscillatory activity was detected for each recording. Note the difference in color scale for humans and rodents. E) Proportion of electrodes with peak activity at each frequency.

Figure 2

Human theta is less continuous compared to rodent theta. A) Proportion of time each frequency was detected averaged across all 284 human recordings and at increasing Pepisode duration criteria. B) Similar to A, but for 30 rodent recordings. C) Proportion of time oscillatory activity was detected at the human peak frequency of 3.4 Hz and the rodent peak frequency of 8 Hz. Gray dashed lines correspond to the half-maximum P-episode duration criteria at the human and rodent peak frequency. D) Average number of cycles for each detected oscillatory event for humans and rodents. Error bars indicate the standard error of the mean across electrodes.