Hippocampal theta oscillations are slower in humans than in rodents: implications for models of spatial navigation and memory

Abstract

The theta oscillation is a neuroscience enigma. When a rat runs through an environment, large-amplitude theta oscillations (4-10 Hz) reliably appear in the hippocampus's electrical activity. The consistency of this pattern led to theta playing a central role in theories on the neural basis of mammalian spatial navigation and memory. However, in fact, hippocampal oscillations at 4-10 Hz are rare in humans and in some other species. This presents a challenge for theories proposing theta as an essential component of the mammalian brain, including models of place and grid cells. Here, I examine this issue by reviewing recent research on human hippocampal oscillations using direct brain recordings from neurosurgical patients. This work indicates that the human hippocampus does indeed exhibit rhythms that are functionally similar to theta oscillations found in rodents, but that these signals have a slower frequency of approximately 1-4 Hz. I argue that oscillatory models of navigation and memory derived from rodent data are relevant for humans, but that they should be modified to account for the slower frequency of the human theta rhythm.

Keywords: electroencephalography; hippocampus; memory; navigation; theta oscillations.

Figure 1.

Example hippocampal theta oscillations in rodents and humans. (a) Recording from the human hippocampus (Jacobs Laboratory 2013, unpublished data). (b) Recording from the rodent hippocampus (Reproduced with permission from [33]). Both recordings have a 1 s duration.

Figure 2.

Hippocampal oscillations in rodents and humans. (a) Human hippocampal theta oscillations. Plots show spike-triggered average hippocampal field potentials from three separate patients (Reproduced with permission from [52]). (b) Example of a rodent hippocampal theta oscillation. Plot shows the mean autocorrelation of a theta signal from [53] (Reproduced with permission). Note that plots in (a,b) share the same timescale, as indicated by the scale bar in the bottom panel.

Figure 3.

Behaviour-related changes in hippocampal activity reveal human and rodent theta oscillations at different frequencies. (a) Theta oscillations in the rodent hippocampus during movement. Plot depicts the probability of observing a significant oscillation as a function of frequency in a rat during movement. Adapted from [10]. Plots are modified so that their frequency axes are approximately aligned for ease of comparison. (b) Theta oscillations in the human hippocampus during virtual navigation. Plot indicates the probability of observing a significant neuronal oscillation at each frequency. Adapted from [55] with permission. (c) Theta oscillations in the human hippocampus during an episodic memory task. Adapted from [56] with permission.