Abstract
Based on rodent models, researchers have theorized that the hippocampus supports episodic memory and navigation via the theta oscillation, a ~4–10 Hz rhythm that coordinates brain-wide neural activity. However, recordings from humans have indicated that hippocampal theta oscillations are lower in frequency and less prevalent than in rodents, suggesting interspecies differences in theta’s function. To characterize human hippocampal theta, we examine the properties of theta oscillations throughout the anterior–posterior length of the hippocampus as neurosurgical subjects performed a virtual spatial navigation task. During virtual movement, we observe hippocampal oscillations at multiple frequencies from 2 to 14 Hz. The posterior hippocampus prominently displays oscillations at ~8-Hz and the precise frequency of these oscillations correlates with the speed of movement, implicating these signals in spatial navigation. We also observe slower ~3 Hz oscillations, but these signals are more prevalent in the anterior hippocampus and their frequency does not vary with movement speed. Our results converge with recent findings to suggest an updated view of human hippocampal electrophysiology. Rather than one hippocampal theta oscillation with a single general role, high- and low-frequency theta oscillations, respectively, may reflect spatial and non-spatial cognitive processes.
Highlights
Based on rodent models, researchers have theorized that the hippocampus supports episodic memory and navigation via the theta oscillation, a ~4–10 Hz rhythm that coordinates brainwide neural activity
We analyzed intracranial electroencephalographic recordings from the hippocampi of 14 neurosurgical subjects performing a virtual-reality (VR) spatial navigation task, in which subjects were asked to remember the location of an object as they were moved along a linear track (Fig. 1)
A distinct feature of our experimental design compared with previous work is that our task randomly varied the subjects’ movement speed along the virtual track. This design encouraged subjects to continually attend to their spatial location throughout movement, because a nonspatial strategy based on remembering the time delay to each object would not be viable due to speed changes within trials. We hypothesized that this feature of our task would more clearly elicit human hippocampal oscillations related to navigation
Summary
Researchers have theorized that the hippocampus supports episodic memory and navigation via the theta oscillation, a ~4–10 Hz rhythm that coordinates brainwide neural activity. There is evidence that human movement-related hippocampal theta oscillations vary substantially in frequency according to whether a subject is in a physical or virtual environment[7,8,9,10] Together, these studies and others have been interpreted to suggest that the human hippocampus does show a signal analogous to theta oscillations observed in rodents, but that this oscillation is more variable and slower in frequency[6]. A distinct feature of our experimental design compared with previous work is that our task randomly varied the subjects’ movement speed along the virtual track This design encouraged subjects to continually attend to their spatial location throughout movement, because a nonspatial strategy based on remembering the time delay to each object would not be viable due to speed changes within trials. By demonstrating multiple patterns of hippocampal oscillations with different anatomical and functional properties, our findings suggest that human hippocampal oscillations at different frequencies are generated by separate anatomical networks to support distinct functions
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