Human hippocampal theta power indicates movement onset and distance travelled

Abstract

Theta frequency oscillations in the 6- to 10-Hz range dominate the rodent hippocampal local field potential during translational movement, suggesting that theta encodes self-motion. Increases in theta power have also been identified in the human hippocampus during both real and virtual movement but appear as transient bursts in distinct high- and low-frequency bands, and it is not yet clear how these bursts relate to the sustained oscillation observed in rodents. Here, we examine depth electrode recordings from the temporal lobe of 13 presurgical epilepsy patients performing a self-paced spatial memory task in a virtual environment. In contrast to previous studies, we focus on movement-onset periods that incorporate both initial acceleration and an immediately preceding stationary interval associated with prominent theta oscillations in the rodent hippocampal formation. We demonstrate that movement-onset periods are associated with a significant increase in both low (2-5 Hz)- and high (6-9 Hz)-frequency theta power in the human hippocampus. Similar increases in low- and high-frequency theta power are seen across lateral temporal lobe recording sites and persist throughout the remainder of movement in both regions. In addition, we show that movement-related theta power is greater both before and during longer paths, directly implicating human hippocampal theta in the encoding of translational movement. These findings strengthen the connection between studies of theta-band activity in rodents and humans and offer additional insight into the neural mechanisms of spatial navigation.

Keywords: hippocampus; intracranial EEG; navigation; spatial memory; theta.

Fig. 1.

Behavioral data. (A) Schematic of the spatial memory task. Participants navigate freely in a square VR environment, 100 vm per side, with distal cues for orientation. Participants memorize the location of one of four objects across 20 encoding trials (five for each object). Encoding is followed by a 30-s break period during which participants are instructed to focus on memorizing object locations. Each of 20 retrieval trials (five for each object) begins with a 3-s cue period, during which an image of one object is presented on screen. Participants are then placed back at one of four starting locations and are instructed to navigate to the remembered location of that object and make a response. Following this response, the object appears in its correct location to provide feedback on their performance in each trial. (B) Heat map of all responses for the object location in session one with the largest mean error across patients. The true object location is marked with a yellow star. (C) Histogram of $\mathrm{\Delta }d$s across all objects and patients. Chance performance is marked with a red dashed line. (D) Change in mean $\mathrm{\Delta }d$ for all objects across retrieval trials. Linear fits to each patient’s performance are marked with a light gray line, and the average is marked with a thick red line.

Fig. 2.

Theta power changes during virtual movement across the temporal lobe. (A) Average power spectrum for movement-onset periods, baseline corrected by mean power at each frequency during stationary periods, for electrode contacts in the hippocampus. Power is increased in both low (2–5 Hz) and high (6–9 Hz) theta bands (marked in gray). (B) Spectrogram of power around virtual movement onset, baseline corrected by mean power at each frequency during stationary periods, for electrode contacts in the hippocampus. Black dashed regions indicate the low- and high-frequency theta bands for the 1-s period around movement onset. (C) Average power spectrum for remainder of movement periods, baseline corrected by mean power at each frequency during stationary periods, for electrode contacts in the hippocampus. Peaks in the low- and high-frequency theta bands (marked in gray) are visible but are less pronounced than during movement onset. (D–F) Mean z-scored power in the low (2–5 Hz) and high (6–9 Hz) theta bands during movement-onset, remainder-of-movement, and stationary periods in the hippocampus (D), amygdala (E), and lateral temporal lobe (F). Both low and high theta power are significantly increased during virtual movement onset, compared with stationary periods, on electrode contacts in the hippocampus and lateral temporal lobe but not on those located in the amygdala. In addition, mean z-scored power in the low- and high-frequency theta bands is greater than zero during movement onset on electrode contacts in the hippocampus and lateral temporal lobe and during the remainder of movement on electrode contacts in the hippocampus.

Fig. 3.

Theta power changes with path length in the hippocampus and lateral temporal lobe. (A and C) Mean z-scored power in the low (2–5 Hz) and high (6–9 Hz) theta bands averaged across movement-onset and remainder-of-movement periods for long and short paths across the virtual environment on hippocampal (A) and lateral temporal lobe (C) electrode contacts. In each region, both low and high theta power are significantly increased during long paths compared with short paths. (B and D) Power spectra averaged across movement-onset and remainder-of-movement periods for long and short paths across the virtual environment in the hippocampus (B) and lateral temporal lobe (D). In both regions, broadband low-frequency oscillatory power is increased during long paths compared with short paths. Low (2–5 Hz) and high (6–9 Hz) theta bands are marked in gray.