Functionally distinct high and low theta oscillations in the human hippocampus

Abstract

22Based on rodent models, researchers have theorized that the hippocampus supports episodic 23 memory and navigation via the theta oscillation, a ∼4-10-Hz rhythm that coordinates brain-wide 24 neural activity. However, recordings from humans have indicated that hippocampal theta oscillations 25 are lower in frequency and less prevalent than in rodents, suggesting interspecies differences in 26 theta's function. To characterize human hippocampal theta, we examined the properties of theta 27 oscillations throughout the anterior-posterior length of the hippocampus as neurosurgical subjects 28 performed a virtual spatial navigation task. During virtual movement, we observed hippocampal 29 oscillations at multiple frequencies from 2 to 14 Hz. The posterior hippocampus prominently 30 displayed oscillations at ∼8-Hz and the precise frequency of these oscillations correlated with the 31 speed of movement, implicating these signals in spatial navigation. We also observed slower ∼3-Hz 32 oscillations, but these signals were more prevalent in the anterior hippocampus and their frequency 33 did not vary with movement speed. Our results converge with recent findings to suggest an updated 34 view of human hippocampal electrophysiology. Rather than one hippocampal theta oscillation with a 35 single general role, high-and low-theta oscillations, respectively, may reflect spatial and non-spatial 36 cognitive processes. 38The theta oscillation is a large-scale network rhythm that appears at ∼4-10 Hz in rodents and is 39 hypothesized to play a fundamental role in mammalian spatial navigation and memory (Kahana et 40 al., 2001; Buzsáki, 2005). However, in humans, there is mixed evidence regarding the relevance and 41 properties of hippocampal theta. Some studies in humans show hippocampal oscillations at 1-5 Hz that 42 have similar functional properties as the theta oscillations seen in rodents (e.g., Arnolds et al., 1980; 43 There is also evidence that human movement-related hippocampal theta oscillations vary substantially 45 in frequency according to whether a subject is in a physical or virtual environment (Aghajan et al., 2016; 46 Bohbot et al., 2017; Yassa, 2018). Together, these studies have been interpreted to suggest that the 47 human hippocampus does show a signal analogous to theta oscillations observed in rodents but that 48 this oscillation is more variable and slower in frequency (Jacobs, 2014). These apparent discrepancies 49 in the frequency of theta between species and behaviors shed doubt on the notion that theta exists as 50 a single general oscillatory phenomenon that coordinates brain-wide neural activity consistently across 51 species and tasks. 52Our study aimed to resolve these discrepancies by characterizing the properties of human hip-53 pocampal oscillations in spatial cognition. We analyzed intracranial electroencephalographic (iEEG) 54 recordings from the hippocampi of fourteen neurosurgical subjects performing a virtual-reality (VR) 55 spatial navigation task, in which subjects were aske...

Theta power and theta‐gamma coupling support long‐term spatial memory retrieval

“…We had previously shown that hippocampal theta power was indicative of movement onset in this task (Bush et al, 2017) and spatial memory retrieval in MEG (Kaplan et al, 2014). Other studies performing a different hybrid navigation and memory paradigm have suggested diverse roles for low theta depending on laterality and hippocampal subregion (Miller et al, 2018;Goyal et al, 2020;Herweg et al, 2020). There has been an increasing body of evidence to suggest that low frequency power decrease and high frequency power increase is associated with performance in a variety of tasks, with this "tilt" in the 1/frequency characteristic inherent to human EEG thought to reflect increased regional neural activity (Fellner et al, 2019).…”

Mammillothalamic Disconnection Alters Hippocampocortical Oscillatory Activity and Microstructure: Implications for Diencephalic Amnesia

“…The lesions in the Sharp and Koester (2008) study included both the MBs and supramammillary nuclei; however, our present findings would suggest that their results were at least in part driven by the loss of the MBs. Theta frequency is considered a mechanism for timing the flow of information in the hippocampus (Richard et al, 2013), and high-frequency theta in particular has been linked to spatial memory in both rodents and humans (Olvera-Cortés et al, 2002; Goyal et al, 2018). Furthermore, reducing the frequency of theta in otherwise normal animals impairs performance on spatial memory tasks (Pan and McNaughton, 1997).…”

Mammillothalamic disconnection alters hippocampo-cortical oscillatory activity and microstructure: Implications for diencephalic amnesia

“…The lesions in Sharp and Koester's study included both the mammillary bodies and supramammillary nuclei, however, our present findings would suggest their results were at least in part driven by the loss of the mammillary bodies. Theta frequency is considered a mechanism for timing the flow of information in the hippocampus (Richard et al, 2013) and high-frequency theta in particular has been linked to spatial memory in both rodents and humans (Goyal et al, 2018;Olvera-Cortes et al, 2002). Furthermore, reducing the frequency of theta in otherwise normal animals impairs performance on spatial memory tasks (Pan and McNaughton, 1997).…”