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Functionally distinct high and low theta oscillations in the human hippocampus.

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.

SUBMITTER: Goyal A

PROVIDER: S-EPMC7235253 | biostudies-literature | 2020 May

REPOSITORIES: biostudies-literature

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Functionally distinct high and low theta oscillations in the human hippocampus.

Goyal Abhinav A Miller Jonathan J Qasim Salman E SE Watrous Andrew J AJ Zhang Honghui H Stein Joel M JM Inman Cory S CS Gross Robert E RE Willie Jon T JT Lega Bradley B Lin Jui-Jui JJ Sharan Ashwini A Wu Chengyuan C Sperling Michael R MR Sheth Sameer A SA McKhann Guy M GM Smith Elliot H EH Schevon Catherine C Jacobs Joshua J

Nature communications 20200518 1

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 ...[more]

PMID: 32424312

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Project description:Interactions between the hippocampus (area CA1) and prefrontal cortex (PFC) are crucial for memory-guided behavior. Theta oscillations (?8 Hz) underlie a key physiological mechanism for mediating these coordinated interactions, and theta oscillatory coherence and phase-locked spiking in the two regions have been shown to be important for spatial memory. Hippocampal place-cell activity associated with theta oscillations encodes spatial position during behavior, and theta phase-associated spiking is known to further mediate a temporal code for space within CA1 place fields. Although prefrontal neurons are prominently phase-locked to hippocampal theta oscillations in spatial memory tasks, whether and how theta oscillations mediate processing of spatial information across these networks remains unclear. Here, we addressed these questions using simultaneous recordings of dorsal CA1-PFC ensembles and population decoding analyses in male rats performing a continuous spatial working memory task known to require hippocampal-prefrontal interactions. We found that in addition to CA1, population activity in PFC can also encode the animal's current spatial position on a theta-cycle timescale during memory-guided behavior. Coding of spatial position was coherent for CA1 and PFC ensembles, exhibiting correlated position representations within theta cycles. In addition, incorporating theta-phase information during decoding to account for theta-phase associated spiking resulted in a significant improvement in the accuracy of prefrontal spatial representations, similar to concurrent CA1 representations. These findings indicate a theta-oscillation-mediated mechanism of temporal coordination for shared processing and communication of spatial information across the two networks during spatial memory-guided behavior.SIGNIFICANCE STATEMENT Theta oscillation- (?8 Hz) mediated interactions between the hippocampus and prefrontal cortex are known to be important for spatial memory. Hippocampal place-cell activity associated with theta oscillations underlies a rate and temporal code for spatial position, but it is not known whether these oscillations mediate simultaneous coding of spatial information in hippocampal-prefrontal networks. Here, we found that population activity in prefrontal cortex encodes animals' current position coherently with hippocampal populations on a theta-cycle timescale. Further we found that theta phase-associated spiking significantly improves prefrontal coding of spatial position, in parallel with hippocampal coding. Our findings establish that theta oscillations mediate a temporal coordination mechanism for coherent coding of spatial position in hippocampal-prefrontal networks during memory-guided behavior.

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Functionally distinct high and low theta oscillations in the human hippocampus.

Publications

Functionally distinct high and low theta oscillations in the human hippocampus.

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