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Theta oscillations coordinate grid-like representations between ventromedial prefrontal and entorhinal cortex

ABSTRACT: Description Human iEEG reveals synchronous theta oscillations and coordinated grid-like representations between vmPFC and entorhinal cortex. Grid cells and theta oscillations are fundamental constituents of the brain’s navigation system and have been described in the entorhinal cortex (EC). Recent fMRI studies reveal that the ventromedial prefrontal cortex (vmPFC) contains grid-like representations. However, the neural mechanisms underlying human vmPFC grid-like representations and their interactions with EC grid activity have remained unknown. We conducted intracranial electroencephalography (iEEG) recordings from epilepsy patients during a virtual spatial navigation task. Oscillatory theta power in the vmPFC exhibited a sixfold rotational symmetry that was coordinated with grid-like representations in the EC. We found that synchronous theta oscillations occurred between these regions that predicted navigational performance. Analysis of information transfer revealed a unidirectional signal from vmPFC to EC during memory retrieval. Together, this study provides insights into the previously unknown neural signature and functional role of grid-like representations outside the EC and their synchronization with the entorhinal grid during human spatial navigation.

SUBMITTER: Chen D

PROVIDER: S-EPMC8550230 | biostudies-literature |

REPOSITORIES: biostudies-literature

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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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Theta oscillations coordinate grid-like representations between ventromedial prefrontal and entorhinal cortex

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