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Theta and gamma rhythmic coding through two spike output modes in the hippocampus during spatial navigation.

ABSTRACT: Hippocampal CA1 neurons generate single spikes and stereotyped bursts of spikes. However, it is unclear how individual neurons dynamically switch between these output modes and whether these two spiking outputs relay distinct information. We performed extracellular recordings in spatially navigating rats and cellular voltage imaging and optogenetics in awake mice. We found that spike bursts are preferentially linked to cellular and network theta rhythms (3-12 Hz) and encode an animal's position via theta phase precession, particularly as animals are entering a place field. In contrast, single spikes exhibit additional coupling to gamma rhythms (30-100 Hz), particularly as animals leave a place field. Biophysical modeling suggests that intracellular properties alone are sufficient to explain the observed input frequency-dependent spike coding. Thus, hippocampal neurons regulate the generation of bursts and single spikes according to frequency-specific network and intracellular dynamics, suggesting that these spiking modes perform distinct computations to support spatial behavior.

SUBMITTER: Lowet E

PROVIDER: S-EPMC10530698 | biostudies-literature | 2023 Aug

REPOSITORIES: biostudies-literature

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Theta and gamma rhythmic coding through two spike output modes in the hippocampus during spatial navigation.

Lowet Eric E Sheehan Daniel J DJ Chialva Ulises U De Oliveira Pena Rodrigo R Mount Rebecca A RA Xiao Sheng S Zhou Samuel L SL Tseng Hua-An HA Gritton Howard H Shroff Sanaya S Kondabolu Krishnakanth K Cheung Cyrus C Wang Yangyang Y Piatkevich Kiryl D KD Boyden Edward S ES Mertz Jerome J Hasselmo Michael E ME Rotstein Horacio G HG Han Xue X

Cell reports 20230803 8

Hippocampal CA1 neurons generate single spikes and stereotyped bursts of spikes. However, it is unclear how individual neurons dynamically switch between these output modes and whether these two spiking outputs relay distinct information. We performed extracellular recordings in spatially navigating rats and cellular voltage imaging and optogenetics in awake mice. We found that spike bursts are preferentially linked to cellular and network theta rhythms (3-12 Hz) and encode an animal's position ...[more]

PMID: 37540599

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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.

Project description:Humans and non-human animals show great flexibility in spatial navigation, including the ability to return to specific locations based on as few as one single experience. To study spatial navigation in the laboratory, watermaze tasks, in which rats have to find a hidden platform in a pool of cloudy water surrounded by spatial cues, have long been used. Analogous tasks have been developed for human participants using virtual environments. Spatial learning in the watermaze is facilitated by the hippocampus. In particular, rapid, one-trial, allocentric place learning, as measured in the delayed-matching-to-place variant of the watermaze task, which requires rodents to learn repeatedly new locations in a familiar environment, is hippocampal dependent. In this article, we review some computational principles, embedded within a reinforcement learning framework, that utilise hippocampal spatial representations for navigation in watermaze tasks. We consider which key elements underlie their efficacy, and discuss their limitations in accounting for hippocampus-dependent navigation, both in terms of behavioural performance (i.e. how well do they reproduce behavioural measures of rapid place learning) and neurobiological realism (i.e. how well do they map to neurobiological substrates involved in rapid place learning). We discuss how an actor-critic architecture, enabling simultaneous assessment of the value of the current location and of the optimal direction to follow, can reproduce one-trial place learning performance as shown on watermaze and virtual delayed-matching-to-place tasks by rats and humans, respectively, if complemented with map-like place representations. The contribution of actor-critic mechanisms to delayed-matching-to-place performance is consistent with neurobiological findings implicating the striatum and hippocampo-striatal interaction in delayed-matching-to-place performance, given that the striatum has been associated with actor-critic mechanisms. Moreover, we illustrate that hierarchical computations embedded within an actor-critic architecture may help to account for aspects of flexible spatial navigation. The hierarchical reinforcement learning approach separates trajectory control via a temporal-difference error from goal selection via a goal prediction error and may account for flexible, trial-specific, navigation to familiar goal locations, as required in some arm-maze place memory tasks, although it does not capture one-trial learning of new goal locations, as observed in open field, including watermaze and virtual, delayed-matching-to-place tasks. Future models of one-shot learning of new goal locations, as observed on delayed-matching-to-place tasks, should incorporate hippocampal plasticity mechanisms that integrate new goal information with allocentric place representation, as such mechanisms are supported by substantial empirical evidence.

Dataset Information

Theta and gamma rhythmic coding through two spike output modes in the hippocampus during spatial navigation.

Publications

Theta and gamma rhythmic coding through two spike output modes in the hippocampus during spatial navigation.

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