The role of replay and theta sequences in mediating hippocampal‐prefrontal interactions for memory and cognition

Zielinski, Mark C.; Tang, Wenbo; Jadhav, Shantanu P.

doi:10.1002/hipo.22821

Cited by 68 publications

(56 citation statements)

References 131 publications

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“…Interestingly, spatial decoding accuracy showed a behavioral-dependent decrease near choice points in both CA1 and PFC. Hippocampal theta sequences are known to be prominent during these behavioral epochs and support non-local representations of behaviorally relevant trajectories or upcoming goals (Johnson and Redish, 2007;Gupta et al, 2012;Wikenheiser and Redish, 2015;Zielinski et al, 2017). Our results raise the possibility that a similar mechanism of theta phase-mediated coordination can support non-local coding in hippocampal-prefrontal networks.…”

Section: Discussionmentioning

confidence: 51%

Coherent Coding of Spatial Position Mediated by Theta Oscillations in the Hippocampus and Prefrontal Cortex

Zielinski¹,

Shin²,

Jadhav

2019

J. Neurosci.

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Interactions between the hippocampus (area CA1) and prefrontal cortex (PFC) are crucial for memory-guided behavior. Theta oscillations (ϳ8 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 thetaphase 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.Theta oscillation-(ϳ8 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 hippocampalprefrontal 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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Section: Discussionmentioning

confidence: 51%

Coherent Coding of Spatial Position Mediated by Theta Oscillations in the Hippocampus and Prefrontal Cortex

Zielinski¹,

Shin²,

Jadhav

2019

J. Neurosci.

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“…from seconds down to less than 100 ms) and with reduced numbers of total action potentials [2,9,10]. These compressed sequences may occur during SWRs that happen either during offline waking states such as during eating or drinking [11,12] or during non-rapid eye movement (nonREM) sleep when SWRs are most common [2,6,9,13].…”

Section: Replay In the Hippocampusmentioning

confidence: 99%

Patterned activation of action potential patterns during offline states in the neocortex: replay and non-replay

Liu

Watson

2020

Phil. Trans. R. Soc. B

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Action potential generation (spiking) in the neocortex is organized into repeating non-random patterns during both awake experiential states and non-engaged states ranging from inattention to sleep to anaesthesia—and even occur in slice preparations. Repeating patterns in a given population of neurons between states may imply a common means by which cortical networks can be engaged despite brain state changes, but super-imposed on this common firing is a variability that is both specific to ongoing inputs and can be re-shaped by experience. This similarity with specifically induced variance may allow for a range of processes including perception, memory consolidation and network homeostasis. Here, we review how patterned activity in neocortical populations has been studied and what it may imply for a cortex that must be both static and plastic. This article is part of the Theo Murphy meeting issue ‘Memory reactivation: replaying events past, present and future’.

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“…Coherent CA1-PFC replay can thus mediate planning of correct future trajectory based on the completed past trajectory. This PFC read-out interpretation is supported by a bias toward CA1-leading-PFC directionality during replay Rothschild et al, 2016), which can potentially be tested using selective causal perturbation of coherent PFC replay (Shin and Jadhav, 2016;Tang and Jadhav, 2018;Zielinski et al, 2017).…”

Section: Discussionmentioning

confidence: 99%

Awake hippocampal-prefrontal replay mediates spatial learning and decision making

Shin

Tang

Jadhav

2019

Preprint

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Spatial learning requires remembering and choosing paths to goals. Hippocampal place cells replay spatial paths during immobility in reverse and forward order, offering a potential mechanism. However, how replay mediates both goal-directed learning and memory-guided decision making is unclear. We therefore continuously tracked replay in the same hippocampalprefrontal ensembles throughout learning of a spatial alternation task. We found that during pauses between behavioral trajectories, awake reverse and forward hippocampal replay consistently mediated an internal cognitive search of all available past and future possibilities, and exhibited opposing learning gradients for prediction of past and future behavioral paths, respectively. Coordinated hippocampal-prefrontal replay mediated recall of correct past paths and selection of future choices leading to reward based on the hippocampal cognitive search, executing spatial working memory rules. Our findings reveal a learning shift from hippocampal reverse-replay-based retrospective evaluation to forward-replay-based prospective planning, with prefrontal filtering of memory-guided paths for learning and decision-making.

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The role of replay and theta sequences in mediating hippocampal‐prefrontal interactions for memory and cognition

Cited by 68 publications

References 131 publications

Coherent Coding of Spatial Position Mediated by Theta Oscillations in the Hippocampus and Prefrontal Cortex

Coherent Coding of Spatial Position Mediated by Theta Oscillations in the Hippocampus and Prefrontal Cortex

Patterned activation of action potential patterns during offline states in the neocortex: replay and non-replay

Awake hippocampal-prefrontal replay mediates spatial learning and decision making

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