Parvalbumin-positive interneurons mediate neocortical-hippocampal interactions that are necessary for memory consolidation

Xia, Frances; Richards, Blake A; Tran, Matthew M; Josselyn, Sheena A.; Takehara‐Nishiuchi, Kaori; Frankland, Paul W.

doi:10.7554/elife.27868

Cited by 166 publications

(203 citation statements)

References 75 publications

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“…The mechanistic details of how new myelin formation acts to support remote memory is a salient question and requires a thorough understanding of how neuronal ensembles act in concert to achieve memory consolidation and retrieval. Though this remains an active area of research, several points appear to be true: 1) systems consolidation involves substantial interregional reorganization of neuronal networks in the form of neuronal engram ensembles 24,25,28,43,44 ; 2) active interregional communication between brain regions separated in space, arbitrated by the myelinated axons of projection neurons, is required for both successful memory consolidation and retrieval 24,25,27,45,46,47,48 ; 3) this interregional communication seems to be characterized by a high degree of temporal precision, particularly in the form of synchronized oscillatory activity , 46,47 . Thus, there are several conceivable ways through which new myelin formation can interact with or complement neural circuits to support systems consolidation and remote memory retrieval.…”

Section: Future Directionsmentioning

confidence: 99%

Preservation of a remote fear memory requires new myelin formation

et al. 2020

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Section: Future Directionsmentioning

confidence: 99%

Preservation of a remote fear memory requires new myelin formation

et al. 2020

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“…These oscillations modulate grid cell spiking and organize neuronal activity into temporal windows that is believed to be important for episodic memory formation and plasticity (38,39). PV + neurons are vital for producing synchronized activity in local networks and for organizing information transfer between brain areas (40,41). Hence, changes in PV + cell function and inhibitory plasticity could have a widespread effect on the synchronized activity of the MEC network.…”

Section: Pnn Removal Alters Theta Oscillationsmentioning

confidence: 99%

Perineuronal nets stabilize the grid cell network

Christensen

Lensjø

Lepperød

et al. 2019

Preprint

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Grid cells are part of a widespread network that supports navigation and spatial memory. Stable grid patterns appear late in development, in concert with extracellular matrix aggregates termed perineuronal nets (PNNs) that condense around inhibitory neurons. To reveal the relationship between stable spatial representations and the presence of PNNs we recorded from populations of neurons in adult rats. We show that removal of PNNs leads to lower inhibitory spiking activity, and reduces grid cells' ability to create stable representations of a novel environment. Furthermore, in animals with disrupted PNNs, exposure to a novel arena corrupted the spatiotemporal relationships within grid cell modules, and the stored representations of a familiar arena. Finally, we show that PNN removal in entorhinal cortex distorted spatial representations in downstream hippocampal neurons. Together this work suggests that PNNs provide a key stabilizing element for the grid cell network.(9, 11). Once established, the periodic spiking pattern of grid cells is remarkably stable when animals revisit the same environment. Local perturbations of different cell types in MEC cause changes to grid field spike rates or an increased number of out-of-field spikes, but the location of the fields remains unaltered (12)(13)(14). Furthermore, when placed in a different environment, neighboring populations of grid cells show a coherent shift of grid fields (15) that retains their relative spatiotemporal relationships (16). In contrast the hippocampal place cells remap by independently and unpredictably changing their activity. This suggests that the mature grid cell network is more hardwired and less plastic than the hippocampal place cell network.The network that controls grid cell spiking is not yet fully understood, but recurrent inhibition appears to be fundamental to the specific activity of grid cells. Stellate cells, one of the two principal cell types that display grid cell firing (7 ), are connected via parvalbumin expressing (PV + ) inhibitory interneurons (17 , 18). PV + cells account for about 50% of the inhibitory cells in MEC (19), making them the main inhibitory mediator in the local grid cell network. In sensory cortex, PV + cells play a central role in shaping the excitatory activity of principal neurons by regulating the onset of periods of high synaptic plasticity (20). Whether PV + inhibitory neurons in MEC play a similar role for development of the grid cell network remains elusive.A hallmark of maturing PV + cells is that aggregates of specialized extracellular matrix, called perineuronal nets (PNNs), condense on the cell soma and proximal dendrites, leaving openings only for synaptic connections (21). PNNs are believed to help stabilize the activity of PV + cells by supporting synaptic integrity and limiting synaptogenesis, in addition to supporting PV + cell physiology (22). By the time PNNs in sensory cortex are fully mature, plasticity in the local network is strongly reduced. However, juvenile levels of plasticity can be r...

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“…Recent in vivo work has shown the importance of parvalbumin-expressing (PV+) fast-spiking interneurons in hippocampal fear memory consolidation (18,20,29). Optogenetic or pharmacogenetic inhibition of PV+ interneurons in hippocampal area CA1 decreased theta-band oscillations during both post-CFC REM and NREM sleep, without altering the firing frequency of neighboring cells.…”

Section: Theta-band Resonance In the Network Mediates Increased Netwomentioning

confidence: 99%

Network resonance during slow-wave sleep facilitates memory consolidation through phase-coding

Skilling

Clawson

Eniwaye

et al. 2019

Preprint

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Sleep plays a critical role in memory consolidation, however, the exact role that sleep and its effects on neural network dynamics play in this process is still unclear. Here, we combine computational and experimental approaches to study the dynamical, network-wide underpinnings of hippocampal memory consolidation during sleep. We provide data to support a novel hypothesis on the role of cellular resonance with sleep-associated theta band (4-12 Hz) hippocampal oscillations in this process. We show that increases in the stability of hippocampal memory representations after learning (which predicts successful memory consolidation) are mediated through emergent network-wide resonance and locking of neuronal activity to network oscillations. These changes arise in the network as a function of changes to network structure during learning, and mirror experimental findings in the hippocampus. Finally, we show that input-dependent pattern formation (e.g. "replay") in the hippocampus during sleep states, together with spike timing dependent plasticity (STDP)-based memory consolidation, leads to universal network activity reorganization. This reorganization generates heterogeneous changes in neuronal spiking frequency, similar to what has been observed in a variety of brain circuits across periods of sleep. Our results support the hypothesis that sleep plays an active role in memory consolidation by switching the hippocampal network from rate-based to phase-based information representation. The mechanisms through which this occurs supports the integration of heterogeneous cell populations into memory traces. 2Significance Statement : In this study, we provide a mechanistic explanation of how sleep selectively facilitates memory consolidation, through recruitment of heterogeneous neuronal populations and structural reorganization of the network into an engram. Specifically, we show that emergent theta band oscillations during sleep facilitate stabilization of memory representations via spike timing dependent reinforcement. This stabilization, together with STDP, allows for systematic reorganization of synaptic connections within these populations, universally redistributing firing rates of participating neurons. Simultaneously, network oscillations facilitate a switch from rate-to phase-coding of information among neuronal populations with highly heterogenous firing frequencies, incorporating more neurons into the engram. Our results reconcile discrepant findings on network reorganization during sleep, and demonstrate a clear mechanism for both strengthening and weakening of synaptic efficacy during sleep.

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Parvalbumin-positive interneurons mediate neocortical-hippocampal interactions that are necessary for memory consolidation

Cited by 166 publications

References 75 publications

Preservation of a remote fear memory requires new myelin formation

Preservation of a remote fear memory requires new myelin formation

Perineuronal nets stabilize the grid cell network

Network resonance during slow-wave sleep facilitates memory consolidation through phase-coding

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