Selective neuromodulation and mutual inhibition within the <scp>CA3–CA2</scp> system can prioritize sequences for replay

Stöber, Tristan M.; Lehr, Andrew B.; Hafting, Torkel; Kumar, Arvind; Fyhn, Marianne

doi:10.1002/hipo.23256

Cited by 23 publications

(23 citation statements)

References 94 publications

(188 reference statements)

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“…8a-d ), which may lead to interference between these memories. These finding suggest a key contribution of ripple-associated CA2 activity may be in the selection or prioritization of specific assemblies to participate in a given SWR event(Stober et al, 2020). Whether this is due to CA2 input directly into CA1 or its recruitment of local inhibition in CA3(Boehringer et al, 2017) cannot be determined from the current data.…”

Section: Discussionmentioning

confidence: 99%

CA2 inhibition reduces the precision of hippocampal assembly reactivation

Boehringer

Huang

et al. 2020

Preprint

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The structured reactivation of hippocampal neuronal ensembles during fast synchronous oscillatory events termed sharp-wave ripples (SWRs) has been suggested to play a crucial role in the storage and use of memory. Activity in both the CA2 and CA3 subregions can proceed this population activity in CA1 and chronic inhibition of either region alters SWR oscillations. However, the precise contribution of CA2 to the oscillation, as well as to the reactivation of CA1 neurons within it, remains unclear. Here we employ chemogenetics to transiently silence CA2 pyramidal cells in mice and observe that while SWRs still occur, the reactivation of CA1 pyramidal cell ensembles within the events lose both temporal and informational precision. These observations suggest that CA2 activity contributes to the fidelity of experience-dependent hippocampal replay.

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Section: Discussionmentioning

confidence: 99%

CA2 inhibition reduces the precision of hippocampal assembly reactivation

Boehringer

Huang

et al. 2020

Preprint

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“…In hippocampal CA2, selective release of neuromodulators has been suggested to prioritize important experiences for replay via neuromodulator-dependent plasticity (dependent e.g. on vasopressin, oxytocin, or substance P; 70 , 71 ). Our results here suggest that widespread release coming after an experience can still selectively determine the neuronal subpopulation recruited to store a memory.…”

Section: Discussionmentioning

confidence: 99%

“…In addition to synaptic consolidation, they may also affect excitability 50 , 69 and early-phase synaptic plasticity at the time of encoding 74 – 78 , which can serve to select a subpopulation of neurons for memory formation 50 before undergoing neuromodulator-dependent consolidation. Even without strong electrical stimulation, neuromodulators can induce a slow-onset potentiation that lasts for hours 49 , 70 , 79 , 80 . Furthermore, for different brain regions, there can be different neuromodulatory requirements for STC, for example in hippocampal CA1 vs. CA2 80 – 83 .…”

Section: Discussionmentioning

confidence: 99%

Neuromodulator-dependent synaptic tagging and capture retroactively controls neural coding in spiking neural networks

Lehr

Luboeinski

Tetzlaff

2022

Sci Rep

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Events that are important to an individual’s life trigger neuromodulator release in brain areas responsible for cognitive and behavioral function. While it is well known that the presence of neuromodulators such as dopamine and norepinephrine is required for memory consolidation, the impact of neuromodulator concentration is, however, less understood. In a recurrent spiking neural network model featuring neuromodulator-dependent synaptic tagging and capture, we study how synaptic memory consolidation depends on the amount of neuromodulator present in the minutes to hours after learning. We find that the storage of rate-based and spike timing-based information is controlled by the level of neuromodulation. Specifically, we find better recall of temporal information for high levels of neuromodulation, while we find better recall of rate-coded spatial patterns for lower neuromodulation, mediated by the selection of different groups of synapses for consolidation. Hence, our results indicate that in minutes to hours after learning, the level of neuromodulation may alter the process of synaptic consolidation to ultimately control which type of information becomes consolidated in the recurrent neural network.

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“…CA2 neurons have been shown to interact with CA1 neurons [193][194][195][196][197], modulating the classical function of CA1 neurons [198]. Evidence for specific modulation by vasopressin [199], oxytocin [199,200], substance P (SP) [201] and the enriched expression of their associated receptors in area CA2 suggests possible integration of neuromodulator signalling into the hippocampal information processing circuit via CA2 neurons [202,203].…”

Section: Synaptic Tagging In the Hippocampal Ca2 Areamentioning

confidence: 99%

Long‐term plasticity in the hippocampus: maintaining within and ‘tagging’ between synapses

2021

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Synapses between neurons are malleable biochemical structures, strengthening and diminishing over time dependent on the type of information they receive. This phenomenon known as synaptic plasticity underlies learning and memory, and its different forms, Long-Term Potentiation (LTP) and Long-Term Depression (LTD) perform varied cognitive roles in reinforcement, relearning and associating memories. Moreover, both LTP and LTD can exist in an early transient form (early-LTP/LTD) or a late persistent form (late-LTP/LTD), which are triggered by different induction protocols, and also differ in their dependence on protein synthesis and the involvement of key molecular players. Beyond homosynaptic modifications, synapses can also interact with one another. This is encapsulated in the Synaptic Tagging and Capture hypothesis (STC), where synapses expressing early-LTP/LTD present a 'tag' that can capture the protein synthesis products generated during a temporally proximal late-LTP/LTD induction. This 'tagging' phenomenon forms the framework of synaptic interactions in various conditions, and accounts for the cellular basis of the time-dependent associativity of short-lasting and long-lasting memories. All these synaptic modifications take place under controlled neuronal conditions, regulated by subcellular elements such as epigenetic regulation, proteasomal degradation and neuromodulatory signals. Here, we review current understanding of the different forms of synaptic plasticity and its regulatory mechanisms in the hippocampus, a brain region critical for memory formation. We also discuss expression of plasticity in hippocampal CA2 area, a long-overlooked narrow hippocampal subfield, and the behavioural correlate of STC. Lastly, we put forth perspectives for an integrated view of memory representation in synapses.

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Selective neuromodulation and mutual inhibition within the CA3–CA2 system can prioritize sequences for replay

Cited by 23 publications

References 94 publications

CA2 inhibition reduces the precision of hippocampal assembly reactivation

CA2 inhibition reduces the precision of hippocampal assembly reactivation

Neuromodulator-dependent synaptic tagging and capture retroactively controls neural coding in spiking neural networks

Long‐term plasticity in the hippocampus: maintaining within and ‘tagging’ between synapses

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