Dendritic spikes in hippocampal granule cells are necessary for long-term potentiation at the perforant path synapse

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Abstract

Long-term potentiation (LTP) of synaptic responses is essential for hippocampal memory function. Perforant-path (PP) synapses on hippocampal granule cells (GCs) contribute to the formation of associative memories, which are considered the cellular correlates of memory engrams. However, the mechanisms of LTP at these synapses are not well understood. Due to sparse firing activity and the voltage attenuation in their dendrites, it remains unclear how associative LTP at distal synapses occurs. Here, we show that NMDA receptor-dependent LTP can be induced at PP-GC synapses without backpropagating action potentials (bAPs) in acute rat brain slices. Dendritic recordings reveal substantial attenuation of bAPs as well as local dendritic Na ⁺ spike generation during PP-GC input. Inhibition of dendritic Na ⁺ spikes impairs LTP induction at PP-GC synapse. These data suggest that dendritic spikes may constitute a key cellular mechanism for memory formation in the dentate gyrus.

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Theta oscillations in the hippocampus.

György Buzsáki (2002)

Theta oscillations represent the "on-line" state of the hippocampus. The extracellular currents underlying theta waves are generated mainly by the entorhinal input, CA3 (Schaffer) collaterals, and voltage-dependent Ca(2+) currents in pyramidal cell dendrites. The rhythm is believed to be critical for temporal coding/decoding of active neuronal ensembles and the modification of synaptic weights. Nevertheless, numerous critical issues regarding both the generation of theta oscillations and their functional significance remain challenges for future research.

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A critical period for enhanced synaptic plasticity in newly generated neurons of the adult brain.

Shaoyu Ge, Chih-Hao Yang, Kuei-Sen Hsu … (2007)

Active adult neurogenesis occurs in discrete brain regions of all mammals and is widely regarded as a neuronal replacement mechanism. Whether adult-born neurons make unique contributions to brain functions is largely unknown. Here we systematically characterized synaptic plasticity of retrovirally labeled adult-born dentate granule cells at different stages during their neuronal maturation. We identified a critical period between 1 and 1.5 months of the cell age when adult-born neurons exhibit enhanced long-term potentiation with increased potentiation amplitude and decreased induction threshold. Furthermore, such enhanced plasticity in adult-born neurons depends on developmentally regulated synaptic expression of NR2B-containing NMDA receptors. Our study demonstrates that adult-born neurons exhibit the same classic critical period plasticity as neurons in the developing nervous system. The transient nature of such enhanced plasticity may provide a fundamental mechanism allowing adult-born neurons within the critical period to serve as major mediators of experience-induced plasticity while maintaining stability of the mature circuitry.

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Computational analysis of the role of the hippocampus in memory.

A. Treves, E Rolls (1994)

The authors draw together the results of a series of detailed computational studies and show how they are contributing to the development of a theory of hippocampal function. A new part of the theory introduced here is a quantitative analysis of how backprojections from the hippocampus to the neocortex could lead to the recall of recent memories. The theory is then compared with other theories of hippocampal function. First, what is computed by the hippocampus is considered. The hypothesis the authors advocate, on the basis of the effects of damage to the hippocampus and neuronal activity recorded in it, is that it is involved in the formation of new memories by acting as an intermediate-term buffer store for information about episodes, particularly for spatial, but probably also for some nonspatial, information. The authors analyze how the hippocampus could perform this function, by producing a computational theory of how it operates, based on neuroanatomical and neurophysiological information about the different neuronal systems contained within the hippocampus. Key hypotheses are that the CA3 pyramidal cells operate as a single autoassociation network to store new episodic information as it arrives via a number of specialized preprocessing stages from many association areas of the cerebral cortex, and that the dentate granule cell/mossy fiber system is important, particularly during learning, to help to produce a new pattern of firing in the CA3 cells for each episode. The computational analysis shows how many memories could be stored in the hippocampus and how quickly the CA3 autoassociation system would operate during recall. The analysis is then extended to show how the CA3 system could be used to recall a whole episodic memory when only a fragment of it is presented. It is shown how this recall could operate using modified synapses in backprojection pathways from the hippocampus to the cerebral neocortex, resulting in reinstatement of neuronal activity in association areas of the cerebral neocortex similar to that present during the original episode. The recalled information in the cerebral neocortex could then be used by the neocortex in the formation of long-term memories.

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Author and article information

Contributors

Sooyun Kim:

ORCID: http://orcid.org/0000-0002-2035-3247

Yoonsub Kim

Suk-Ho Lee

Won-Kyung Ho:

ORCID: http://orcid.org/0000-0003-1568-1710

John Huguenard: Role: Reviewing Editor

Journal

Journal ID (nlm-ta): eLife

Journal ID (iso-abbrev): Elife

Journal ID (publisher-id): eLife

Title: eLife

Publisher: eLife Sciences Publications, Ltd

ISSN (Electronic): 2050-084X

Publication date (Electronic, pub): 26 March 2018

Publication date Collection: 2018

Volume: 7

Electronic Location Identifier: e35269

Affiliations

[1 ]deptDepartment of Physiology Seoul National University College of Medicine SeoulKorea

[2 ]deptNeuroscience Research Institute Seoul National University College of Medicine SeoulKorea

[3]Stanford University School of Medicine United States

[4]Stanford University School of Medicine United States

Author information

Sooyun Kim http://orcid.org/0000-0002-2035-3247

Won-Kyung Ho http://orcid.org/0000-0003-1568-1710

Article

Publisher ID: 35269

DOI: 10.7554/eLife.35269

PMC ID: 5896953

PubMed ID: 29578411

SO-VID: 5ce55c95-99cd-440c-b22b-16f4629abe32

License:

This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

History

Date received : 21 January 2018

Date accepted : 25 March 2018

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100003725, National Research Foundation of Korea;

Award ID: NRF-2015R1C1A1A02037776

Award Recipient : Sooyun Kim

Funded by: FundRef http://dx.doi.org/10.13039/501100002701, Ministry of Education;

Award ID: Brain Korea 21 PLUS Program

Award Recipient : Sooyun Kim

Funded by: FundRef http://dx.doi.org/10.13039/501100003725, National Research Foundation of Korea;

Award ID: NRF-2010-0027941

Award Recipient : Won-Kyung Ho

Funded by: FundRef http://dx.doi.org/10.13039/501100003725, National Research Foundation of Korea;

Award ID: NRF-2017R1A2B2010186

Award Recipient : Won-Kyung Ho

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

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Author impact statement A novel mechanism of local plasticity in the distal dendrites of hippocampal granule cells.

ScienceOpen disciplines: Life sciences

Keywords: dentate gyrus granule cell,dendritic spike,perforant-path synapse,long-term potentiation,action potential backpropagation,active dendrites,rat

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ScienceOpen disciplines: Life sciences

Keywords: dentate gyrus granule cell, dendritic spike, perforant-path synapse, long-term potentiation, action potential backpropagation, active dendrites, rat

Dendritic spikes in hippocampal granule cells are necessary for long-term potentiation at the perforant path synapse

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Universal stem cells

Most cited references 47

Theta oscillations in the hippocampus.

A critical period for enhanced synaptic plasticity in newly generated neurons of the adult brain.

Computational analysis of the role of the hippocampus in memory.

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