Intrinsic cellular and molecular properties of in vivo hippocampal synaptic plasticity are altered in the absence of key synaptic matrix molecules
Abstract
Hippocampal synaptic plasticity comprises a key cellular mechanism for information storage. In the hippocampus, both long‐term potentiation (LTP) and long‐term depression (LTD) are triggered by synaptic Ca 2+‐elevations that are typically mediated by the opening of voltage‐gated cation channels, such as N‐methyl‐d‐aspartate receptors (NMDAR), in the postsynaptic density. The integrity of the post‐synaptic density is ensured by the extracellular matrix (ECM). Here, we explored whether synaptic plasticity is affected in adult behaving mice that lack the ECM proteins brevican, neurocan, tenascin‐C, and tenascin‐R (KO). We observed that the profiles of synaptic potentiation and depression in the dentate gyrus (DG) were profoundly altered compared to plasticity profiles in wild‐type littermates (WT). Specifically, synaptic depression was amplified in a frequency‐dependent manner and although late‐LTP (>24 hr) was expressed following strong afferent tetanization, the early component of LTP (<75 min post‐tetanization) was absent. LTP (>4 hr) elicited by weaker tetanization was equivalent in WT and KO animals. Furthermore, this latter form of LTP was NMDAR‐dependent in WT but not KO mice. Scrutiny of DG receptor expression revealed significantly lower levels of both the GluN2A and GluN2B subunits of the N‐methyl‐d‐aspartate receptor, of the metabotropic glutamate receptor, mGlu5 and of the L‐type calcium channel, Ca v 1.3 in KO compared to WT animals. Homer 1a and of the P/Q‐type calcium channel, Ca v 1.2 were unchanged in KO mice. Taken together, findings suggest that in mice that lack multiple ECM proteins, synaptic plasticity is intact, but is fundamentally different.
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The quadruple knockout mouse exhibited reduced short-term depression connected with changed frequency dependence in the dentate gyrus of the hippocampus subjected to a classical LTP paradigm.
“This also translates in an altered synaptic plasticity in vivo as the quadruple knockout mouse exhibited a reduced short-term depression connected with changed frequency dependence in the dentate gyrus of the hippocampus subjected to a classical LTP paradigm30.”
From Elimination of the four extracellular matrix molecules tenascin-C, tenascin-R, brevican and neurocan alters the ratio of excitatory and inhibitory synapses (2019) · cites this paper as [30]
A recently published study demonstrated altered synaptic plasticity in the dorsal dentate gyrus of the quadruple knockout hippocampus that translated into enhanced short-term depression in conjunction with modified frequency-dependence in vivo.
“A recently published study has demonstrated an altered synaptic plasticity in the dorsal dentate gyrus of the quadruple knockout hippocampus that translated into an enhanced short-term depression in conjunction with a modified frequency-dependence in vivo30.”
From Elimination of the four extracellular matrix molecules tenascin-C, tenascin-R, brevican and neurocan alters the ratio of excitatory and inhibitory synapses (2019) · cites this paper as [30]
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Reinhard, J., Mueller-Buehl, C., Wiemann, S., Roll, L., Luft, V., Shabani, H., Rathbun, D. L., Gan, L., Kuo, C., Franzen, J., et al. (2024) · iScience · doi:10.1016/j.isci.2024.108846 · Cited by 3 · see citing works
Self-citationNeural extracellular matrix regulates visual sensory motor integrationPreprint
Reinhard, J., Mueller-Buehl, C., Wiemann, S., Roll, L., Luft, V., Shabani, H., Rathbun, D. L., Gan, L., Kuo, C., Franzen, J., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.04.17.537074 · Cited by 2 · see citing works
Self-citationWhy do hippocampal mossy cells matter? It depends on the frequency and contextPreprint
Kolaric, K., Strauch, C., Li, Y., Woods, S. M., Lopes, M. A., Sivarajah, N., Teixeira, C. M., Lerch, J. P., Frankland, P. W., Henkelman, R. M., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.12.04.467951
Self-citation
- Authors
- Jansen, S., Gottschling, C., Faissner, A., & Manahan‐Vaughan, D.
- Affiliations
- Ruhr University Bochum (DE)
- Department of Cell Morphology and Molecular Neurobiology, Faculty of Biology and Biotechnology Ruhr University Bochum Bochum Germany
- Corresponding author
- Manahan‐Vaughan, Denise
- Venue
- Hippocampus
- Publisher
- Wiley
- Published
- 2017-05-29
- Volume
- 27
- Issue
- 8
- Pages
- 920-933
- ISSN
- 1050-9631 (ISSN-L)
- 1098-1063
- OpenAlex
- W2616760772
- Cited by
- 26
- References
- 76
- Citations by year
- 2025: 3 · 2024: 3 · 2023: 2 · 2022: 3 · 2021: 3 · 2020: 1 · 2019: 3 · 2018: 4 · 2017: 4
- FWCI
- 1.61
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Hippocampus (publishedVersion)
- PubMed (publishedVersion)
- Funders
- German Research Foundation (DFG) (FOR 1581/P2, FA159/22-1)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- hippocampal synaptic plasticity, extracellular matrix, brevican, neurocan, tenascin-C, tenascin-R, long-term potentiation, long-term depression, NMDA receptor, GluN2A, GluN2B, mGlu5, Cav1.3, dentate gyrus, knockout mice
- MeSH terms
- Animals, Animals, Newborn, Electric Stimulation, Extracellular Matrix, Hippocampus, Male, Mice, Transgenic, Neuronal Plasticity, Piperazines, Wakefulness, Receptors, N-Methyl-D-Aspartate, Patch-Clamp Techniques, Excitatory Amino Acid Antagonists, Tenascin, Calcium Channels, L-Type, Mice, Neurocan, Brevican
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