Presynaptic BDNF Required for a Presynaptic but Not Postsynaptic Component of LTP at Hippocampal CA1-CA3 Synapses
Open accessAbstract
Brain-derived neurotrophic factor (BDNF) has been implicated in several forms of long-term potentiation (LTP) at different hippocampal synapses. Using two-photon imaging of FM 1-43, a fluorescent marker of synaptic vesicle cycling, we find that BDNF is selectively required for those forms of LTP at Schaffer collateral synapses that recruit a presynaptic component of expression. BDNF-dependent forms of LTP also require activation of L-type voltage-gated calcium channels. One form of LTP with presynaptic expression, theta burst LTP, is thought to be of particular behavioral importance. Using restricted genetic deletion to selectively disrupt BDNF production in either the entire forebrain (CA3 and CA1) or in only the postsynaptic CA1 neuron, we localize the source of BDNF required for LTP to presynaptic neurons. These results suggest that long-term synaptic plasticity has distinct presynaptic and postsynaptic modules. Release of BDNF from CA3 neurons is required to recruit the presynaptic, but not postsynaptic, module of plasticity.
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Presynaptic release of BDNF is critical for LTP-induction in the hippocampus Schaffer collaterals.
“Presynaptic release of BDNF has been shown to be critical for LTP-induction in the hippocampus Schaffer collaterals (Zakharenko et al., 2003).”
From BDNF - a key transducer of antidepressant effects (2016) · cites this paper as Zakharenko et al., 2003
With intense induction protocols for LTP, a component of LTP requires the activation of VDCCs.
“with intense induction protocols for LTP a component of LTP requires the activation of VDCCs (49–51, 193, 196).”
From Synaptic memory and CaMKII (2023) · cites this paper as [196]
Cites
AMPA Receptor Trafficking and Synaptic Plasticity
Malinow, R., & Malenka, R. C. (2002) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.25.112701.142758 · Cited by 2,588 · see citing works
Neurotrophins as synaptic modulators
Poo, M.-M. (2001) · Nature Reviews Neuroscience · doi:10.1038/35049004 · Cited by 1,775 · see citing works
NEUROTROPHINS AND SYNAPTIC PLASTICITY
McAllister, A. K., Katz, L. C., & Lo, D. C. (1999) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.22.1.295 · Cited by 1,337 · see citing works
Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neurons
Frey, U., Huang, Y.-Y., & Kandel, E. R. (1993) · Science · doi:10.1126/science.8389057 · Cited by 1,218 · see citing works
Mice lacking brain-derived neurotrophic factor develop with sensory deficits
Ernfors, P., Lee, K.-F., & Jaenisch, R. (1994) · Nature · doi:10.1038/368147a0 · Cited by 1,067 · see citing works
Korte, M., Griesbeck, O., Gravel, C., Carroll, P., Staiger, V, Thoenen, H., & Bonhoeffer, T. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.22.12547 · Cited by 351 · see citing works
Visualization of changes in presynaptic function during long-term synaptic plasticity
Zakharenko, S. S., Zablow, L., & Siegelbaum, S. A. (2001) · Nature Neuroscience · doi:10.1038/89498 · Cited by 305 · see citing works
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Neurotrophin-regulated signalling pathways
Reichardt, L. F. (2006) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2006.1894 · Cited by 2,195 · see citing works
Neurotrophin regulation of neural circuit development and function
Park, H., & Poo, M.-M. (2013) · Nature Reviews Neuroscience · doi:10.1038/nrn3379 · Cited by 2,060 · see citing works
Fritsch, B., Reis, J., Martinowich, K., Schambra, H. M., Ji, Y., Cohen, L. G., & Lu, B. (2010) · Neuron · doi:10.1016/j.neuron.2010.03.035 · Cited by 1,420 · see citing works
BDNF: A Key Factor with Multipotent Impact on Brain Signaling and Synaptic Plasticity
Kowiański, P., Lietzau, G., Czuba, E., Waśkow, M., Steliga, A., & Moryś, J. (2018) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-017-0510-4 · Cited by 1,359 · see citing works
BDNF function in adult synaptic plasticity: The synaptic consolidation hypothesis
Bramham, C. R., & Messaoudi, E. (2005) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2005.06.003 · Cited by 1,193 · see citing works
Translational control of long-lasting synaptic plasticity and memory
Costa-Mattioli, M., Sossin, W. S., Klann, E., & Sonenberg, N. (2009) · Neuron · doi:10.1016/j.neuron.2008.10.055 · Cited by 944 · see citing works
BDNF - a key transducer of antidepressant effects
Björkholm, C., & Monteggia, L. M. (2016) · Neuropharmacology · doi:10.1016/j.neuropharm.2015.10.034 · Cited by 958 · see citing works
“Presynaptic release of BDNF has been shown to be critical for LTP-induction in the hippocampus Schaffer collaterals (Zakharenko et al., 2003).”
BackgroundKleim, J. A., Chan, S., Pringle, E., Schallert, K., Procaccio, V., Jimenez, R., & Cramer, S. C. (2006) · Nature Neuroscience · doi:10.1038/nn1699 · Cited by 529 · see citing works
BDNF and Hippocampal Synaptic Plasticity
Leal, G., Bramham, C. R., & Duarte, C. B. (2017) · Vitamins and Hormones · doi:10.1016/bs.vh.2016.10.004 · Cited by 425 · see citing works
Adachi, M., Barrot, M., Autry, A. E., Theobald, D., & Monteggia, L. M. (2008) · Biological Psychiatry · doi:10.1016/j.biopsych.2007.09.019 · Cited by 380 · see citing works
Neurobiology of local and intercellular BDNF signaling
Sasi, M., Vignoli, B., Canossa, M., & Blum, R. (2017) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-017-1964-4 · Cited by 324 · see citing works
Noble, E. E., Billington, C. J., Kotz, C. M., & Wang, C. (2011) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00776.2010 · Cited by 284 · see citing works
A conditional knockout mouse line of the oxytocin receptor
Lee, H.-J., Caldwell, H. K., Macbeth, A. H., Tolu, S. G., & Young, W. S. (2008) · Endocrinology · doi:10.1210/en.2007-1710 · Cited by 269 · see citing works
Molecular signals of plasticity at the tetrapartite synapse
Dityatev, A., & Rusakov, D. A. (2011) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2010.12.006 · Cited by 267 · see citing works
Pre- and postsynaptic twists in BDNF secretion and action in synaptic plasticity.
Edelmann, E., Leßmann, V., & Brigadski, T. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.05.043 · Cited by 248 · see citing works
Form follows function: BDNF and its involvement in sculpting the function and structure of synapses
Zagrebelsky, M., & Korte, M. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.05.029 · Cited by 241 · see citing works
Barrientos, R. M., Sprunger, D. B., Campeau, S., Watkins, L. R., Rudy, J. W., & Maier, S. F. (2004) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2004.06.009 · Cited by 192 · see citing works
Midbrain dopamine neurons bidirectionally regulate CA3-CA1 synaptic drive
Rosen, Z. B., Cheung, S., & Siegelbaum, S. A. (2015) · Nature Neuroscience · doi:10.1038/nn.4152 · Cited by 183 · see citing works
Ninan, I., Bath, K. G., Dagar, K., Perez-Castro, R., Plummer, M. R., Lee, F. S., & Chao, M. V. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.1405-10.2010 · Cited by 180 · see citing works
De Vincenti, A. P., Ríos, A. S., Paratcha, G., & Ledda, F. (2019) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00135 · Cited by 157 · see citing works
Park, H., Popescu, A., & Poo, M.-M. (2014) · Neuron · doi:10.1016/j.neuron.2014.10.045 · Cited by 142 · see citing works
Houlton, J., Abumaria, N., Hinkley, S. F. R., & Clarkson, A. N. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00790 · Cited by 138 · see citing works
Casey, B. J., Glatt, C. E., Tottenham, N., Soliman, F., Bath, K., Amso, D., Altemus, M., Pattwell, S., Jones, R., Levita, L., et al. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.03.081 · Cited by 129 · see citing works
Nicoll, R. A., & Schulman, H. (2023) · Physiological Reviews · doi:10.1152/physrev.00034.2022 · Cited by 126 · see citing works
“It is well accepted that CaMKII is required for the induction of NMDAR-dependent LTP, and the property of autonomy made CaMKII an ideal candidate for maintaining LTP.”
BackgroundInfluentialHigh abundance of BDNF within glutamatergic presynapses of cultured hippocampal neurons
Andreska, T., Aufmkolk, S., Sauer, M., & Blum, R. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00107 · Cited by 100 · see citing works
Cazorla, M., Jouvenceau, A., Rose, C., Guilloux, J.-P., Pilon, C., Dranovsky, A., & Prémont, J. (2010) · PLoS ONE · doi:10.1371/journal.pone.0009777 · Cited by 99 · see citing works
Macbeth, A. H., Stepp, J. E., Lee, H.-J., Young, W. S., & Caldwell, H. K. (2010) · Behavioral Neuroscience · doi:10.1037/a0020799 · Cited by 98 · see citing works
Earls, L. R., Bayazitov, I. T., Fricke, R. G., Berry, R. B., Illingworth, E., Mittleman, G., & Zakharenko, S. S. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.1425-10.2010 · Cited by 79 · see citing works
Self-citationOxytocin and the oxytocin receptor underlie intrastrain, but not interstrain, social recognition
Macbeth, A. H., Lee, H. ‐., Edds, J., & Young, W. S. (2009) · Genes, Brain and Behavior · doi:10.1111/j.1601-183x.2009.00506.x · Cited by 81 · see citing works
Dhakar, M. B., Rich, M. E., Reno, E. L., Lee, H.-J., & Caldwell, H. K. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2012.05.007 · Cited by 54 · see citing works
- Authors
- Zakharenko, S. S., Patterson, S. L., Dragatsis, I., Zeitlin, S. O., Siegelbaum, S. A., Kandel, E. R., & Morozov, A.
- Affiliations
- Howard Hughes Medical Institute (US)
- Columbia University (US)
- University of Virginia (US)
- Corresponding author
- Siegelbaum, Steven A
- ORCID
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2003-09
- Volume
- 39
- Issue
- 6
- Pages
- 975-990
- ISSN
- 0896-6273 (ISSN-L)
- OpenAlex
- W2013966390
- Cited by
- 334
- References
- 7
- Citations by year
- 2026: 7 · 2025: 7 · 2024: 8 · 2023: 8 · 2022: 7 · 2021: 5 · 2020: 14 · 2019: 12 · 2018: 13 · 2017: 10 · 2016: 7 · 2015: 11 · 2014: 20 · 2013: 22 · 2012: 15
- FWCI
- 6.02
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Mental Health (P50MH050733, MH-50733)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Nerve injury and regeneration
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- brain-derived neurotrophic factor, long-term potentiation, presynaptic plasticity, postsynaptic plasticity, Schaffer collateral synapses, L-type calcium channels, synaptic vesicle recycling, FM1-43, synaptic plasticity
- MeSH terms
- Animals, Female, Gene Expression Regulation, Hippocampus, Male, Mice, Inbred C57BL, Mice, Transgenic, Neurons, Synapses, Presynaptic Terminals, Long-Term Potentiation, Mice, Knockout, Brain-Derived Neurotrophic Factor, Mice
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