Activity-regulated dynamic behavior of early dendritic protrusions: evidence for different types of dendritic filopodia
Open accessAbstract
Dendritic filopodia are long and thin protrusions that occur predominantly during early development of the mammalian CNS. The function of dendritic filopodia is unknown, but they could serve to form early synapses, to generate spines, or to regulate dendritic branching and growth. We used two-photon imaging to characterize the motile behavior of dendritic protrusions during early postnatal development (P2-P12) in pyramidal neurons from acute slices of mouse neocortex. Dendritic protrusions in immature neurons are highly dynamic, and this motility is actin based. Motility and turnover of these early protrusions decreases throughout development, mirroring an increase in their average lifetime and density. Interestingly, density, motility, and length of filopodia are greater in dendritic growth cones than in dendritic shafts. These growth cones disappear after P5. Blocking synaptic transmission globally using TTX or calcium-free solutions led to a 40-120% increase in the density and length of dendritic filopodia in shafts but not in growth cones. Moreover, blocking ionotropic glutamate receptors resulted in an approximately 35% decrease in the density and turnover of shaft filopodia, whereas focal glutamate application led to a 75% increase in the length of shaft filopodia, but neither manipulation affected growth cone filopodia. Our results support the existence of two populations of filopodia, in growth cones and shafts, which are differentially regulated by neuronal activity. We propose that filopodia in dendritic growth cones are involved in dendritic growth and branching in an activity-independent manner, whereas shaft filopodia are responsible for activity-dependent synaptogenesis and, in some cases, may become dendritic spines.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Spine motility permits the sampling of large numbers of potential presynaptic partners before connections are stabilized via activity-dependent mechanisms.
“This would be advantageous, because spine motility permits the sampling of large numbers of potential presynaptic partners before connections are stabilized via activity-dependent mechanisms (Jontes and Smith, 2000; Portera-Cailliau et al., 2003).”
From The E3 ubiquitin ligase IDOL regulates synaptic ApoER2 levels and is important for plasticity and learning (2017) · cites this paper as Portera-Cailliau et al., 2003
The Introduction says spines are motile, and the discussion section 'Shaft filopodia: a role in synaptogenesis or spinogenesis' proposes that motile shaft filopodia seek suitable synaptic partners and that dendritic protrusions stabilize as activity increases. But the proposed partner-search mechanism concerns filopodia rather than spines; the paper does not establish that spine motility samples large numbers of partners before connections stabilize. (LLM, conf=0.86)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Long-term dendritic spine stability in the adult cortex
Grutzendler, J., Kasthuri, N., & Gan, W.-B. (2002) · Nature · doi:10.1038/nature01276 · Cited by 1,198 · see citing works
Rapid Actin-Based Plasticity in Dendritic Spines
Fischer, M., Kaech, S., Knutti, D., & Matus, A. (1998) · Neuron · doi:10.1016/s0896-6273(00)80467-5 · Cited by 905 · see citing works
Developmental regulation of spine motility in the mammalian central nervous system
Dunaevsky, A., Tashiro, A., Majewska, A., Mason, C., & Yuste, R. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.23.13438 · Cited by 412 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Experience-dependent structural synaptic plasticity in the mammalian brain
Holtmaat, A., & Svoboda, K. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2699 · Cited by 1,934 · see citing works
Transient and persistent dendritic spines in the neocortex in vivo
Holtmaat, A. J. G. D., Trachtenberg, J. T., Wilbrecht, L., Shepherd, G. M., Zhang, X., Knott, G. W., & Svoboda, K. (2005) · Neuron · doi:10.1016/j.neuron.2005.01.003 · Cited by 1,131 · see citing works
Microglia contact induces synapse formation in developing somatosensory cortex
Miyamoto, A., Wake, H., Ishikawa, A. W., Eto, K., Shibata, K., Murakoshi, H., Koizumi, S., Moorhouse, A. J., Yoshimura, Y., & Nabekura, J. (2016) · Nature Communications · doi:10.1038/ncomms12540 · Cited by 649 · see citing works
Synapse formation on neurons born in the adult hippocampus
Toni, N., Teng, E. M., Bushong, E. A., Aimone, J. B., Zhao, C., Consiglio, A., van Praag, H., Martone, M. E., Ellisman, M. H., & Gage, F. H. (2007) · Nature Neuroscience · doi:10.1038/nn1908 · Cited by 579 · see citing works
Korobova, F., & Svitkina, T. (2010) · Molecular Biology of the Cell · doi:10.1091/mbc.e09-07-0596 · Cited by 399 · see citing works
Bhatt, D. H., Zhang, S., & Gan, W.-B. (2009) · Annual Review of Physiology · doi:10.1146/annurev.physiol.010908.163140 · Cited by 380 · see citing works
Delayed Stabilization of Dendritic Spines in Fragile X Mice
Cruz-Martin, A., Crespo, M., & Portera-Cailliau, C. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.0577-10.2010 · Cited by 321 · see citing works
Self-citationRole of actin cytoskeleton in dendritic spine morphogenesis
Sekino, Y., Kojima, N., & Shirao, T. (2007) · Neurochemistry International · doi:10.1016/j.neuint.2007.04.029 · Cited by 294 · see citing works
Reversal of long-term dendritic spine alterations in Alzheimer disease models
Smith, D. L., Pozueta, J., Gong, B., Arancio, O., & Shelanski, M. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0908706106 · Cited by 229 · see citing works
Gao, X., Deng, P., Xu, Z. C., & Chen, J. (2011) · PLoS ONE · doi:10.1371/journal.pone.0024566 · Cited by 218 · see citing works
Spontaneous, synchronous electrical activity in neonatal mouse cortical neurones
Corlew, R., Bosma, M. M., & Moody, W. J. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2004.071621 · Cited by 163 · see citing works
Morphological Development of Thick-Tufted Layer V Pyramidal Cells in the Rat Somatosensory Cortex
Romand, S., Wang, Y., Toledo-Rodriguez, M., & Markram, H. (2011) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2011.00005 · Cited by 122 · see citing works
Yang, X.-D., Liao, X.-M., Uribe-Mariño, A., Liu, R., Xie, X.-M., Jia, J., Su, Y.-A., Li, J.-T., Schmidt, M. V., Wang, X.-D., et al. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2014.304 · Cited by 93 · see citing works
Khanal, P., & Hotulainen, P. (2021) · Cells · doi:10.3390/cells10092392 · Cited by 60 · see citing works
Krzisch, M., Temprana, S. G., Mongiat, L. A., Armida, J., Schmutz, V., Virtanen, M. A., Kocher-Braissant, J., Kraftsik, R., Vutskits, L., Conzelmann, K.-K., et al. (2015) · Brain Structure and Function · doi:10.1007/s00429-014-0768-y · Cited by 57 · see citing works
Mateos, J. M., Lüthi, A., Savic, N., Stierli, B., Streit, P., Gähwiler, B. H., & McKinney, R. A. (2007) · The Journal of Physiology · doi:10.1113/jphysiol.2006.120550 · Cited by 53 · see citing works
De Rubeis, S., Fernández, E., Buzzi, A., Di Marino, D., & Bagni, C. (2012) · Advances in Experimental Medicine and Biology · doi:10.1007/978-3-7091-0932-8_23 · Cited by 48 · see citing works
Gao, J., Marosi, M., Choi, J., Achiro, J. M., Kim, S., Li, S., Otis, K., Martin, K. C., Portera-Cailliau, C., & Tontonoz, P. (2017) · eLife · doi:10.7554/elife.29178 · Cited by 30 · see citing works
Self-citationZago, W. M., Massey, K. A., & Berg, D. K. (2006) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2005.11.009 · Cited by 24 · see citing works
- Authors
- Portera-Cailliau, C., Pan, D. T., & Yuste, R.
- Affiliations
- Columbia University (US)
- ORCID
- Yuste, Rafael
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2003-08-06
- Volume
- 23
- Issue
- 18
- Pages
- 7129-7142
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6740658
- OpenAlex
- W1834463603
- Cited by
- 269
- References
- 3
- Citations by year
- 2026: 2 · 2025: 5 · 2024: 7 · 2023: 9 · 2022: 2 · 2021: 10 · 2020: 14 · 2019: 7 · 2018: 6 · 2017: 11 · 2016: 11 · 2015: 10 · 2014: 16 · 2013: 13 · 2012: 21
- FWCI
- 4.95
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Parkinson Foundation
- John Merck Fund
- Parkinsonfonden
- National Eye Institute (R01EY013237, EY 13237)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Axon Guidance and Neuronal Signaling
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- dendritic filopodia, dendritic protrusions, dendritic shafts, dendritic spine formation, synaptogenesis, activity-dependent regulation, actin-based motility, glutamate receptors, TTX, dendritic branching, pyramidal neurons, neocortex
- MeSH terms
- Animals, Dendrites, Mice, Inbred C57BL, Mice, Transgenic, Synaptic Transmission, Pseudopodia, Somatosensory Cortex, Tetrodotoxin, Video Recording, Visual Cortex, Receptors, Glutamate, Pyramidal Cells, Excitatory Amino Acid Antagonists, Glutamic Acid, Microscopy, Video, Internet, Growth Cones, Mice, In Vitro Techniques
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
