The DOI matches its Crossref record; 56 of the 56 references it cites were found in a registry or an index.
Dendritic spines disappear with chilling but proliferate excessively upon rewarming of mature hippocampus
Abstract
More dendritic spine synapses occur on mature neurons in hippocampal slices by 2 h of incubation in vitro, than in perfusion-fixed hippocampus. What conditions initiate this spinogenesis and how rapidly do the spines begin to proliferate on mature neurons? To address these questions, CA1 field of the hippocampus neurons expressing green fluorescent protein in living slices from mature mice were imaged with two-photon microscopy. Spines disappeared and dendrites were varicose immediately after slice preparation in ice-cold artificial cerebrospinal fluid (ACSF). Electron microscopy (EM) revealed disrupted dendritic cytoplasm, enlarged or free-floating postsynaptic densities, and excessive axonal endocytosis. Upon warming dendritic varicosities shrank and spines rapidly reappeared within a few minutes illustrating the remarkable resilience of mature hippocampal neurons in slices. When membrane impermeant sucrose was substituted for NaCl in ACSF dendrites remained spiny at ice-cold temperatures and EM revealed less disruption. Nevertheless, spine number and length increased within 30 min in warm ACSF even when the extracellular calcium concentration was zero and synaptic transmission was blocked. When slices were first recovered for several hours and then chilled in 6 degrees C ACSF many spines disappeared and the dendrites became varicose. Upon re-warming varicosities shrank and spines reemerged in the same position from which they disappeared. In addition, new spines formed and…
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“Data from investigators using in vitro ischemia, tissue cooling, and epilepsy support findings that spines can be reversibly altered (Hasbani et al., 2001;Kirov et al., 2004;Zeng et al., 2007).”
From Two-Photon Imaging of Stroke Onset In Vivo Reveals That NMDA-Receptor Independent Ischemic Depolarization Is the Major Cause of Rapid Reversible Damage to Dendrites and Spines (2008) · cites this paper as Kirov et al., 2004
In the citing paper
“In the case of ion imbalance brought about by brain slicing in vitro, a similar phenomenon occurs, and the recovered dendrites are apparently functional because synaptic transmission is observed (Hasbani et al., 2001;Kirov et al., 2004).”
From Rapid Reversible Changes in Dendritic Spine Structure In Vivo Gated by the Degree of Ischemia (2005) · cites this paper as Kirov et al., 2004
In the citing paper
“The cytoskeleton appears to be quite resilient in vivo, because reperfusion is associated with a remarkable reversal of swollen spines and their dendrites toward normal structure, consistent with work done in vitro (Hasbani et al., 2001;Kirov et al., 2004).”
From Rapid Reversible Changes in Dendritic Spine Structure In Vivo Gated by the Degree of Ischemia (2005) · cites this paper as Kirov et al., 2004
In the citing paper
“These in vitro findings suggest that the presynaptic terminal is still attached during the reversible dendritic swelling.”
From Rapid Reversible Changes in Dendritic Spine Structure In Vivo Gated by the Degree of Ischemia (2005) · cites this paper as Kirov et al., 2004
Citations
Cites
An Energy Budget for Signaling in the Grey Matter of the Brain
Attwell, D., & Laughlin, S. B. (2001) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1097/00004647-200110000-00001 · Cited by 3,543
Synaptic Activity and the Construction of Cortical Circuits
Katz, L. C., & Shatz, C. J. (1996) · Science · doi:10.1126/science.274.5290.1133 · Cited by 3,048
Ischemic Cell Death in Brain Neurons
Lipton, P. (1999) · Physiological Reviews · doi:10.1152/physrev.1999.79.4.1431 · Cited by 3,043
Imaging Neuronal Subsets in Transgenic Mice Expressing Multiple Spectral Variants of GFP
Feng, G., Mellor, R. H., Bernstein, M., Keller-Peck, C., Nguyen, Q. T., Wallace, M., Nerbonne, J. M., Lichtman, J. W., & Sanes, J. R. (2000) · Neuron · doi:10.1016/s0896-6273(00)00084-2 · Cited by 3,042
Gautier, J. (1993) · Trends in Biochemical Sciences · doi:10.1016/0968-0004(93)90025-i · Cited by 2,200
Longitudinal Assessment of Neurocognitive Function after Coronary-Artery Bypass Surgery
Newman, M. F., Kirchner, J., Phillips‐Bute, B., Gaver, V., Grocott, H. P., Jones, R. H., Mark, D. B., Reves, J. G., & Blumenthal, J. A. (2001) · New England Journal of Medicine · doi:10.1056/nejm200102083440601 · Cited by 1,963
Axo-somatic and axo-dendritic synapses of the cerebral cortex: an electron microscope study.
Eg, G. (1959) · PubMed · Cited by 1,768
Harris, K. M., & Kater, S. B. (1994) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.17.030194.002013 · Cited by 1,020
Self-citationEvidence for a Role of Dendritic Filopodia in Synaptogenesis and Spine Formation
Ziv, N. E., & Smith, S. J. (1996) · Neuron · doi:10.1016/s0896-6273(00)80283-4 · Cited by 882
Synaptogenesis Via Dendritic Filopodia in Developing Hippocampal Area CA1
Fiala, J. C., Feinberg, M., Popov, V., & Harris, K. M. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-21-08900.1998 · Cited by 758
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- Gray, 1959, Axo-somatic and axo-dendritic synapses of the cerebral cortex, J Anat, 93, 420
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Items 101–171 of 171
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Arstikaitis, P., Gauthier-Campbell, C., Huang, K., El-Husseini, A., & Murphy, T. H. (2011) · PLoS ONE · doi:10.1371/journal.pone.0016998 · Cited by 27
Calcium‐triggered exit of F‐actin and IP3 3‐kinase A from dendritic spines is rapid and reversible
Schell, M. J., & Irvine, R. F. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.05125.x · Cited by 25
Slice It Hot: Acute Adult Brain Slicing in Physiological Temperature
Ankri, L., Yarom, Y., & Uusisaari, M. Y. (2014) · Journal of Visualized Experiments · doi:10.3791/52068 · Cited by 25
Technical report: surgical preparation of human brain tissue for clinical and basic research
Straehle, J., Ravi, V. M., Heiland, D. H., Galanis, C., Lenz, M., Zhang, J., Neidert, N. N., Rahal, A. E., Vasilikos, I., Kellmeyer, P., et al. (2023) · Acta Neurochirurgica · doi:10.1007/s00701-023-05611-9 · Cited by 23
Harris, K. M. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.0735-19.2019 · Cited by 20
Self-citationSword, J., Croom, D., Wang, P. L., Thompson, R. J., & Kirov, S. A. (2016) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x16639328 · Cited by 20
Self-citationSuzuki, T., Kametani, K., Weiheng, G., & Li, W. (2017) · Journal of Neurochemistry · doi:10.1111/jnc.14254 · Cited by 20
Rapid dendritic and axonal responses to neuronal insults
Mizielinska, S., Greenwood, S. M., Tummala, H., & Connolly, C. N. (2009) · Biochemical Society Transactions · doi:10.1042/bst0371389 · Cited by 18
Combination of diOlistic labeling with retrograde tract tracing and immunohistochemistry
Neely, M. D., Stanwood, G. D., & Deutch, A. Y. (2009) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2009.08.016 · Cited by 18
Focal Cooling Devices for the Surgical Treatment of Epilepsy
Smyth, M. D., & Rothman, S. M. (2011) · Neurosurgery Clinics of North America · doi:10.1016/j.nec.2011.07.011 · Cited by 18
Cold‐induced exodus of postsynaptic proteins from dendritic spines
Cheng, H., Huang, Z., Lin, W., Chow, W., & Chang, Y. (2008) · Journal of Neuroscience Research · doi:10.1002/jnr.21852 · Cited by 18
Rescue of Synaptic Phenotypes and Spatial Memory in Young Fragile X Mice
Sun, M., Hongpaisan, J., & Alkon, D. L. (2016) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.115.231100 · Cited by 17
Triviño-Paredes, J., Nahirney, P. C., Pinar, C., Grandes, P., & Christie, B. R. (2019) · Journal of Neurophysiology · doi:10.1152/jn.00332.2019 · Cited by 17
Álvarez‐Merz, I., Fomitcheva, I. V., Sword, J., Hernández-Guijo, J. M., Solís, J. M., & Kirov, S. A. (2022) · Glia · doi:10.1002/glia.24241 · Cited by 17
Self-citationChen, S., Tran, S., Sigler, A., & Murphy, T. H. (2010) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2010.12.018 · Cited by 16
Karbowski, J. (2015) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1004532 · Cited by 18
Moniliform deformation of retinal ganglion cells by formaldehyde‐based fixatives
Stradleigh, T. W., Greenberg, K. P., Partida, G. J., Pham, A., & Ishida, A. T. (2014) · The Journal of Comparative Neurology · doi:10.1002/cne.23689 · Cited by 15
Sdrulla, A. D., & Linden, D. J. (2006) · The Cerebellum · doi:10.1080/14734220600620908 · Cited by 16
Ueda, A., & Wu, C. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00010 · Cited by 15
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Bjelobaba, I. M., Lavrnja, I. C., Parabucki, A., Stojkov, D., Stojiljković, M., Peković, S., & Nedeljković, N. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.06.063 · Cited by 14
Activity-Dependent Structural Plasticity of Dendritic Spines
Chapleau, C. A., & Pozzo‐Miller, L. D. (2008) · Elsevier eBooks · doi:10.1016/b978-012370509-9.00039-5 · Cited by 14
Neuronal Activity: From In Vitro Preparation to Behaving Animals
Windels, F. (2006) · Molecular Neurobiology · doi:10.1385/mn:34:1:1 · Cited by 13
Identification of a prosurvival neuroprotective mitochondrial peptide in a mammalian hibernator
Szereszewski, K. E., & Storey, K. B. (2019) · Cell Biochemistry and Function · doi:10.1002/cbf.3422 · Cited by 13
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González-Riaño, C., Tapia‐González, S., Perea, G., González-Arias, C., DeFelipe, J., & Barbas, C. (2021) · Molecular Neurobiology · doi:10.1007/s12035-020-02264-y · Cited by 13
Sheridan, G. K., Pickering, M., Twomey, C., Moynagh, P. N., O'Connor, J. J., & Murphy, K. J. (2007) · Learning & Memory · doi:10.1101/lm.590007 · Cited by 13
Baptisms of fire or death knells for acute-slice physiology in the age of ‘omics’ and light?
Khurana, S., & Li, W.-K. (2013) · Reviews in the Neurosciences · doi:10.1515/revneuro-2013-0028 · Cited by 11
Becker, D., Willems, L. M., Vnencak, M., Zahn, N., Schuldt, G., Jedlička, P., Maggio, N., Deller, T., & Vlachos, A. (2012) · PLoS ONE · doi:10.1371/journal.pone.0048500 · Cited by 12
Morphology and Fractal-Based Classifications of Neurons and Microglia in Two and Three Dimensions
Karperien, A., & Jelinek, H. F. (2024) · Advances in neurobiology · doi:10.1007/978-3-031-47606-8_7 · Cited by 8
Suryavanshi, P. S., Baule, S. M., & Glykys, J. C. (2024) · eNeuro · doi:10.1523/eneuro.0007-24.2024 · Cited by 8
Sword, J., Fomitcheva, I. V., & Kirov, S. A. (2024) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x241257887 · Cited by 9
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Xie, Y., Chen, S., & Murphy, T. H. (2012) · PLoS ONE · doi:10.1371/journal.pone.0036305 · Cited by 8
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Yan, J., Bai, J., Gao, C., Liang, Y., Zhao, B., & Bian, Y. (2017) · Neuroscience Letters · doi:10.1016/j.neulet.2017.02.070 · Cited by 9
Ferrucci, L., Basilico, B., Reverte, I., Pagani, F., Scaringi, G., Cordella, F., Cortese, B., Propris, G. D., Galeone, A., Mazzarella, L., et al. (2024) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2024.1456974 · Cited by 7
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Karperien, A., & Jelinek, H. F. (2016) · Springer series in computational neuroscience · doi:10.1007/978-1-4939-3995-4_6 · Cited by 7
Dumas, T. C., Uttaro, M. R., Barriga, C., Brinkley, T., Halavi, M., Wright, S. N., Ferrante, M., Evans, R. C., Hawes, S., & Sanders, E. M. (2018) · Neuroscience Letters · doi:10.1016/j.neulet.2018.05.011 · Cited by 6
Teilum, M., Krogh, M., Wieloch, T. W., & Mattiasson, G. (2007) · Journal of Proteome Research · doi:10.1021/pr070057l · Cited by 7
Zhang, S., Holmberg, E. G., & Geddes, J. W. (2007) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2007.02.013 · Cited by 6
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Hamad, M. I. K., Daoud, S., Petrova, P., Rabaya, O., Jbara, A., Melliti, N., Stichmann, S., Reiss, G., Herz, J., & Förster, E. (2020) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2020.108666 · Cited by 4
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Luz, L. L., Currie, S. P., & Daw, M. I. (2017) · PLoS ONE · doi:10.1371/journal.pone.0171897 · Cited by 3
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Rasse, T. M. (2005) · doi:10.53846/goediss-309 · Cited by 3
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Gupta, L., Amati, S., Ma, D. K., & Singhal, N. S. (2025) · Experimental Neurology · doi:10.1016/j.expneurol.2025.115558 · Cited by 3
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Hell, J. W., & Ehlers, M. (2008) · Springer eBooks · doi:10.1007/978-0-387-77232-5_1 · Cited by 2
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Trevelyan, A. J., & Yuste, R. (2009) · Neuromethods · doi:10.1007/978-1-60327-263-6_9 · Cited by 2
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Kirov, S. A. (2014) · Springer eBooks · doi:10.1007/978-1-4939-0974-2_7 · Cited by 2
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Suryavanshi, P. S., Tadinada, S. M., Baule, S. M., Jhaveri-Cruz, N., Abel, T. G., & Glykys, J. C. (2025) · Acta Neuropathologica Communications · doi:10.1186/s40478-025-02123-8 · Cited by 1
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D’Agati, D. V., & D’Agati, D. C. (2026) · International Review of Psychiatry · doi:10.1080/09540261.2026.2753429 · Cited by 1
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El-Husseini, A. (2008) · Springer eBooks · doi:10.1007/978-0-387-77232-5_7 · Cited by 1
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Giustarini, D., Ricci, C., Ceccarelli, I., Pieretti, S., André, P., Migliorini, S., Massai, L., Minosi, P., Casini, I., & Aloisi, A. M. (2022) · Open Journal of Endocrine and Metabolic Diseases · doi:10.4236/ojemd.2022.122004 · Cited by 1
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Guire, E. S. (2006) · doi:10.6083/m4mw2fdw
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Metadata
- Authors
- Kirov, S. A., Petrak, L. J., Fiala, J. C., & Harris, K. M.
- Affiliations
- Augusta University (US)
- Boston University (US)
- Corresponding author
- Kirov, S.A
- Venue
- Neuroscience
- Publisher
- Elsevier BV
- Published
- 2004-01
- Volume
- 127
- Issue
- 1
- Pages
- 69-80
- ISSN
- 0306-4522 (ISSN-L)
- OpenAlex
- W2126033680
- Cited by
- 172
- References
- 56
- Citations by year
- 2026: 2 · 2025: 5 · 2024: 5 · 2023: 3 · 2022: 3 · 2021: 4 · 2020: 5 · 2019: 3 · 2018: 2 · 2017: 7 · 2016: 7 · 2015: 7 · 2014: 12 · 2013: 6 · 2012: 12
- FWCI
- 5.63
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Mental Health (K01 MH 02000, K01MH002000)
- National Institute of Neurological Disorders and Stroke (R01NS033574, NS21184, NS33574)
- 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
- dendritic spines, spine plasticity, spinogenesis, CA1 pyramidal neurons, rewarming, dendritic varicosities, postsynaptic density, sucrose replacement, neuronal recovery, ion homeostasis, two-photon imaging
- MeSH terms
- Animals, Calcium, Cerebrospinal Fluid, Cold Temperature, Dendrites, Hippocampus, Homeostasis, Male, Mice, Transgenic, Microscopy, Electron, Synaptic Transmission, Neuronal Plasticity, Sucrose, Synapses, Synaptic Membranes, Temperature, Water-Electrolyte Balance, Cell Size, Mice
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