Dendritic spines disappear with chilling but proliferate excessively upon rewarming of mature hippocampus

Kirov, S.A; Petrak, L.J; Fiala, J.C; Harris, K.M

doi:10.1016/j.neuroscience.2004.04.053

Cited by 172Neuroscience and Neuropharmacology ResearchMemory and Neural MechanismsNeurogenesis and neuroplasticity mechanisms

Dendritic spines disappear with chilling but proliferate excessively upon rewarming of mature hippocampus

Kirov, S.A, Petrak, L.J, Fiala, J.C, Harris, K.M·2004·Neuroscience

DOI 10.1016/j.neuroscience.2004.04.053

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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.
“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 OnsetIn VivoReveals 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 vitro, ion imbalance from brain slicing produces a similar reversible phenomenon, and recovered dendrites are apparently functional because synaptic transmission is observed.
“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 StructureIn VivoGated by the Degree of Ischemia (2005) · cites this paper as Kirov et al., 2004
The cytoskeleton appears quite resilient in vivo, because reperfusion is associated with a remarkable reversal of swollen spines and their dendrites toward normal structure, consistent with work in vitro.
“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 StructureIn VivoGated by the Degree of Ischemia (2005) · cites this paper as Kirov et al., 2004
These in vitro findings suggest that the presynaptic terminal is still attached during reversible dendritic swelling.
“These in vitro findings suggest that the presynaptic terminal is still attached during the reversible dendritic swelling.”
From Rapid Reversible Changes in Dendritic Spine StructureIn VivoGated by the Degree of Ischemia (2005) · cites this paper as Kirov et al., 2004

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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
ORCID: Kirov, S.A
Harris, K.M
Venue: Neuroscience
Publisher: Elsevier BV
Published: 2004-01
Volume: 127
Issue: 1
Pages: 69-80
ISSN: 0306-4522 (ISSN-L)
DOI: 10.1016/j.neuroscience.2004.04.053
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
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
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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Dendritic spines disappear with chilling but proliferate excessively upon rewarming of mature hippocampus

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