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Synapse-Specific Adaptations to Inactivity in Hippocampal Circuits Achieve Homeostatic Gain Control while Dampening Network Reverberation
Open accessAbstract
Synaptic homeostasis, induced by chronic changes in neuronal activity, is well studied in cultured neurons, but not in more physiological networks where distinct synaptic circuits are preserved. We characterized inactivity-induced adaptations at three sets of excitatory synapses in tetrodotoxin-treated organotypic hippocampal cultures. The adaptation to inactivity was strikingly synapse specific. Hippocampal throughput synapses (dentate-to-CA3 and CA3-to-CA1) were upregulated, conforming to homeostatic gain control in order to avoid extreme limits of neuronal firing. However, chronic inactivity decreased mEPSC frequency at CA3-to-CA3 synapses, which were isolated pharmacologically or surgically. This downregulation of recurrent synapses was opposite to that expected for conventional homeostasis, in apparent conflict with typical gain control. However, such changes contributed to an inactivity-induced shortening of reverberatory bursts generated by feedback excitation among CA3 pyramids, safeguarding the network from possible runaway excitation. Thus, synapse-specific adaptations of synaptic weight not only contributed to homeostatic gain control, but also dampened epileptogenic network activity.
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“Interestingly, not all excitatory neurons in cortical networks express synaptic scaling.In hippocampal networks CA1 neurons scale synapses up in response to activity blockade, whereas CA3 neurons do not (Kim and Tsien 2008).”
From Homeostatic Synaptic Plasticity: Local and Global Mechanisms for Stabilizing Neuronal Function (2012) · cites this paper as Kim and Tsien 2008
In the citing paper
“Interestingly, not all excitatory neurons in cortical networks express synaptic scaling.In hippocampal networks CA1 neurons scale synapses up in response to activity blockade, whereas CA3 neurons do not (Kim and Tsien 2008).”
From Homeostatic Synaptic Plasticity: Local and Global Mechanisms for Stabilizing Neuronal Function (2012) · cites this paper as Kim and Tsien 2008
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Cites
Activity-dependent scaling of quantal amplitude in neocortical neurons
Turrigiano, G. G., Leslie, K. R., Desai, N. S., Rutherford, L. C., & Nelson, S. B. (1998) · Nature · doi:10.1038/36103 · Cited by 2,226
HOMEOSTATIC CONTROL OF NEURAL ACTIVITY: From Phenomenology to Molecular Design
Davis, G. W. (2006) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.28.061604.135751 · Cited by 543
Burrone, J., O'Byrne, M., & Murthy, V. N. (2002) · Nature · doi:10.1038/nature01242 · Cited by 487
Selective reconfiguration of layer 4 visual cortical circuitry by visual deprivation
Maffei, A., Nelson, S. B., & Turrigiano, G. G. (2004) · Nature Neuroscience · doi:10.1038/nn1351 · Cited by 415
Potentiation of cortical inhibition by visual deprivation
Maffei, A., Nataraj, K., Nelson, S. B., & Turrigiano, G. G. (2006) · Nature · doi:10.1038/nature05079 · Cited by 383
Kamiya, H., Shinozaki, H., & Yamamoto, C. (1996) · The Journal of Physiology · doi:10.1113/jphysiol.1996.sp021395 · Cited by 327
Activity-dependent regulation of inhibitory synaptic transmission in hippocampal neurons
Hartman, K. N., Pal, S. K., Burrone, J., & Murthy, V. N. (2006) · Nature Neuroscience · doi:10.1038/nn1677 · Cited by 221 · cited 1×
“This sets the interpretation of our data apart from any developmental influence; this is of relevance because responses to inactivity may vary widely depending on the maturity of the neural network (Burrone et al., 2002; Hartman et al., 2006; Karmarkar and Buonomano, 2006; Kirov et al., 2004).”
Flagged first, then by citations
Research works printed but not linked: 64
- Abdul-Ghani, 1996, Sr2+ and quantal events at excitatory synapses between mouse hippocampal neurons in culture, J. Physiol., 495, 113, 10.1113/jphysiol.1996.sp021578 · DOI
- Aptowicz, 2004, Homeostatic plasticity in hippocampal slice cultures involves changes in voltage-gated Na+ channel expression, Brain Res., 998, 155, 10.1016/j.brainres.2003.11.035 · DOI
- Bausch, 2006, Plasticity of both excitatory and inhibitory synapses is associated with seizures induced by removal of chronic blockade of activity in cultured hippocampus, J. Neurophysiol., 96, 2151, 10.1152/jn.00355.2006 · DOI
- Beggs, 2003, Neuronal avalanches in neocortical circuits, J. Neurosci., 23, 11167, 10.1523/JNEUROSCI.23-35-11167.2003 · DOI · Paper page
- Bekkers, 1999, Quantal amplitude and quantal variance of strontium-induced asynchronous EPSCs in rat dentate granule neurons, J. Physiol., 516, 227, 10.1111/j.1469-7793.1999.227aa.x · DOI
- Bennett, 1994, Dynamics of the CA3 pyramidal neuron autoassociative memory network in the hippocampus, Philos. Trans. R. Soc. Lond. B Biol. Sci., 343, 167, 10.1098/rstb.1994.0019 · DOI
- Buchs, 1993, Structural modifications associated with synaptic development in area CA1 of rat hippocampal organotypic cultures, Brain Res. Dev. Brain Res., 71, 81, 10.1016/0165-3806(93)90108-M · DOI
- Buckby, 2006, Network stability through homeostatic scaling of excitatory and inhibitory synapses following inactivity in CA3 of rat organotypic hippocampal slice cultures, Mol. Cell. Neurosci., 31, 805, 10.1016/j.mcn.2006.01.009 · DOI
- Burrone, 2003, Synaptic gain control and homeostasis, Curr. Opin. Neurobiol., 13, 560, 10.1016/j.conb.2003.09.007 · DOI
- Dailey, 1994, Mossy fiber growth and synaptogenesis in rat hippocampal slices in vitro, J. Neurosci., 14, 1060, 10.1523/JNEUROSCI.14-03-01060.1994 · DOI
- De Simoni, 2003, Development of rat CA1 neurones in acute versus organotypic slices: role of experience in synaptic morphology and activity, J. Physiol., 550, 135, 10.1113/jphysiol.2003.039099 · DOI
- Desai, 1999, Plasticity in the intrinsic excitability of cortical pyramidal neurons, Nat. Neurosci., 2, 515, 10.1038/9165 · DOI · Paper page
- Drakew, 1996, Spine loss in experimental epilepsy: quantitative light and electron microscopic analysis of intracellularly stained CA3 pyramidal cells in hippocampal slice cultures, Neuroscience, 70, 31, 10.1016/0306-4522(95)00379-W · DOI
- Echlin, 1963, Epileptiform seizures from chronic isolated cortex, Arch. Neurol., 9, 154, 10.1001/archneur.1963.00460080064009 · DOI
- Fricke, 1984, Electrophysiology of dentate gyrus granule cells, J. Neurophysiol., 51, 195, 10.1152/jn.1984.51.2.195 · DOI
- Furshpan, 1989, Seizure-like activity and cellular damage in rat hippocampal neurons in cell culture, Neuron, 3, 199, 10.1016/0896-6273(89)90033-0 · DOI
- Galvan, 2000, Blockade of neuronal activity during hippocampal development produces a chronic focal epilepsy in the rat, J. Neurosci., 20, 2904, 10.1523/JNEUROSCI.20-08-02904.2000 · DOI
- Galvan, 2003, Postsynaptic contributions to hippocampal network hyperexcitability induced by chronic activity blockade in vivo, Eur. J. Neurosci., 18, 1861, 10.1046/j.1460-9568.2003.02920.x · DOI
- Gerfin-Moser, 1995, Alterations in glutamate but not GABAA receptor subunit expression as a consequence of epileptiform activity in vitro, Neuroscience, 67, 849, 10.1016/0306-4522(95)00130-B · DOI
- Houweling, 2005, Homeostatic synaptic plasticity can explain post-traumatic epileptogenesis in chronically isolated neocortex, Cereb. Cortex, 15, 834, 10.1093/cercor/bhh184 · DOI
- Ju, 2004, Activity-dependent regulation of dendritic synthesis and trafficking of AMPA receptors, Nat. Neurosci., 7, 244, 10.1038/nn1189 · DOI
- Kakegawa, 2004, Input- and subunit-specific AMPA receptor trafficking underlying long-term potentiation at hippocampal CA3 synapses, Eur. J. Neurosci., 20, 101, 10.1111/j.1460-9568.2004.03461.x · DOI
- Kamiya, 1999, Dual mechanism for presynaptic modulation by axonal metabotropic glutamate receptor at the mouse mossy fibre-CA3 synapse, J. Physiol., 518, 497, 10.1111/j.1469-7793.1999.0497p.x · DOI
- Karmarkar, 2006, Different forms of homeostatic plasticity are engaged with distinct temporal profiles, Eur. J. Neurosci., 23, 1575, 10.1111/j.1460-9568.2006.04692.x · DOI
- Kirov, 2004, Age-dependence in the homeostatic upregulation of hippocampal dendritic spine number during blocked synaptic transmission, Neuropharmacology, 47, 640, 10.1016/j.neuropharm.2004.07.039 · DOI
- Lauri, 2003, Activity blockade increases the number of functional synapses in the hippocampus of newborn rats, Mol. Cell. Neurosci., 22, 107, 10.1016/S1044-7431(02)00012-X · DOI
- Liu, 1995, Properties of synaptic transmission at single hippocampal synaptic boutons, Nature, 375, 404, 10.1038/375404a0 · DOI
- McKinney, 1997, Lesion-induced axonal sprouting and hyperexcitability in the hippocampus in vitro: implications for the genesis of posttraumatic epilepsy, Nat. Med., 3, 990, 10.1038/nm0997-990 · DOI
- Miles, 1983, Single neurones can initiate synchronized population discharge in the hippocampus, Nature, 306, 371, 10.1038/306371a0 · DOI
- Miles, 1984, Synchronized afterdischarges in the hippocampus: contribution of local synaptic interactions, Neuroscience, 12, 1179, 10.1016/0306-4522(84)90012-5 · DOI
- Montgomery, 2001, Pair recordings reveal all-silent synaptic connections and the postsynaptic expression of long-term potentiation, Neuron, 29, 691, 10.1016/S0896-6273(01)00244-6 · DOI
- Moulder, 2004, Plastic elimination of functional glutamate release sites by depolarization, Neuron, 42, 423, 10.1016/S0896-6273(04)00184-9 · DOI
- Moulder, 2006, Physiological activity depresses synaptic function through an effect on vesicle priming, J. Neurosci., 26, 6618, 10.1523/JNEUROSCI.5498-05.2006 · DOI
- Muller, 1993, Morphological and functional consequences of chronic epilepsy in rat hippocampal slice cultures, Pflugers Arch., 422, 418, 10.1007/BF00374304 · DOI
- Muller, 1993, Time course of synaptic development in hippocampal organotypic cultures, Brain Res. Dev. Brain Res., 71, 93, 10.1016/0165-3806(93)90109-N · DOI
- Muller, 1993, Reversible loss of dendritic spines and altered excitability after chronic epilepsy in hippocampal slice cultures, Proc. Natl. Acad. Sci. USA, 90, 257, 10.1073/pnas.90.1.257 · DOI
- Nakazawa, 2002, Requirement for hippocampal CA3 NMDA receptors in associative memory recall, Science, 297, 211, 10.1126/science.1071795 · DOI
- O'Brien, 1998, Activity-dependent modulation of synaptic AMPA receptor accumulation, Neuron, 21, 1067, 10.1016/S0896-6273(00)80624-8 · DOI · Paper page
- Petralia, 1996, The metabotropic glutamate receptors, mGluR2 and mGluR3, show unique postsynaptic, presynaptic and glial localizations, Neuroscience, 71, 949, 10.1016/0306-4522(95)00533-1 · DOI
- Robain, 1994, Development of mossy fiber synapses in hippocampal slice culture, Brain Res. Dev. Brain Res., 80, 244, 10.1016/0165-3806(94)90109-0 · DOI
- Rutecki, 1985, Epileptiform activity induced by changes in extracellular potassium in hippocampus, J. Neurophysiol., 54, 1363, 10.1152/jn.1985.54.5.1363 · DOI
- Scanziani, 1994, Role of excitatory amino acid and GABAB receptors in the generation of epileptiform activity in disinhibited hippocampal slice cultures, Neuroscience, 61, 823, 10.1016/0306-4522(94)90405-7 · DOI
- Scanziani, 1995, Presynaptic inhibition of excitatory synaptic transmission by muscarinic and metabotropic glutamate receptor activation in the hippocampus: are Ca2+ channels involved?, Neuropharmacology, 34, 1549, 10.1016/0028-3908(95)00119-Q · DOI
- Schwartzkroin, 1978, Cellular and field potential properties of epileptogenic hippocampal slices, Brain Res., 147, 117, 10.1016/0006-8993(78)90776-X · DOI
- Shigemoto, 1997, Differential presynaptic localization of metabotropic glutamate receptor subtypes in the rat hippocampus, J. Neurosci., 17, 7503, 10.1523/JNEUROSCI.17-19-07503.1997 · DOI · Paper page
- Staley, 1998, Presynaptic modulation of CA3 network activity, Nat. Neurosci., 1, 201, 10.1038/651 · DOI
- Stoppini, 1991, A simple method for organotypic cultures of nervous tissue, J. Neurosci. Methods, 37, 173, 10.1016/0165-0270(91)90128-M · DOI
- Sutton, 2006, Miniature neurotransmission stabilizes synaptic function via tonic suppression of local dendritic protein synthesis, Cell, 125, 785, 10.1016/j.cell.2006.03.040 · DOI · Paper page
- Swann, 1993, Localized excitatory synaptic interactions mediate the sustained depolarization of electrographic seizures in developing hippocampus, J. Neurosci., 13, 4680, 10.1523/JNEUROSCI.13-11-04680.1993 · DOI
- Thiagarajan, 2002, α- and βCaMKII. Inverse regulation by neuronal activity and opposing effects on synaptic strength, Neuron, 36, 1103, 10.1016/S0896-6273(02)01049-8 · DOI
- Thiagarajan, 2005, Adaptation to synaptic inactivity in hippocampal neurons, Neuron, 47, 725, 10.1016/j.neuron.2005.06.037 · DOI
- Thompson, 1992, Comparison of the actions of adenosine at pre- and postsynaptic receptors in the rat hippocampus in vitro, J. Physiol., 451, 347, 10.1113/jphysiol.1992.sp019168 · DOI
- Thomson, 2000, Facilitation, augmentation and potentiation at central synapses, Trends Neurosci., 23, 305, 10.1016/S0166-2236(00)01580-0 · DOI
- Trasande, 2007, Activity deprivation leads to seizures in hippocampal slice cultures: is epilepsy the consequence of homeostatic plasticity?, J. Clin. Neurophysiol., 24, 154, 10.1097/WNP.0b013e318033787f · DOI
- Traub, 1982, Cellular mechanism of neuronal synchronization in epilepsy, Science, 216, 745, 10.1126/science.7079735 · DOI
- Traub, 1993, Synaptic and intrinsic conductances shape picrotoxin-induced synchronized after-discharges in the guinea-pig hippocampal slice, J. Physiol., 461, 525, 10.1113/jphysiol.1993.sp019527 · DOI
- Turrigiano, 2004, Homeostatic plasticity in the developing nervous system, Nat. Rev. Neurosci., 5, 97, 10.1038/nrn1327 · DOI · Paper page
- Tyler, 2003, Miniature synaptic transmission and BDNF modulate dendritic spine growth and form in rat CA1 neurones, J. Physiol., 553, 497, 10.1113/jphysiol.2003.052639 · DOI
- Wong, 1984, Local circuit interactions in synchronization of cortical neurones, J. Exp. Biol., 112, 169, 10.1242/jeb.112.1.169 · DOI
- Wong, 1986, Cellular basis of neuronal synchrony in epilepsy, Adv. Neurol., 44, 583
- Yoon, 1991, Adenosine inhibits excitatory but not inhibitory synaptic transmission in the hippocampus, J. Neurosci., 11, 1375, 10.1523/JNEUROSCI.11-05-01375.1991 · DOI
- Yoshino, 1996, A metabotropic glutamate receptor agonist DCG-IV suppresses synaptic transmission at mossy fiber pathway of the guinea pig hippocampus, Neurosci. Lett., 207, 70, 10.1016/0304-3940(96)12486-1 · DOI
- Zimmer, 1984, Cellular and connective organization of slice cultures of the rat hippocampus and fascia dentata, J. Comp. Neurol., 228, 432, 10.1002/cne.902280310 · DOI
- Zucker, 1989, Short-term synaptic plasticity, Annu. Rev. Neurosci., 12, 13, 10.1146/annurev.ne.12.030189.000305 · DOI
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Metadata
- Authors
- Kim, J., & Tsien, R. W.
- Affiliations
- Stanford Medicine (US)
- Corresponding author
- Tsien, Richard W.
- ORCID
- Tsien, Richard W.
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2008-06
- Volume
- 58
- Issue
- 6
- Pages
- 925-937
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC2561251
- OpenAlex
- W2001651016
- Cited by
- 124
- References
- 0
- Citations by year
- 2026: 4 · 2025: 6 · 2024: 7 · 2023: 2 · 2022: 5 · 2021: 6 · 2020: 6 · 2019: 4 · 2018: 4 · 2017: 7 · 2016: 4 · 2015: 6 · 2014: 9 · 2013: 20 · 2012: 8
- FWCI
- 3.75
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Mental Health (R37MH071739)
- National Institute of General Medical Sciences (R01GM058234)
- National Institute of Neurological Disorders and Stroke (R01NS024067)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- synaptic homeostasis, hippocampus, excitatory synapses, CA3 pyramidal cells, epileptogenesis, organotypic hippocampal slice cultures, tetrodotoxin
- MeSH terms
- Adaptation, Physiological, Animals, Hippocampus, Homeostasis, Nerve Net, Neural Inhibition, Neuronal Plasticity, Synapses, Rats, Sprague-Dawley, Excitatory Postsynaptic Potentials, Rats
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