Multiple forms of synaptic plasticity triggered by selective suppression of activity in individual neurons
Abstract
The rules by which neuronal activity causes long-term modification of synapses in the central nervous system are not fully understood. Whereas competitive or correlation-based rules result in local modification of synapses, homeostatic modifications allow neuron-wide changes in synaptic strength, promoting stability. Experimental investigations of these rules at central nervous system synapses have relied generally on manipulating activity in populations of neurons. Here, we investigated the effect of suppressing excitability in single neurons within a network of active hippocampal neurons by overexpressing an inward-rectifier potassium channel. Reducing activity in a neuron before synapse formation leads to a reduction in functional synaptic inputs to that neuron; no such reduction was observed when activity of all neurons was uniformly suppressed. In contrast, suppressing activity in a single neuron after synapses are established results in a homeostatic increase in synaptic input, which restores the activity of the neuron to control levels. Our results highlight the differences between global and selective suppression of activity, as well as those between early and late manipulation of activity.
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Central neurons are able to maintain average firing rates around a homeostatic set point.
“There is compelling evidence from experiments in neuronal cultures that central neurons are able to maintain average firing rates around a homeostatic set point.”
From Homeostatic Synaptic Plasticity: Local and Global Mechanisms for Stabilizing Neuronal Function (2012) · cites this paper as Burrone et al. 2002
When cortical or hippocampal neurons are induced to fire more than normal, over many hours firing returns to baseline levels; if neuronal firing is reduced over time, neurons compensate and firing is restored.
“When cortical or hippocampal neurons are induced to fire more than normal, over many hours firing returns to baseline levels, and similarly, if neuronal firing is reduced over time, neurons compensate and again firing is restored (Fig. 1A) (Turrigiano et al. 1998;Burrone et al. 2002).”
From Homeostatic Synaptic Plasticity: Local and Global Mechanisms for Stabilizing Neuronal Function (2012) · cites this paper as Burrone et al. 2002
Like synaptic scaling, the presynaptic form of plasticity can be induced in a cell-autonomous manner by a reduction in postsynaptic depolarization.
“Like synaptic scaling, this presynaptic form of plasticity can also be induced in a cell-autonomous manner by a reduction in postsynaptic depolarization (Burrone et al. 2002).”
From Homeostatic Synaptic Plasticity: Local and Global Mechanisms for Stabilizing Neuronal Function (2012) · cites this paper as Burrone et al. 2002
Chronic hyperpolarization of an entire neuron by expression of an inwardly rectifying K channel does not induce postsynaptic scaling, suggesting that chronic global hyperpolarization of neuronal dendrites and somata overrides the signals that induce scaling up in response to a drop in firing.
“Interestingly, chronic hyperpolarization of an entire neuron by expression of an inwardly rectifying K channel (K ir ) does not induce postsynaptic scaling (Burrone et al. 2002;Hou et al. 2008), suggesting that chronic global hyperpolarization of neuronal dendrites and somata overrides the signals that induce scaling up in response to a drop in firing.”
From Homeostatic Synaptic Plasticity: Local and Global Mechanisms for Stabilizing Neuronal Function (2012) · cites this paper as Burrone et al. 2002
Chronic hyperpolarization of entire neurons (including dendrites) results in enhanced Pr, suggesting that Pr can be bidirectionally regulated by changes in the amount of dendritic depolarization.
“This is consistent with evidence that chronic hyperpolarization of entire neurons (including dendrites) results in enhanced P r (Burrone et al. 2002), suggesting that P r can be bidirectionally regulated by changes in the amount of dendritic depolarization.”
From Homeostatic Synaptic Plasticity: Local and Global Mechanisms for Stabilizing Neuronal Function (2012) · cites this paper as Burrone et al. 2002
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References 30 · Cited by 487
- Authors
- Burrone, J., O'Byrne, M., & Murthy, V. N.
- Affiliations
- Harvard University (US)
- Corresponding author
- Murthy, Venkatesh N.
- Venue
- Nature
- Published
- 2002-11
- Volume
- 420
- Issue
- 6914
- Pages
- 414-418
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W2039655932
- Cited by
- 487
- References
- 30
- Citations by year
- 2026: 7 · 2025: 12 · 2024: 21 · 2023: 24 · 2022: 13 · 2021: 12 · 2020: 10 · 2019: 20 · 2018: 13 · 2017: 17 · 2016: 24 · 2015: 27 · 2014: 28 · 2013: 36 · 2012: 18
- FWCI
- 6.53
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Research Portal (King's College London) (submittedVersion)
- Funders
- Alfred P. Sloan Foundation
- National Alliance for Research on Schizophrenia and Depression
- National Institutes of Health
- Office of Naval Research
- 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 plasticity, homeostatic plasticity, neuronal activity, inwardly rectifying potassium channels, hippocampus, synaptic input, network activity, central nervous system synapses
- MeSH terms
- Action Potentials, Cells, Cultured, Hippocampus, Homeostasis, Humans, Neural Inhibition, Neuronal Plasticity, Neurons, Synapses, Tetrodotoxin, Patch-Clamp Techniques, Excitatory Postsynaptic Potentials, Potassium Channels, Inwardly Rectifying
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