Cited by 221Neuroscience and Neuropharmacology ResearchNeural dynamics and brain functionMemory and Neural Mechanisms

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Activity-dependent regulation of inhibitory synaptic transmission in hippocampal neurons

Hartman, Kenichi N, Pal, Sumon K, Burrone, Juan, Murthy, Venkatesh N·2006·Nature Neuroscience

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Abstract

Neural activity regulates the number and properties of GABAergic synapses in the brain, but the mechanisms underlying these changes are unclear. We found that blocking spike activity globally in developing hippocampal neurons from rats reduced the density of GABAergic terminals as well as the frequency and amplitude of miniature inhibitory postsynaptic currents (mIPSCs). Chronic inactivity later in development led to a reduction in the mIPSC amplitude, without any change in GABAergic synapse density. By contrast, hyperpolarizing or abolishing spike activity in single neurons did not alter GABAergic synaptic inputs. Suppressing activity in individual presynaptic GABAergic neurons also failed to decrease synaptic output. Our results indicate that GABAergic synapses are regulated by the level of activity in surrounding neurons. Notably, we found that the expression of GABAergic plasticity involves changes in the amount of neurotransmitter in individual vesicles.

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“For instance, inhibitory postsynaptic potentials (iPSPs) have been shown to decrease when global, but not single neuron, spiking activity is suppressed (Hartman et al. 2006, Peng et al. 2010).”
Background
Reduced neurosteroid potentiation of GABAA receptors in epilepsy and depolarized hippocampal neurons
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“…in the BDNF‐ TrkB signaling pathway could be glutamic acid decarboxylase 67 (GAD67), a GABA‐synthesizing enzyme that has been implicated in synaptic plasticity and dysfunction (Hartman et al., 2006; Hashimoto et al., 2005; Lau & Murthy, 2012; Lazarus et al., 2013; Sánchez‐ Huertas & Rico, 2011).”
BackgroundSelf-citation
Chemogenetic Suppression of GnRH Neurons during Pubertal Development Can Alter Adult GnRH Neuron Firing Rate and Reproductive Parameters in Female Mice
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“As Joseph and Turrigiano (2017) mention, whether previous studies achieved cell-autonomous inhibitory synaptic scaling depended highly on the particular experimental setup and manipulations (Hartman et al., 2006; Peng et al., 2010; Xue et al., 2014).”
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Competition and Homeostasis of Excitatory and Inhibitory Connectivity in the Adult Mouse Visual Cortex
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Unsupervised restoration of a complex learned behavior after large-scale neuronal perturbation
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“…hippocampal neurons during the period of rapid synaptogenesis in vitro, the blocking of spike activity by tetrodotoxin (TTX) reduces the density of inhibitory synapses, both onto glutamatergic and GABAergic target neurons, without affecting density of glutamatergic synapses (Hartman et al., 2006).”
Background
GABAergic synaptic scaling is triggered by changes in spiking activity rather than AMPA receptor activationPreprint
Gonzalez-Islas, C. E., Sabra, Z., Fong, M.-F., Yilmam, P., Yong, N. A., Engisch, K., & Wenner, P. (2024) · bioRxiv · doi:10.1101/2023.03.08.531789 · Cited by 4
“In addition, these homeostatic GABAergic responses precede and can outlast compensatory changes in the glutamatergic system.”
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Reelin Affects Signaling Pathways of a Group of Inhibitory Neurons and the Development of Inhibitory Synapses in Primary Neurons
Lee, S. E., & Lee, G. H. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22147510 · Cited by 5
Differential regulation of apical–basolateral dendrite outgrowth by activity in hippocampal neurons
Yuan, Y., Seong, E., Yuan, L., Singh, D., & Arikkath, J. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00314 · Cited by 4
“1 (Hartman et al., 2006) in developing neurons.”
Cortical inhibitory but not excitatory synaptic transmission and circuit refinement are altered after the deletion of NMDA receptors during early development
Deng, R., Chang, M., Kao, J. P. Y., & Kanold, P. O. (2023) · Scientific Reports · doi:10.1038/s41598-023-27536-0 · Cited by 3
Neural oligarchy: how synaptic plasticity breeds neurons with extreme influencePreprint
Kleberg, F. I., & Triesch, J. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/361394 · Cited by 23
“Although there exists evidence for SN in 119 glutamatergic and GABAergic synapses [27,28,43] as well as slow scaling [9, 45] within 120 dendritic branches [46], we make the assumption that the SN in these synapses is fast, 121 and that the homeostatic change depends on the weight in a multiplicative fashion [44].”
BackgroundMethod
Interactions between homeostatic plasticity and statistical learning: A role for inhibition
Galliano, E., & Keck, T. (2025) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2025.103065 · Cited by 2
“Additionally, the excitatory and inhibitory synapses onto inhibitory neurons themselves can change as a result of changes to sensory input [13–15], which could also alter inhibitory cell activity due to increases or decreases in synaptic drive.”
Striatal Cholinergic Interneurons Control Physical Nicotine Withdrawal via Muscarinic Receptor Signaling
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“…Gois et al. 2005), homeostatically regulated in mature neurons by long-term ( > 24h) changes in activity (Wilson et al. 2005; De Gois et al. 2005; Hartman et al. 2006; Wierenga et al. 2006, Han and Stevens, 2009; Erickson et al. 2006), and they are required to support presynaptic glutamate and…”
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The properties of long-term potentiation at SC-CA1/ TA-CA1 hippocampal synaptic pathways depends upon their input pathway activation patterns
Mosleh, M., Javan, M., & Fathollahi, Y. (2023) · IBRO Neuroscience Reports · doi:10.1016/j.ibneur.2023.03.013 · Cited by 2
Prolonged visual experience accelerates developmental synaptic downscaling via epigenetic regulation and Rab5c mediated AMPA receptor trafficking
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Orchestrated Excitatory and Inhibitory Learning Rules Lead to the Unsupervised Emergence of Self-sustained and Inhibition-stabilized DynamicsPreprint
Soldado-Magraner, S., Laje, R., & Buonomano, D. V. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.12.30.424888 · Cited by 1
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Homeostatic synaptic plasticity of miniature excitatory postsynaptic currents in mouse cortical cultures requires neuronal Rab3aPreprint
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“Another way to increase the presynaptic quantum is to increase levels of the transmitter transporter ( Daniels et al., 2004 ; De Gois et al., 2005 ; Wilson et al., 2005 ; Hartman et al., 2006 ).”
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Authors: Hartman, K. N., Pal, S. K., Burrone, J., & Murthy, V. N.
Affiliations: Harvard University (US)
Corresponding author: Murthy, Venkatesh N
ORCID: Burrone, Juan
Murthy, Venkatesh N
Venue: Nature Neuroscience
Publisher: Springer Science and Business Media LLC
Published: 2006-04-02
Volume: 9
Issue: 5
Pages: 642-649
ISSN: 1097-6256 (ISSN-L)
1546-1726
DOI: 10.1038/nn1677
OpenAlex: W2156087438
Cited by: 221
References: 0
Citations by year: 2026: 3 · 2025: 6 · 2024: 10 · 2023: 9 · 2022: 4 · 2021: 9 · 2020: 11 · 2019: 10 · 2018: 9 · 2017: 10 · 2016: 9 · 2015: 14 · 2014: 12 · 2013: 25 · 2012: 11
FWCI: 5.53
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Nature Neuroscience (publishedVersion)
PubMed (publishedVersion)
Research Portal (King's College London) (submittedVersion)
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: activity-dependent synaptic plasticity, GABAergic synapses, synaptic inhibition, miniature inhibitory postsynaptic currents, hippocampal neurons, synaptic density, presynaptic inhibition, neuronal activity regulation
MeSH terms: Animals, Animals, Newborn, Carrier Proteins, Cells, Cultured, Drug Interactions, Electric Stimulation, Glutamate Decarboxylase, Hippocampus, Isoenzymes, Membrane Potentials, Membrane Proteins, Microtubule-Associated Proteins, Neural Inhibition, Synaptic Transmission, Neurons, Phosphinic Acids, Pyridines, Tetrodotoxin, Transfection, Patch-Clamp Techniques, Potassium Channels, Inwardly Rectifying, Vesicular Glutamate Transport Protein 1, Rats

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Activity-dependent regulation of inhibitory synaptic transmission in hippocampal neurons

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