 |
|||||
|
|||||
|
|||||
|
|||||
|
|||||
Previous Article | Next Article
The Journal of Neuroscience, February 15, 2002, 22(4):1328-1337
Activity Deprivation Reduces Miniature IPSC Amplitude by Decreasing the Number of Postsynaptic GABAA Receptors Clustered at Neocortical Synapses
Valerie Kilman, Mark C. W. van Rossum, and Gina G. Turrigiano Department of Biology and Center for Complex Systems, Brandeis University, Waltham, Massachusetts 02454
Maintaining the proper balance between excitation and inhibition is necessary to prevent cortical circuits from either falling silent or generating epileptiform activity. One mechanism through which cortical networks maintain this balance is through the activity-dependent regulation of inhibition, but whether this is achieved primarily through changes in synapse number or synaptic strength is not clear. Previously, we found that 2 d of activity deprivation increased the amplitude of miniature EPSCs (mEPSCs) onto cultured visual cortical pyramidal neurons. Here we find that this same manipulation decreases the amplitude of mIPSCs. This occurs with no change in single-channel conductance but is accompanied by a reduction in the average number of channels open during the mIPSC peak and a reduction in the intensity of staining for GABAA receptors (GABAARs) at postsynaptic sites. In addition, the number of synaptic sites that express detectable levels of GABAARs was decreased by ~50% after activity blockade, although there was no reduction in the total number of presynaptic contacts. These data suggest that activity deprivation reduces cortical inhibition by reducing both the number of GABAARs clustered at synaptic sites and the number of functional inhibitory synapses. Because excitatory and inhibitory synaptic currents are regulated in opposite directions by activity blockade, these data suggest that the balance between excitation and inhibition is dynamically regulated by ongoing activity.
Key words: synaptic plasticity; activity-dependent; mIPSC; GABAA receptor; synapse elimination; nonstationary fluctuation analysis
Copyright © 2002 Society for Neuroscience 0270-6474/02/2241328-10$05.00/0
This article has been cited by other articles:
R. S. Saliba, Z. Gu, Z. Yan, and S. J. Moss
Blocking L-type Voltage-gated Ca2+ Channels with Dihydropyridines Reduces {gamma}-Aminobutyric Acid Type A Receptor Expression and Synaptic Inhibition
J. Biol. Chem., November 20, 2009; 284(47): 32544 - 32550.
[Abstract] [Full Text] [PDF]
J. R. Gibson, K. M. Huber, and T. C. Sudhof
Neuroligin-2 Deletion Selectively Decreases Inhibitory Synaptic Transmission Originating from Fast-Spiking but Not from Somatostatin-Positive Interneurons
J. Neurosci., November 4, 2009; 29(44): 13883 - 13897.
[Abstract] [Full Text] [PDF]
S.-y. Zhang, M. Xu, Q.-l. Miao, M.-m. Poo, and X.-h. Zhang
Endocannabinoid-Dependent Homeostatic Regulation of Inhibitory Synapses by Miniature Excitatory Synaptic Activities
J. Neurosci., October 21, 2009; 29(42): 13222 - 13231.
[Abstract] [Full Text] [PDF]
R. Schaette and R. Kempter
Predicting Tinnitus Pitch From Patients' Audiograms With a Computational Model for the Development of Neuronal Hyperactivity
J Neurophysiol, June 1, 2009; 101(6): 3042 - 3052.
[Abstract] [Full Text] [PDF]
D. Tropea, A. Van Wart, and M. Sur
Molecular mechanisms of experience-dependent plasticity in visual cortex
Phil Trans R Soc B, February 12, 2009; 364(1515): 341 - 355.
[Abstract] [Full Text] [PDF]
E. C. Sarro, V. C. Kotak, D. H. Sanes, and C. Aoki
Hearing Loss Alters the Subcellular Distribution of Presynaptic GAD and Postsynaptic GABAA Receptors in the Auditory Cortex
Cereb Cortex, December 1, 2008; 18(12): 2855 - 2867.
[Abstract] [Full Text] [PDF]
N. Kuczewski, A. Langlois, H. Fiorentino, S. Bonnet, T. Marissal, D. Diabira, N. Ferrand, C. Porcher, and J.-L. Gaiarsa
Spontaneous glutamatergic activity induces a BDNF-dependent potentiation of GABAergic synapses in the newborn rat hippocampus
J. Physiol., November 1, 2008; 586(21): 5119 - 5128.
[Abstract] [Full Text] [PDF]
A. F. Bartley, Z. J. Huang, K. M. Huber, and J. R. Gibson
Differential Activity-Dependent, Homeostatic Plasticity of Two Neocortical Inhibitory Circuits
J Neurophysiol, October 1, 2008; 100(4): 1983 - 1994.
[Abstract] [Full Text] [PDF]
V. C. Kotak, A. E. Takesian, and D. H. Sanes
Hearing Loss Prevents the Maturation of GABAergic Transmission in the Auditory Cortex
Cereb Cortex, September 1, 2008; 18(9): 2098 - 2108.
[Abstract] [Full Text] [PDF]
J. C. Wilhelm and P. Wenner
GABAA transmission is a critical step in the process of triggering homeostatic increases in quantal amplitude
PNAS, August 12, 2008; 105(32): 11412 - 11417.
[Abstract] [Full Text] [PDF]
S. Taverna, E. Ilijic, and D. J. Surmeier
Recurrent Collateral Connections of Striatal Medium Spiny Neurons Are Disrupted in Models of Parkinson's Disease
J. Neurosci., May 21, 2008; 28(21): 5504 - 5512.
[Abstract] [Full Text] [PDF]
P. J. Sjostrom, E. A. Rancz, A. Roth, and M. Hausser
Dendritic Excitability and Synaptic Plasticity
Physiol Rev, April 1, 2008; 88(2): 769 - 840.
[Abstract] [Full Text] [PDF]
F. Frohlich, M. Bazhenov, and T. J. Sejnowski
Pathological Effect of Homeostatic Synaptic Scaling on Network Dynamics in Diseases of the Cortex
J. Neurosci., February 13, 2008; 28(7): 1709 - 1720.
[Abstract] [Full Text] [PDF]
Q. Hou, D. Zhang, L. Jarzylo, R. L. Huganir, and H.-Y. Man
Homeostatic regulation of AMPA receptor expression at single hippocampal synapses
PNAS, January 15, 2008; 105(2): 775 - 780.
[Abstract] [Full Text] [PDF]
E. D. Nelson, E. T. Kavalali, and L. M. Monteggia
Activity-Dependent Suppression of Miniature Neurotransmission through the Regulation of DNA Methylation
J. Neurosci., January 9, 2008; 28(2): 395 - 406.
[Abstract] [Full Text] [PDF]
R. S. Saliba, G. Michels, T. C. Jacob, M. N. Pangalos, and S. J. Moss
Activity-Dependent Ubiquitination of GABAA Receptors Regulates Their Accumulation at Synaptic Sites
J. Neurosci., November 28, 2007; 27(48): 13341 - 13351.
[Abstract] [Full Text] [PDF]
K. C. Riegle and R. L. Meyer
Rapid Homeostatic Plasticity in the Intact Adult Visual System
J. Neurosci., September 26, 2007; 27(39): 10556 - 10567.
[Abstract] [Full Text] [PDF]
A. L. Howard, A. Neu, R. J. Morgan, J. C. Echegoyen, and I. Soltesz
Opposing Modifications in Intrinsic Currents and Synaptic Inputs in Post-Traumatic Mossy Cells: Evidence for Single-Cell Homeostasis in a Hyperexcitable Network
J Neurophysiol, March 1, 2007; 97(3): 2394 - 2409.
[Abstract] [Full Text] [PDF]
S. L. Pallas, P. Wenner, C. Gonzalez-Islas, M. Fagiolini, K. A. Razak, G. Kim, D. Sanes, and B. Roerig
Developmental Plasticity of Inhibitory Circuitry
J. Neurosci., October 11, 2006; 26(41): 10358 - 10361.
[Full Text] [PDF]
S. J. Liu and P. Lachamp
The Activation of Excitatory Glutamate Receptors Evokes a Long-Lasting Increase in the Release of GABA from Cerebellar Stellate Cells
J. Neurosci., September 6, 2006; 26(36): 9332 - 9339.
[Abstract] [Full Text] [PDF]
I. Rabinowitch and I. Segev
The Interplay Between Homeostatic Synaptic Plasticity and Functional Dendritic Compartments
J Neurophysiol, July 1, 2006; 96(1): 276 - 283.
[Abstract] [Full Text] [PDF]
J. R. Gibson, A. F. Bartley, and K. M. Huber
Role for the Subthreshold Currents ILeak and IH in the Homeostatic Control of Excitability in Neocortical Somatostatin-Positive Inhibitory Neurons
J Neurophysiol, July 1, 2006; 96(1): 420 - 432.
[Abstract] [Full Text] [PDF]
B. A. Graham, P. R. Schofield, P. Sah, T. W. Margrie, and R. J. Callister
Distinct physiological mechanisms underlie altered glycinergic synaptic transmission in the murine mutants spastic, spasmodic, and oscillator.
J. Neurosci., May 3, 2006; 26(18): 4880 - 4890.
[Abstract] [Full Text] [PDF]
B. Walmsley, A. Berntson, R. N. Leao, and R. E. W. Fyffe
Activity-dependent regulation of synaptic strength and neuronal excitability in central auditory pathways
J. Physiol., April 15, 2006; 572(2): 313 - 321.
[Abstract] [Full Text] [PDF]
D. A. Nita, Y. Cisse, I. Timofeev, and M. Steriade
Increased Propensity to Seizures After Chronic Cortical Deafferentation In Vivo
J Neurophysiol, February 1, 2006; 95(2): 902 - 913.
[Abstract] [Full Text] [PDF]
M. M. Carrasco, K. A. Razak, and S. L. Pallas
Visual Experience Is Necessary for Maintenance But Not Development of Receptive Fields in Superior Colliculus
J Neurophysiol, September 1, 2005; 94(3): 1962 - 1970.
[Abstract] [Full Text] [PDF]
S. De Gois, M. K.-H. Schafer, N. Defamie, C. Chen, A. Ricci, E. Weihe, H. Varoqui, and J. D. Erickson
Homeostatic Scaling of Vesicular Glutamate and GABA Transporter Expression in Rat Neocortical Circuits
J. Neurosci., August 3, 2005; 25(31): 7121 - 7133.
[Abstract] [Full Text] [PDF]
J. C. Echegoyen and I. Soltesz
Mini-I on Epilepsy. Focus on "Changes in mIPSCs and sIPSCs After Kainate Treatment: Evidence for Loss of Inhibitory Input to Dentate Granule Cells and Possible Compensatory Responses"
J Neurophysiol, August 1, 2005; 94(2): 903 - 904.
[Full Text] [PDF]
A. R. Houweling, M. Bazhenov, I. Timofeev, M. Steriade, and T. J. Sejnowski
Homeostatic Synaptic Plasticity Can Explain Post-traumatic Epileptogenesis in Chronically Isolated Neocortex
Cereb Cortex, June 1, 2005; 15(6): 834 - 845.
[Abstract] [Full Text] [PDF]
B. Fierro, F. Brighina, G. Vitello, A. Piazza, S. Scalia, G. Giglia, O. Daniele, and A. Pascual-Leone
Modulatory effects of low- and high-frequency repetitive transcranial magnetic stimulation on visual cortex of healthy subjects undergoing light deprivation
J. Physiol., June 1, 2005; 565(2): 659 - 665.
[Abstract] [Full Text] [PDF]
V. C. Kotak, S. Fujisawa, F. A. Lee, O. Karthikeyan, C. Aoki, and D. H. Sanes
Hearing Loss Raises Excitability in the Auditory Cortex
J. Neurosci., April 13, 2005; 25(15): 3908 - 3918.
[Abstract] [Full Text] [PDF]
D. Stellwagen, E. C. Beattie, J. Y. Seo, and R. C. Malenka
Differential Regulation of AMPA Receptor and GABA Receptor Trafficking by Tumor Necrosis Factor-{alpha}
J. Neurosci., March 23, 2005; 25(12): 3219 - 3228.
[Abstract] [Full Text] [PDF]
C. J. Wierenga, K. Ibata, and G. G. Turrigiano
Postsynaptic Expression of Homeostatic Plasticity at Neocortical Synapses
J. Neurosci., March 16, 2005; 25(11): 2895 - 2905.
[Abstract] [Full Text] [PDF]
D. Gonzalez-Forero, A. M. Pastor, E. J. Geiman, B. Benitez-Temino, and F. J. Alvarez
Regulation of Gephyrin Cluster Size and Inhibitory Synaptic Currents on Renshaw Cells by Motor Axon Excitatory Inputs
J. Neurosci., January 12, 2005; 25(2): 417 - 429.
[Abstract] [Full Text] [PDF]
I. Mody
Aspects of the homeostaic plasticity of GABAA receptor-mediated inhibition
J. Physiol., January 1, 2005; 562(1): 37 - 46.
[Abstract] [Full Text] [PDF]
G. Ohtsuki, S.-y. Kawaguchi, M. Mishina, and T. Hirano
Enhanced Inhibitory Synaptic Transmission in the Cerebellar Molecular Layer of the GluR{delta}2 Knock-Out Mouse
J. Neurosci., December 1, 2004; 24(48): 10900 - 10907.
[Abstract] [Full Text] [PDF]
T. Koos, J. M. Tepper, and C. J. Wilson
Comparison of IPSCs Evoked by Spiny and Fast-Spiking Neurons in the Neostriatum
J. Neurosci., September 8, 2004; 24(36): 7916 - 7922.
[Abstract] [Full Text] [PDF]
I. Colin-Le Brun, N. Ferrand, O. Caillard, P. Tosetti, Y. Ben-Ari, and J.-L. Gaiarsa
Spontaneous synaptic activity is required for the formation of functional GABAergic synapses in the developing rat hippocampus
J. Physiol., August 15, 2004; 559(1): 129 - 139.
[Abstract] [Full Text] [PDF]
S. B. Elmariah, M. A. Crumling, T. D. Parsons, and R. J. Balice-Gordon
Postsynaptic TrkB-Mediated Signaling Modulates Excitatory and Inhibitory Neurotransmitter Receptor Clustering at Hippocampal Synapses
J. Neurosci., March 10, 2004; 24(10): 2380 - 2393.
[Abstract] [Full Text] [PDF]
C. Linnemann, F. Sultan, C. M. Pedroarena, C. Schwarz, and P. Thier
Lurcher Mice Exhibit Potentiation of GABAA-Receptor-Mediated Conductance in Cerebellar Nuclei Neurons in Close Temporal Relationship to Purkinje Cell Death
J Neurophysiol, February 1, 2004; 91(2): 1102 - 1107.
[Abstract] [Full Text] [PDF]
Y. Mizoguchi, T. Kanematsu, M. Hirata, and J. Nabekura
A Rapid Increase in the Total Number of Cell Surface Functional GABAA Receptors Induced by Brain-derived Neurotrophic Factor in Rat Visual Cortex
J. Biol. Chem., November 7, 2003; 278(45): 44097 - 44102.
[Abstract] [Full Text] [PDF]
B A Graham, P R Schofield, P Sah, and R J Callister
Altered inhibitory synaptic transmission in superficial dorsal horn neurones in spastic and oscillator mice
J. Physiol., September 15, 2003; 551(3): 905 - 916.
[Abstract] [Full Text] [PDF]
E. H. Chang, V. C. Kotak, and D. H. Sanes
Long-Term Depression of Synaptic Inhibition Is Expressed Postsynaptically in the Developing Auditory System
J Neurophysiol, September 1, 2003; 90(3): 1479 - 1488.
[Abstract] [Full Text] [PDF]
Y. Iwai, M. Fagiolini, K. Obata, and T. K. Hensch
Rapid Critical Period Induction by Tonic Inhibition in Visual Cortex
J. Neurosci., July 30, 2003; 23(17): 6695 - 6702.
[Abstract] [Full Text] [PDF]
A. De Simoni, C. B Griesinger, and F. A Edwards
Development of rat CA1 neurones in acute Versus organotypic slices: role of experience in synaptic morphology and activity
J. Physiol., July 1, 2003; 550(1): 135 - 147.
[Abstract] [Full Text] [PDF]
E. M. Petrini, P. Zacchi, A. Barberis, J. W. Mozrzymas, and E. Cherubini
Declusterization of GABAA Receptors Affects the Kinetic Properties of GABAergic Currents in Cultured Hippocampal Neurons
J. Biol. Chem., April 25, 2003; 278(18): 16271 - 16279.
[Abstract] [Full Text] [PDF]
C. Gally and J.-L. Bessereau
GABA Is Dispensable for the Formation of Junctional GABA Receptor Clusters in Caenorhabditis elegans
J. Neurosci., April 1, 2003; 23(7): 2591 - 2599.
[Abstract] [Full Text] [PDF]
C. L. Brumwell, J. L. Johnson, and M. H. Jacob
Extrasynaptic alpha 7-Nicotinic Acetylcholine Receptor Expression in Developing Neurons Is Regulated by Inputs, Targets, and Activity
J. Neurosci., September 15, 2002; 22(18): 8101 - 8109.
[Abstract] [Full Text] [PDF]
|
|
|
|
 |
|