 |
||||
|
||||
|
||||
|
||||
Previous Article | Next Article
Volume 17, Number 12, Issue of June 15, 1997 pp. 4527-4535
Copyright ©1997 Society for NeuroscienceBrain-Derived Neurotrophic Factor Mediates the Activity-Dependent Regulation of Inhibition in Neocortical Cultures
Received Jan. 17, 1997; revised March 26, 1997; accepted March 28, 1997.
Lana C. Rutherford, Andrew DeWan, Holly M. Lauer, and Gina G. Turrigiano Department of Biology and Volen Center for Complex Systems, Brandeis University, Waltham, Massachusetts 02254
The excitability of cortical circuits is modulated by interneurons that release the inhibitory neurotransmitter GABA. In primate and rodent visual cortex, activity deprivation leads to a decrease in the expression of GABA. This suggests that activity is able to adjust the strength of cortical inhibition, but this has not been demonstrated directly. In addition, the nature of the signal linking activity to GABA expression has not been determined. Activity is known to regulate the expression of the neurotrophin brain-derived neurotrophic factor (BDNF), and BDNF has been shown to influence the phenotype of GABAergic interneurons. We use a culture system from postnatal rat visual cortex to test the hypothesis that activity is regulating the strength of cortical inhibition through the regulation of BDNF. Cultures were double-labeled against GABA and the neuronal marker MAP2, and the percentage of neurons that were GABA-positive was determined. Blocking spontaneous activity in these cultures reversibly decreased the number of GABA-positive neurons without affecting neuronal survival. Voltage-clamp analysis of inhibitory currents demonstrated that activity blockade also decreased GABA-mediated inhibition onto pyramidal neurons and raised pyramidal neuron firing rates. All of these effects were prevented by incubation with BDNF during activity blockade, but not by neurotrophin 3 or nerve growth factor. Additionally, blockade of neurotrophin signaling mimicked the effects of activity blockade on GABA expression. These data suggest that activity regulates cortical inhibition through a BDNF-dependent mechanism and that this neurotrophin plays an important role in the control of cortical excitability.
Key words: BDNF; visual cortex; dissociated culture; activity-dependent; inhibition; GABA; interneurons
This article has been cited by other articles:
A. Patrizi, B. Scelfo, L. Viltono, F. Briatore, M. Fukaya, M. Watanabe, P. Strata, F. Varoqueaux, N. Brose, J.-M. Fritschy, et al.
Synapse formation and clustering of neuroligin-2 in the absence of GABAA receptors
PNAS, September 2, 2008; 105(35): 13151 - 13156.
[Abstract] [Full Text] [PDF]
N. Kuczewski, C. Porcher, N. Ferrand, H. Fiorentino, C. Pellegrino, R. Kolarow, V. Lessmann, I. Medina, and J.-L. Gaiarsa
Backpropagating Action Potentials Trigger Dendritic Release of BDNF during Spontaneous Network Activity
J. Neurosci., July 2, 2008; 28(27): 7013 - 7023.
[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]
I. Abidin, U. T. Eysel, V. Lessmann, and T. Mittmann
Impaired GABAergic inhibition in the visual cortex of brain-derived neurotrophic factor heterozygous knockout mice
J. Physiol., April 1, 2008; 586(7): 1885 - 1901.
[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]
R. Kolarow, T. Brigadski, and V. Lessmann
Postsynaptic Secretion of BDNF and NT-3 from Hippocampal Neurons Depends on Calcium Calmodulin Kinase II Signaling and Proceeds via Delayed Fusion Pore Opening
J. Neurosci., September 26, 2007; 27(39): 10350 - 10364.
[Abstract] [Full Text] [PDF]
K. Kohara, H. Yasuda, Y. Huang, N. Adachi, K. Sohya, and T. Tsumoto
A Local Reduction in Cortical GABAergic Synapses after a Loss of Endogenous Brain-Derived Neurotrophic Factor, as Revealed by Single-Cell Gene Knock-Out Method
J. Neurosci., July 4, 2007; 27(27): 7234 - 7244.
[Abstract] [Full Text] [PDF]
H. A. Johnson and D. V. Buonomano
Development and Plasticity of Spontaneous Activity and Up States in Cortical Organotypic Slices
J. Neurosci., May 30, 2007; 27(22): 5915 - 5925.
[Abstract] [Full Text] [PDF]
R. A. Gomes, C. Hampton, F. El-Sabeawy, S. L. Sabo, and A. K. McAllister
The Dynamic Distribution of TrkB Receptors before, during, and after Synapse Formation between Cortical Neurons.
J. Neurosci., November 1, 2006; 26(44): 11487 - 11500.
[Abstract] [Full Text] [PDF]
C. J. Wierenga, M. F. Walsh, and G. G. Turrigiano
Temporal Regulation of the Expression Locus of Homeostatic Plasticity
J Neurophysiol, October 1, 2006; 96(4): 2127 - 2133.
[Abstract] [Full Text] [PDF]
S. B. Bausch, S. He, Y. Petrova, X.-M. Wang, and J. O. McNamara
Plasticity of Both Excitatory and Inhibitory Synapses Is Associated With Seizures Induced by Removal of Chronic Blockade of Activity in Cultured Hippocampus
J Neurophysiol, October 1, 2006; 96(4): 2151 - 2167.
[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]
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]
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]
S. B. Elmariah, E. J. Oh, E. G. Hughes, and R. J. Balice-Gordon
Astrocytes Regulate Inhibitory Synapse Formation via Trk-Mediated Modulation of Postsynaptic GABAA Receptors
J. Neurosci., April 6, 2005; 25(14): 3638 - 3650.
[Abstract] [Full Text] [PDF]
P. Baldelli, J.-M. Hernandez-Guijo, V. Carabelli, and E. Carbone
Brain-Derived Neurotrophic Factor Enhances GABA Release Probability and Nonuniform Distribution of N- and P/Q-Type Channels on Release Sites of Hippocampal Inhibitory Synapses
J. Neurosci., March 30, 2005; 25(13): 3358 - 3368.
[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]
S. Ohba, T. Ikeda, Y. Ikegaya, N. Nishiyama, N. Matsuki, and M. K. Yamada
BDNF Locally Potentiates GABAergic Presynaptic Machineries: Target-selective Circuit Inhibition
Cereb Cortex, March 1, 2005; 15(3): 291 - 298.
[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. 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]
K. Kohara, A. Kitamura, N. Adachi, M. Nishida, C. Itami, S. Nakamura, and T. Tsumoto
Inhibitory But Not Excitatory Cortical Neurons Require Presynaptic Brain-Derived Neurotrophic Factor for Dendritic Development, as Revealed by Chimera Cell Culture
J. Neurosci., July 9, 2003; 23(14): 6123 - 6131.
[Abstract] [Full Text] [PDF]
X. Jin, H. Hu, P. H. Mathers, and A. Agmon
Brain-Derived Neurotrophic Factor Mediates Activity-Dependent Dendritic Growth in Nonpyramidal Neocortical Interneurons in Developing Organotypic Cultures
J. Neurosci., July 2, 2003; 23(13): 5662 - 5673.
[Abstract] [Full Text] [PDF]
M. Neal, J. Cunningham, I. Lever, S. Pezet, and M. Malcangio
Mechanism by which Brain-Derived Neurotrophic Factor Increases Dopamine Release from the Rabbit Retina
Invest. Ophthalmol. Vis. Sci., February 1, 2003; 44(2): 791 - 798.
[Abstract] [Full Text] [PDF]
H. Nadeau and H. A. Lester
NRSF Causes cAMP-Sensitive Suppression of Sodium Current in Cultured Hippocampal Neurons
J Neurophysiol, July 1, 2002; 88(1): 409 - 421.
[Abstract] [Full Text] [PDF]
V. Kilman, M. C. W. van Rossum, and G. G. Turrigiano
Activity Deprivation Reduces Miniature IPSC Amplitude by Decreasing the Number of Postsynaptic GABAA Receptors Clustered at Neocortical Synapses
J. Neurosci., February 15, 2002; 22(4): 1328 - 1337.
[Abstract] [Full Text] [PDF]
O. Rahimi and S. L. Juliano
Transplants of NGF-Secreting Fibroblasts Restore Stimulus-Evoked Activity in Barrel Cortex of Basal-Forebrain-Lesioned Rats
J Neurophysiol, October 1, 2001; 86(4): 2081 - 2096.
[Abstract] [Full Text] [PDF]
J. Shi, S. M. Aamodt, M. Townsend, and M. Constantine-Paton
Developmental Depression of Glutamate Neurotransmission by Chronic Low-Level Activation of NMDA Receptors
J. Neurosci., August 15, 2001; 21(16): 6233 - 6244.
[Abstract] [Full Text] [PDF]
G. S. Pollock, E. Vernon, M. E. Forbes, Q. Yan, Y.-T. Ma, T. Hsieh, R. Robichon, D. O. Frost, and J. E. Johnson
Effects of Early Visual Experience and Diurnal Rhythms on BDNF mRNA and Protein Levels in the Visual System, Hippocampus, and Cerebellum
J. Neurosci., June 1, 2001; 21(11): 3923 - 3931.
[Abstract] [Full Text] [PDF]
D. C. Gillespie, M. C. Crair, and M. P. Stryker
Neurotrophin-4/5 Alters Responses and Blocks the Effect of Monocular Deprivation in Cat Visual Cortex during the Critical Period
J. Neurosci., December 15, 2000; 20(24): 9174 - 9186.
[Abstract] [Full Text] [PDF]
S. Marty, R. Wehrle, and C. Sotelo
Neuronal Activity and Brain-Derived Neurotrophic Factor Regulate the Density of Inhibitory Synapses in Organotypic Slice Cultures of Postnatal Hippocampus
J. Neurosci., November 1, 2000; 20(21): 8087 - 8095.
[Abstract] [Full Text] [PDF]
T. W. Troyer and A. J. Doupe
An Associational Model of Birdsong Sensorimotor Learning I. Efference Copy and the Learning of Song Syllables
J Neurophysiol, September 1, 2000; 84(3): 1204 - 1223.
[Abstract] [Full Text] [PDF]
F. J. Seil and R. Drake-Baumann
TrkB Receptor Ligands Promote Activity-Dependent Inhibitory Synaptogenesis
J. Neurosci., July 15, 2000; 20(14): 5367 - 5373.
[Abstract] [Full Text] [PDF]
M. M. Bolton, A. J. Pittman, and D. C. Lo
Brain-Derived Neurotrophic Factor Differentially Regulates Excitatory and Inhibitory Synaptic Transmission in Hippocampal Cultures
J. Neurosci., May 1, 2000; 20(9): 3221 - 3232.
[Abstract] [Full Text] [PDF]
C. Lodovichi, N. Berardi, T. Pizzorusso, and L. Maffei
Effects of Neurotrophins on Cortical Plasticity: Same or Different?
J. Neurosci., March 15, 2000; 20(6): 2155 - 2165.
[Abstract] [Full Text] [PDF]
S. M. Aamodt, J. Shi, M. T. Colonnese, W. Veras, and M. Constantine-Paton
Chronic NMDA Exposure Accelerates Development of GABAergic Inhibition in the Superior Colliculus
J Neurophysiol, March 1, 2000; 83(3): 1580 - 1591.
[Abstract] [Full Text] [PDF]
A. Balkowiec, D. L. Kunze, and D. M. Katz
Brain-Derived Neurotrophic Factor Acutely Inhibits AMPA-Mediated Currents in Developing Sensory Relay Neurons
J. Neurosci., March 1, 2000; 20(5): 1904 - 1911.
[Abstract] [Full Text] [PDF]
A. Nitta, M. Ito, H. Fukumitsu, M. Ohmiya, H. Ito, A. Sometani, H. Nomoto, Y. Furukawa, and S. Furukawa
4-Methylcatechol Increases Brain-Derived Neurotrophic Factor Content and mRNA Expression in Cultured Brain Cells and in Rat Brain In Vivo
J. Pharmacol. Exp. Ther., December 1, 1999; 291(3): 1276 - 1283.
[Abstract] [Full Text]
A. K. McAllister
Subplate neurons: A missing link among neurotrophins, activity, and ocular dominance plasticity?
PNAS, November 23, 1999; 96(24): 13600 - 13602.
[Full Text] [PDF]
E. S. Lein, E. M. Finney, P. S. McQuillen, and C. J. Shatz
Subplate neuron ablation alters neurotrophin expression and ocular dominance column formation
PNAS, November 9, 1999; 96(23): 13491 - 13495.
[Abstract] [Full Text] [PDF]
J. M. Kittelberger and R. Mooney
Lesions of an Avian Forebrain Nucleus That Disrupt Song Development Alter Synaptic Connectivity and Transmission in the Vocal Premotor Pathway
J. Neurosci., November 1, 1999; 19(21): 9385 - 9398.
[Abstract] [Full Text] [PDF]
D. Kryl, T. Yacoubian, A. Haapasalo, E. Castren, D. Lo, and P. A. Barker
Subcellular Localization of Full-Length and Truncated Trk Receptor Isoforms in Polarized Neurons and Epithelial Cells
J. Neurosci., July 15, 1999; 19(14): 5823 - 5833.
[Abstract] [Full Text] [PDF]
R. A. Crozier, I. B. Black, and M. R. Plummer
Blockade of NR2B-Containing NMDA Receptors Prevents BDNF Enhancement of Glutamatergic Transmission in Hippocampal Neurons
Learn. Mem., May 1, 1999; 6(3): 257 - 266.
[Abstract] [Full Text]
S. Bao, L. Chen, X. Qiao, and R. F. Thompson
Transgenic Brain-Derived Neurotrophic Factor Modulates a Developing Cerebellar Inhibitory Synapse
Learn. Mem., May 1, 1999; 6(3): 276 - 283.
[Abstract] [Full Text]
N. S. Desai, L. C. Rutherford, and G. G. Turrigiano
BDNF Regulates the Intrinsic Excitability of Cortical Neurons
Learn. Mem., May 1, 1999; 6(3): 284 - 291.
[Abstract] [Full Text]
T. Kushikata, J. Fang, and J. M. Krueger
Brain-derived neurotrophic factor enhances spontaneous sleep in rats and rabbits
Am J Physiol Regulatory Integrative Comp Physiol, May 1, 1999; 276(5): R1334 - R1338.
[Abstract] [Full Text] [PDF]
Y.-X. Li, Y. Zhang, H. A. Lester, E. M. Schuman, and N. Davidson
Enhancement of Neurotransmitter Release Induced by Brain-Derived Neurotrophic Factor in Cultured Hippocampal Neurons
J. Neurosci., December 15, 1998; 18(24): 10231 - 10240.
[Abstract] [Full Text] [PDF]
M. Kokaia, F. Asztely, K. Olofsdotter, C. B. Sindreu, D. M. Kullmann, and O. Lindvall
Endogenous Neurotrophin-3 Regulates Short-Term Plasticity at Lateral Perforant Path-Granule Cell Synapses
J. Neurosci., November 1, 1998; 18(21): 8730 - 8739.
[Abstract] [Full Text] [PDF]
D. D. Murphy, N. B. Cole, and M. Segal
Brain-derived neurotrophic factor mediates estradiol-induced dendritic spine formation in hippocampal neurons
PNAS, September 15, 1998; 95(19): 11412 - 11417.
[Abstract] [Full Text] [PDF]
J. L. Dantzker and E. M. Callaway
The Development of Local, Layer-Specific Visual Cortical Axons in the Absence of Extrinsic Influences and Intrinsic Activity
J. Neurosci., June 1, 1998; 18(11): 4145 - 4154.
[Abstract] [Full Text] [PDF]
S. T. Lockhart, G. G. Turrigiano, and S. J. Birren
Nerve Growth Factor Modulates Synaptic Transmission between Sympathetic Neurons and Cardiac Myocytes
J. Neurosci., December 15, 1997; 17(24): 9573 - 9582.
[Abstract] [Full Text] [PDF]
J. L. Hanover, Z. J. Huang, S. Tonegawa, and M. P. Stryker
Brain-Derived Neurotrophic Factor Overexpression Induces Precocious Critical Period in Mouse Visual Cortex
J. Neurosci., November 15, 1999; 19(22): RC40 - RC40.
[Abstract] [Full Text] [PDF]
K. R. Leslie, S. B. Nelson, and G. G. Turrigiano
Postsynaptic Depolarization Scales Quantal Amplitude in Cortical Pyramidal Neurons
J. Neurosci., October 1, 2001; 21(19): RC170 - RC170.
[Abstract] [Full Text] [PDF]
|
|
|
|
 |
|