Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.
Subscribe

Logo for

Science 303 (5664): 1681-1683

Copyright © 2004 by the American Association for the Advancement of Science

Specific GABAA Circuits for Visual Cortical Plasticity

Michela Fagiolini,1 Jean-Marc Fritschy,2 Karin Löw,2 Hanns Möhler,2,3 Uwe Rudolph,2 Takao K. Hensch1*

Abstract: Weak inhibition within visual cortex early in life prevents experience-dependent plasticity. Loss of responsiveness to an eye deprived of vision can be initiated prematurely by enhancing {gamma}-aminobutyric acid (GABA)–mediated transmission with benzodiazepines. Here, we use a mouse "knockin" mutation to {alpha} subunits that renders individual GABA type A (GABAA) receptors insensitive to diazepam to show that a particular inhibitory network controls expression of the critical period. Only {alpha}1-containing circuits were found to drive cortical plasticity, whereas {alpha}2-enriched connections separately regulated neuronal firing. This dissociation carries implications for models of brain development and the safe design of benzodiazepines for use in infants.

1 Laboratory for Neuronal Circuit Development, RIKEN Brain Science Institute, 2-1 Hirosawa, Wako-shi, Saitama, 351-0198 Japan.
2 Institute of Pharmacology and Toxicology, University of Zürich, Winterthurerstrasse 190, Zurich, CH-8057 Switzerland.
3 Department of Chemistry and Applied Biosciences, Swiss Federal Institute of Technology (ETH), Winterthurerstrasse 190, Zürich, CH-8057 Switzerland.

* To whom correspondence should be addressed. E-mail: hensch{at}postman.riken.go.jp

THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Subgroups of parvalbumin-expressing interneurons in layers 2/3 of the visual cortex.
J. Helm, G. Akgul, and L. P. Wollmuth (2013)
J Neurophysiol 109, 1600-1613
   Abstract »    Full Text »    PDF »
Visual experience and subsequent sleep induce sequential plastic changes in putative inhibitory and excitatory cortical neurons.
S. J. Aton, C. Broussard, M. Dumoulin, J. Seibt, A. Watson, T. Coleman, and M. G. Frank (2013)
PNAS 110, 3101-3106
   Abstract »    Full Text »    PDF »
Homeoprotein Signaling in Development, Health, and Disease: A Shaking of Dogmas Offers Challenges and Promises from Bench to Bed.
J. Spatazza, E. Di Lullo, A. Joliot, E. Dupont, K. L. Moya, and A. Prochiantz (2013)
Pharmacol. Rev. 65, 90-104
   Abstract »    Full Text »    PDF »
Development of the GABAergic System from Birth to Adolescence.
W. Kilb (2012)
Neuroscientist 18, 613-630
   Abstract »    Full Text »    PDF »
Developmental Switch in Spike Timing-Dependent Plasticity at Layers 4-2/3 in the Rodent Barrel Cortex.
C. Itami and F. Kimura (2012)
J. Neurosci. 32, 15000-15011
   Abstract »    Full Text »    PDF »
Prenatal exposure to antidepressants and depressed maternal mood alter trajectory of infant speech perception.
W. M. Weikum, T. F. Oberlander, T. K. Hensch, and J. F. Werker (2012)
PNAS 109, 17221-17227
   Abstract »    Full Text »    PDF »
Optimizing Cholinergic Tone Through Lynx Modulators of Nicotinic Receptors: Implications for Plasticity and Nicotine Addiction.
J. M. Miwa, H. A. Lester, and A. Walz (2012)
Physiology 27, 187-199
   Abstract »    Full Text »    PDF »
Impaired Gamma-Band Activity during Perceptual Organization in Adults with Autism Spectrum Disorders: Evidence for Dysfunctional Network Activity in Frontal-Posterior Cortices.
L. Sun, C. Grutzner, S. Bolte, M. Wibral, T. Tozman, S. Schlitt, F. Poustka, W. Singer, C. M. Freitag, and P. J. Uhlhaas (2012)
J. Neurosci. 32, 9563-9573
   Abstract »    Full Text »    PDF »
Influence of a Subtype of Inhibitory Interneuron on Stimulus-Specific Responses in Visual Cortex.
R. Mao, J. Schummers, U. Knoblich, C. J. Lacey, A. Van Wart, I. Cobos, C. Kim, J. R. Huguenard, J. L. R. Rubenstein, and M. Sur (2012)
Cereb Cortex 22, 493-508
   Abstract »    Full Text »    PDF »
Age-dependent effect of hearing loss on cortical inhibitory synapse function.
A. E. Takesian, V. C. Kotak, and D. H. Sanes (2012)
J Neurophysiol 107, 937-947
   Abstract »    Full Text »    PDF »
Inhibition to excitation ratio regulates visual system responses and behavior in vivo.
W. Shen, C. R. McKeown, J. A. Demas, and H. T. Cline (2011)
J Neurophysiol 106, 2285-2302
   Abstract »    Full Text »    PDF »
Distinct maturation profiles of perisomatic and dendritic targeting GABAergic interneurons in the mouse primary visual cortex during the critical period of ocular dominance plasticity.
M. S. Lazarus and Z. J. Huang (2011)
J Neurophysiol 106, 775-787
   Abstract »    Full Text »    PDF »
Positive Feedback Regulation between {gamma}-Aminobutyric Acid Type A (GABAA) Receptor Signaling and Brain-derived Neurotrophic Factor (BDNF) Release in Developing Neurons.
C. Porcher, C. Hatchett, R. E. Longbottom, K. McAinch, T. S. Sihra, S. J. Moss, A. M. Thomson, and J. N. Jovanovic (2011)
J. Biol. Chem. 286, 21667-21677
   Abstract »    Full Text »    PDF »
Fetal Alcohol Spectrum Disorders and Abnormal Neuronal Plasticity.
A. E. Medina (2011)
Neuroscientist 17, 274-287
   Abstract »    PDF »
Natural Restoration of Critical Period Plasticity in the Juvenile and Adult Primary Auditory Cortex.
X. Zhou, R. Panizzutti, E. de Villers-Sidani, C. Madeira, and M. M. Merzenich (2011)
J. Neurosci. 31, 5625-5634
   Abstract »    Full Text »    PDF »
Input-Specific Critical Periods for Experience-Dependent Plasticity in Layer 2/3 Pyramidal Neurons.
J. A. Wen and A. L. Barth (2011)
J. Neurosci. 31, 4456-4465
   Abstract »    Full Text »    PDF »
Laminar-Specific Maturation of GABAergic Transmission and Susceptibility to Visual Deprivation Are Related to Endocannabinoid Sensitivity in Mouse Visual Cortex.
B. Jiang, K. Sohya, A. Sarihi, Y. Yanagawa, and T. Tsumoto (2010)
J. Neurosci. 30, 14261-14272
   Abstract »    Full Text »    PDF »
Animals lacking link protein have attenuated perineuronal nets and persistent plasticity.
D. Carulli, T. Pizzorusso, J. C. F. Kwok, E. Putignano, A. Poli, S. Forostyak, M. R. Andrews, S. S. Deepa, T. T. Glant, and J. W. Fawcett (2010)
Brain 133, 2331-2347
   Abstract »    Full Text »    PDF »
Fast activation of feedforward inhibitory neurons from thalamic input and its relevance to the regulation of spike sequences in the barrel cortex.
F. Kimura, C. Itami, K. Ikezoe, H. Tamura, I. Fujita, Y. Yanagawa, K. Obata, and M. Ohshima (2010)
J. Physiol. 588, 2769-2787
   Abstract »    Full Text »    PDF »
A Critical Role for {alpha}4{beta}{delta} GABAA Receptors in Shaping Learning Deficits at Puberty in Mice.
H. Shen, N. Sabaliauskas, A. Sherpa, A. A. Fenton, A. Stelzer, C. Aoki, and S. S. Smith (2010)
Science 327, 1515-1518
   Abstract »    Full Text »    PDF »
Critical Period for Inhibitory Plasticity in RodentBinocular V1.
A. Maffei, M. E. Lambo, and G. G. Turrigiano (2010)
J. Neurosci. 30, 3304-3309
   Abstract »    Full Text »    PDF »
Cortical Plasticity Induced by Inhibitory Neuron Transplantation.
D. G. Southwell, R. C. Froemke, A. Alvarez-Buylla, M. P. Stryker, and S. P. Gandhi (2010)
Science 327, 1145-1148
   Abstract »    Full Text »    PDF »
Neonatal Cerebral Hypoxia-Ischemia Impairs Plasticity in Rat Visual Cortex.
S. Failor, V. Nguyen, D. P. Darcy, J. Cang, M. F. Wendland, M. P. Stryker, and P. S. McQuillen (2010)
J. Neurosci. 30, 81-92
   Abstract »    Full Text »    PDF »
Long-term sensory deprivation selectively rearranges functional inhibitory circuits in mouse barrel cortex.
P. Li, U. Rudolph, and M. M. Huntsman (2009)
PNAS 106, 12156-12161
   Abstract »    Full Text »    PDF »
Co-regulation of ocular dominance plasticity and NMDA receptor subunit expression in glutamic acid decarboxylase-65 knock-out mice.
P. O. Kanold, Y. A. Kim, T. GrandPre, and C. J. Shatz (2009)
J. Physiol. 587, 2857-2867
   Abstract »    Full Text »    PDF »
Equalization of Ocular Dominance Columns Induced by an Activity-Dependent Learning Rule and the Maturation of Inhibition.
T. Toyoizumi and K. D. Miller (2009)
J. Neurosci. 29, 6514-6525
   Abstract »    Full Text »    PDF »
Feature-Dependent Sensitive Periods in the Development of Complex Sound Representation.
M. N. Insanally, H. Kover, H. Kim, and S. Bao (2009)
J. Neurosci. 29, 5456-5462
   Abstract »    Full Text »    PDF »
Molecular mechanisms of experience-dependent plasticity in visual cortex.
D. Tropea, A. Van Wart, and M. Sur (2009)
Phil Trans R Soc B 364, 341-355
   Abstract »    Full Text »    PDF »
Delayed plasticity of inhibitory neurons in developing visual cortex.
S. P. Gandhi, Y. Yanagawa, and M. P. Stryker (2008)
PNAS 105, 16797-16802
   Abstract »    Full Text »    PDF »
Notch1 Signaling in Pyramidal Neurons Regulates Synaptic Connectivity and Experience-Dependent Modifications of Acuity in the Visual Cortex.
M. Dahlhaus, J. M. Hermans, L. H. Van Woerden, M. H. Saiepour, K. Nakazawa, H. D. Mansvelder, J. A. Heimel, and C. N. Levelt (2008)
J. Neurosci. 28, 10794-10802
   Abstract »    Full Text »    PDF »
Hearing Loss Prevents the Maturation of GABAergic Transmission in the Auditory Cortex.
V. C. Kotak, A. E. Takesian, and D. H. Sanes (2008)
Cereb Cortex 18, 2098-2108
   Abstract »    Full Text »    PDF »
Highly Selective Receptive Fields in Mouse Visual Cortex.
C. M. Niell and M. P. Stryker (2008)
J. Neurosci. 28, 7520-7536
   Abstract »    Full Text »    PDF »
Vision Triggers an Experience-Dependent Sensitive Period at the Retinogeniculate Synapse.
B. M. Hooks and C. Chen (2008)
J. Neurosci. 28, 4807-4817
   Abstract »    Full Text »    PDF »
The transience of interneuron circuit diversity just "sped" up.
E. Krook-Magnuson and M. M. Huntsman (2007)
PNAS 104, 16723-16724
   Full Text »    PDF »
Contrast Sensitivity Is Reduced in Children with Infantile Spasms.
G. Mirabella, S. Morong, J. R. Buncic, O. C. Snead, W. J. Logan, S. K. Weiss, M. Abdolell, and C. A. Westall (2007)
Invest. Ophthalmol. Vis. Sci. 48, 3610-3615
   Abstract »    Full Text »    PDF »
Hippocampal Metaplasticity Induced by Deficiency in the Extracellular Matrix Glycoprotein Tenascin-R.
O. Bukalo, M. Schachner, and A. Dityatev (2007)
J. Neurosci. 27, 6019-6028
   Abstract »    Full Text »    PDF »
GABAergic and Pyramidal Neurons of Deep Cortical Layers Directly Receive and Differently Integrate Callosal Input.
T. Karayannis, I. Huerta-Ocampo, and M. Capogna (2007)
Cereb Cortex 17, 1213-1226
   Abstract »    Full Text »    PDF »
Changes in EMG coherence between long and short thumb abductor muscles during human development.
S. F. Farmer, J. Gibbs, D. M. Halliday, L. M. Harrison, L. M. James, M. J. Mayston, and J. A. Stephens (2007)
J. Physiol. 579, 389-402
   Abstract »    Full Text »    PDF »
Brain-Derived Neurotrophic Factor Regulates the Maturation of Layer 4 Fast-Spiking Cells after the Second Postnatal Week in the Developing Barrel Cortex.
C. Itami, F. Kimura, and S. Nakamura (2007)
J. Neurosci. 27, 2241-2252
   Abstract »    Full Text »    PDF »
Developmental Plasticity of Inhibitory Circuitry.
S. L. Pallas, P. Wenner, C. Gonzalez-Islas, M. Fagiolini, K. A. Razak, G. Kim, D. Sanes, and B. Roerig (2006)
J. Neurosci. 26, 10358-10361
   Full Text »    PDF »
GABAA receptor subtype specific enhancement of inhibition in human motor cortex.
V. Di Lazzaro, F. Pilato, M. Dileone, F. Ranieri, V. Ricci, P. Profice, P. Bria, P. A. Tonali, and U. Ziemann (2006)
J. Physiol. 575, 721-726
   Abstract »    Full Text »    PDF »
Major Effects of Sensory Experiences on the Neocortical Inhibitory Circuits..
Y. Jiao, C. Zhang, Y. Yanagawa, and Q.-Q. Sun (2006)
J. Neurosci. 26, 8691-8701
   Abstract »    Full Text »    PDF »
Specific Subtypes of GABAA Receptors Mediate Phasic and Tonic Forms of Inhibition in Hippocampal Pyramidal Neurons.
G. A. Prenosil, E. M. Schneider Gasser, U. Rudolph, R. Keist, J.-M. Fritschy, and K. E. Vogt (2006)
J Neurophysiol 96, 846-857
   Abstract »    Full Text »    PDF »
Structural and functional recovery from early monocular deprivation in adult rats.
T. Pizzorusso, P. Medini, S. Landi, S. Baldini, N. Berardi, and L. Maffei (2006)
PNAS 103, 8517-8522
   Abstract »    Full Text »    PDF »
Dendritic Branch Typing and Spine Expression Patterns in Cortical Nonpyramidal Cells.
Y. Kawaguchi, F. Karube, and Y. Kubota (2006)
Cereb Cortex 16, 696-711
   Abstract »    Full Text »    PDF »
From Neuroscience to Application in Neuropharmacology: A Generation of Progress in Electrophysiology.
S. Carozzo, S. Fornaro, S. Garbarino, M. Saturno, and W. G. Sannita (2006)
Clinical EEG and Neuroscience 37, 121-134
   Abstract »    Full Text »    PDF »
Gap junctions among dendrites of cortical GABAergic neurons establish a dense and widespread intercolumnar network..
T. Fukuda, T. Kosaka, W. Singer, and R. A. W. Galuske (2006)
J. Neurosci. 26, 3434-3443
   Abstract »    Full Text »    PDF »
Reply from Vincenzo Di Lazzaro, Fabio Pilato, Michele Dileone, Pietro A. Tonali and Ulf Ziemann.
V. Di Lazzaro, F. Pilato, M. Dileone, P. A. Tonali, and U. Ziemann (2005)
J. Physiol. 569, 710
   Full Text »    PDF »
Dissociated effects of diazepam and lorazepam on short-latency afferent inhibition.
V. Di Lazzaro, F. Pilato, M. Dileone, P. A. Tonali, and U. Ziemann (2005)
J. Physiol. 569, 315-323
   Abstract »    Full Text »    PDF »
Patterning and Plasticity of the Cerebral Cortex.
M. Sur and J. L. R. Rubenstein (2005)
Science 310, 805-810
   Abstract »    Full Text »    PDF »
Complementary Roles of Cholecystokinin- and Parvalbumin-Expressing GABAergic Neurons in Hippocampal Network Oscillations.
T. Klausberger, L. F. Marton, J. O'Neill, J. H. J. Huck, Y. Dalezios, P. Fuentealba, W. Y. Suen, E. Papp, T. Kaneko, M. Watanabe, et al. (2005)
J. Neurosci. 25, 9782-9793
   Abstract »    Full Text »    PDF »
Experience-Driven Plasticity of Visual Cortex Limited by Myelin and Nogo Receptor.
A. W. McGee, Y. Yang, Q. S. Fischer, N. W. Daw, and S. M. Strittmatter (2005)
Science 309, 2222-2226
   Abstract »    Full Text »    PDF »
Influence of Lateral Connections on the Structure of Cortical Maps.
M. A. Carreira-Perpinan and G. J. Goodhill (2004)
J Neurophysiol 92, 2947-2959
   Abstract »    Full Text »    PDF »
Requirement for the RII{beta} Isoform of PKA, But Not Calcium-Stimulated Adenylyl Cyclase, in Visual Cortical Plasticity.
Q. S. Fischer, C. J. Beaver, Y. Yang, Y. Rao, K. B. Jakobsdottir, D. R. Storm, G. S. McKnight, and N. W. Daw (2004)
J. Neurosci. 24, 9049-9058
   Abstract »    Full Text »    PDF »
NEUROSCIENCE: Blocking Plasticity in the Visual Cortex.
D. Ferster (2004)
Science 303, 1619-1621
   Abstract »    Full Text »    PDF »
Columnar Architecture Sculpted by GABA Circuits in Developing Cat Visual Cortex.
T. K. Hensch and M. P. Stryker (2004)
Science 303, 1678-1681
   Abstract »    Full Text »    PDF »

To Advertise     Find Products

Science Signaling. ISSN 1937-9145 (online), 1945-0877 (print). Pre-2008: Science's STKE. ISSN 1525-8882