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Identified Sources and Targets of Slow Inhibition in the Neocortex
Gábor Tamás,*Andrea Lrincz, Anna Simon,János Szabadics
There are two types of inhibitory postsynaptic potentials in the
cerebral cortex. Fast inhibition is mediated by ionotropic-aminobutyric acid type A (GABAA) receptors, and slow
inhibitionis due to metabotropic GABAB receptors. Several
neuron classeselicit inhibitory postsynaptic potentials through
GABAA receptors,but possible distinct sources of slow
inhibition remain unknown.We identified a class of GABAergic
interneurons, the neurogliaformcells, that, in contrast to other
GABA-releasing cells, elicitedcombined GABAA and
GABAB receptor-mediated responses with singleaction
potentials and that predominantly targeted the dendriticspines of
pyramidal neurons. Slow inhibition evoked by a distinctinterneuron in
spatially restricted postsynaptic compartmentscould locally and
selectively modulate cortical excitability.
Department of Comparative Physiology, University of Szeged,
Közép fasor 52, Szeged H-6726, Hungary.
*
To whom correspondence should be addressed. E-mail:
gtamas{at}bio.u-szeged.hu
Interneuron Diversity in Layers 2-3 of Monkey Prefrontal Cortex.
A. V. Zaitsev, N. V. Povysheva, G. Gonzalez-Burgos, D. Rotaru, K. N. Fish, L. S. Krimer, and D. A. Lewis (2009)
Cereb Cortex
19, 1597-1615
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Distinct Roles of GABAA and GABAB Receptors in Balancing and Terminating Persistent Cortical Activity.
L2/3 Interneuron Groups Defined by Multiparameter Analysis of Axonal Projection, Dendritic Geometry, and Electrical Excitability.
M. Helmstaedter, B. Sakmann, and D. Feldmeyer (2009)
Cereb Cortex
19, 951-962
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Neuronal Correlates of Local, Lateral, and Translaminar Inhibition with Reference to Cortical Columns.
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Cereb Cortex
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J. Neurosci.
29, 3642-3659
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G. Gonzalez-Burgos, D. C. Rotaru, A. V. Zaitsev, N. V. Povysheva, and D. A. Lewis (2009)
J Neurophysiol
101, 533-547
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Laminar Specificity of Functional Input to Distinct Types of Inhibitory Cortical Neurons.
GABAB Receptor Modulation of Feedforward Inhibition through Hippocampal Neurogliaform Cells.
C. J. Price, R. Scott, D. A. Rusakov, and M. Capogna (2008)
J. Neurosci.
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M. Uematsu, Y. Hirai, F. Karube, S. Ebihara, M. Kato, K. Abe, K. Obata, S. Yoshida, M. Hirabayashi, Y. Yanagawa, et al. (2008)
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The transience of interneuron circuit diversity just "sped" up.
E. Krook-Magnuson and M. M. Huntsman (2007)
PNAS
104, 16723-16724
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Different transmitter transients underlie presynaptic cell type specificity of GABAA,slow and GABAA,fast.
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S. Kroner, L. S. Krimer, D. A. Lewis, and G. Barrionuevo (2007)
Cereb Cortex
17, 1020-1032
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Electrophysiological Differences Between Neurogliaform Cells From Monkey and Rat Prefrontal Cortex.
N. V. Povysheva, A. V. Zaitsev, S. Kroner, O. A. Krimer, D. C. Rotaru, G. Gonzalez-Burgos, D. A. Lewis, and L. S. Krimer (2007)
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Neocortical Inhibitory Terminals Innervate Dendritic Spines Targeted by Thalamocortical Afferents.
Y. Kubota, S. Hatada, S. Kondo, F. Karube, and Y. Kawaguchi (2007)
J. Neurosci.
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Correlation Between Axonal Morphologies and Synaptic Input Kinetics of Interneurons from Mouse Visual Cortex.
D. Dumitriu, R. Cossart, J. Huang, and R. Yuste (2007)
Cereb Cortex
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The cellular basis for parallel neural transmission of a high-frequency stimulus and its low-frequency envelope.
J. W. Middleton, A. Longtin, J. Benda, and L. Maler (2006)
PNAS
103, 14596-14601
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Realistic Modeling of Entorhinal Cortex Field Potentials and Interpretation of Epileptic Activity in the Guinea Pig Isolated Brain Preparation.
E. Labyt, L. Uva, M. de Curtis, and F. Wendling (2006)
J Neurophysiol
96, 363-377
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Cluster Analysis-Based Physiological Classification and Morphological Properties of Inhibitory Neurons in Layers 2-3 of Monkey Dorsolateral Prefrontal Cortex.
L. S. Krimer, A. V. Zaitsev, G. Czanner, S. Kroner, G. Gonzalez-Burgos, N. V. Povysheva, S. Iyengar, G. Barrionuevo, and D. A. Lewis (2005)
J Neurophysiol
94, 3009-3022
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Electrical Coupling between Interneurons with Different Excitable Properties in the Stratum Lacunosum-Moleculare of the Juvenile CA1 Rat Hippocampus.
Reducing Contralateral SI Activity Reveals Hindlimb Receptive Fields in the SI Forelimb-Stump Representation of Neonatally Amputated Rats.
C. P. Pluto, N. L. Chiaia, R. W. Rhoades, and R. D. Lane (2005)
J Neurophysiol
94, 1727-1732
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Neurogliaform Neurons Form a Novel Inhibitory Network in the Hippocampal CA1 Area.
C. J. Price, B. Cauli, E. R. Kovacs, A. Kulik, B. Lambolez, R. Shigemoto, and M. Capogna (2005)
J. Neurosci.
25, 6775-6786
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Gap-Junctional Coupling between Neurogliaform Cells and Various Interneuron Types in the Neocortex.
A. Simon, S. Olah, G. Molnar, J. Szabadics, and G. Tamas (2005)
J. Neurosci.
25, 6278-6285
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Integration of Synaptic Responses to Neighboring Whiskers in Rat Barrel Cortex In Vivo.
C. Foldy, J. Dyhrfjeld-Johnsen, and I. Soltesz (2005)
J. Physiol.
562, 47-54
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Experience and Activity-Dependent Maturation of Perisomatic GABAergic Innervation in Primary Visual Cortex during a Postnatal Critical Period.
B. Chattopadhyaya, G. Di Cristo, H. Higashiyama, G. W. Knott, S. J. Kuhlman, E. Welker, and Z. J. Huang (2004)
J. Neurosci.
24, 9598-9611
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Chandelier Cells Control Excessive Cortical Excitation: Characteristics of Whisker-Evoked Synaptic Responses of Layer 2/3 Nonpyramidal and Pyramidal Neurons.