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Volume 17, Number 10,
Issue of May 15, 1997
pp. 3894-3906
Copyright ©1997 Society for Neuroscience
Molecular and Physiological Diversity of Cortical
Nonpyramidal Cells
Received Dec. 30, 1996; revised Jan. 31, 1997; accepted Feb. 27, 1997.
Bruno Cauli1,
Etienne Audinat1,
Bertrand Lambolez1,
Maria Cecilia Angulo1,
Nicole Ropert2,
Keisuke Tsuzuki3,
Shaul Hestrin4, and
Jean Rossier1
1 Neurobiologie et Diversité Cellulaire, Centre
National de la Recherche Scientifique Unité de Recherche
Associée 2054, Ecole Supérieure de Physique et de Chimie
Industrielles de la ville de Paris, 75231 Paris cedex 5, France,
2 Institut Alfred Fessard, Centre National de la Recherche
Scientifique, 91198 Gif-sur-Yvette, France, 3 Department of
Physiology, School of Medicine, Gunma University, Maebashi, Gunma 371, Japan, and 4 Department of Anatomy and Neurobiology,
University of Tennessee Memphis, Memphis, Tennessee 38163
The physiological and molecular features of nonpyramidal cells were
investigated in acute slices of sensory-motor cortex using whole-cell
recordings combined with single-cell RT-PCR to detect simultaneously
the mRNAs of three calcium binding proteins (calbindin D28k,
parvalbumin, and calretinin) and four neuropeptides (neuropeptide Y,
vasoactive intestinal polypeptide, somatostatin, and cholecystokinin). In the 97 neurons analyzed, all expressed mRNAs of at least one calcium
binding protein, and the majority (n = 73)
contained mRNAs of at least one neuropeptide. Three groups of
nonpyramidal cells were defined according to their firing pattern. (1)
Fast spiking cells (n = 34) displayed tonic
discharges of fast action potentials with no accommodation. They
expressed parvalbumin (n = 30) and/or calbindin
(n = 19) mRNAs, and half of them also contained
transcripts of at least one of the four neuropeptides. (2) Regular
spiking nonpyramidal cells (n = 48) displayed a
firing behavior characterized by a marked accommodation and presented a
large diversity of expression patterns of the seven biochemical
markers. (3) Finally, a small population of vertically oriented bipolar
cells, termed irregular spiking cells (n = 15),
fired bursts of action potentials at an irregular frequency. They
consistently co-expressed calretinin and vasoactive intestinal
polypeptide. Additional investigations of these cells showed that they
also co-expressed glutamic acid decarboxylase and choline acetyl
transferase. Our results indicate that neocortical nonpyramidal neurons
display a large diversity in their firing properties and biochemical
patterns of co-expression and that both characteristics could be
correlated to define discrete subpopulations.
Key words:
interneurons;
neocortex;
calbindin D28k;
parvalbumin;
calretinin;
neuropeptide Y;
vasoactive intestinal
polypeptide;
somatostatin;
cholecystokinin;
glutamic acid
decarboxylase;
choline acetyl transferase;
single-cell RT-PCR;
bipolar
cell;
fast spiking cell
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October 13, 2004;
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8940 - 8949.
[Abstract]
[Full Text]
[PDF]
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D. A. Fortin, J. Trettel, and E. S. Levine
Brief Trains of Action Potentials Enhance Pyramidal Neuron Excitability Via Endocannabinoid-Mediated Suppression of Inhibition
J Neurophysiol,
October 1, 2004;
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[Abstract]
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J. H. Goldberg, C. O. Lacefield, and R. Yuste
Global dendritic calcium spikes in mouse layer 5 low threshold spiking interneurones: implications for control of pyramidal cell bursting
J. Physiol.,
July 15, 2004;
558(2):
465 - 478.
[Abstract]
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F. Karube, Y. Kubota, and Y. Kawaguchi
Axon Branching and Synaptic Bouton Phenotypes in GABAergic Nonpyramidal Cell Subtypes
J. Neurosci.,
March 24, 2004;
24(12):
2853 - 2865.
[Abstract]
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Q. Xu, I. Cobos, E. De La Cruz, J. L. Rubenstein, and S. A. Anderson
Origins of Cortical Interneuron Subtypes
J. Neurosci.,
March 17, 2004;
24(11):
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[Abstract]
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S. Patz, J. Grabert, T. Gorba, M. J. Wirth, and P. Wahle
Parvalbumin Expression in Visual Cortical Interneurons Depends on Neuronal Activity and TrkB Ligands during an Early Period of Postnatal Development
Cereb Cortex,
March 1, 2004;
14(3):
342 - 351.
[Abstract]
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[PDF]
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L. Kang, V. H. Routh, E. V. Kuzhikandathil, L. D. Gaspers, and B. E. Levin
Physiological and Molecular Characteristics of Rat Hypothalamic Ventromedial Nucleus Glucosensing Neurons
Diabetes,
March 1, 2004;
53(3):
549 - 559.
[Abstract]
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[PDF]
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S. Therianos, M. Zhu, E. Pyun, and P. D. Coleman
Single-Channel Quantitative Multiplex Reverse Transcriptase-Polymerase Chain Reaction for Large Numbers of Gene Products Differentiates Nondemented from Neuropathological Alzheimer's Disease
Am. J. Pathol.,
March 1, 2004;
164(3):
795 - 806.
[Abstract]
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[PDF]
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X.-J. Wang, J. Tegner, C. Constantinidis, and P. S. Goldman-Rakic
Division of labor among distinct subtypes of inhibitory neurons in a cortical microcircuit of working memory
PNAS,
February 3, 2004;
101(5):
1368 - 1373.
[Abstract]
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[PDF]
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M. Beierlein, J. R. Gibson, and B. W. Connors
Two Dynamically Distinct Inhibitory Networks in Layer 4 of the Neocortex
J Neurophysiol,
November 1, 2003;
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[Abstract]
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A. Bacci, U. Rudolph, J. R. Huguenard, and D. A. Prince
Major Differences in Inhibitory Synaptic Transmission onto Two Neocortical Interneuron Subclasses
J. Neurosci.,
October 22, 2003;
23(29):
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[Abstract]
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M. Thoby-Brisson, B. Cauli, J. Champagnat, G. Fortin, and D. M. Katz
Expression of Functional Tyrosine Kinase B Receptors by Rhythmically Active Respiratory Neurons in the Pre-Botzinger Complex of Neonatal Mice
J. Neurosci.,
August 20, 2003;
23(20):
7685 - 7689.
[Abstract]
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C. Holmgren, T. Harkany, B. Svennenfors, and Y. Zilberter
Pyramidal cell communication within local networks in layer 2/3 of rat neocortex
J. Physiol.,
August 15, 2003;
551(1):
139 - 153.
[Abstract]
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J. H Goldberg, G. Tamas, and R. Yuste
Ca2+ imaging of mouse neocortical interneurone dendrites: Ia-type K+ channels control action potential backpropagation
J. Physiol.,
August 15, 2003;
551(1):
49 - 65.
[Abstract]
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J. H Goldberg, R. Yuste, and G. Tamas
Ca2+ imaging of mouse neocortical interneurone dendrites: Contribution of Ca2+-permeable AMPA and NMDA receptors to subthreshold Ca2+dynamics
J. Physiol.,
August 15, 2003;
551(1):
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Q. Xu, E. de la Cruz, and S. A. Anderson
Cortical Interneuron Fate Determination: Diverse Sources for Distinct Subtypes?
Cereb Cortex,
June 1, 2003;
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[Abstract]
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C.-C. Lien and P. Jonas
Kv3 Potassium Conductance is Necessary and Kinetically Optimized for High-Frequency Action Potential Generation in Hippocampal Interneurons
J. Neurosci.,
March 15, 2003;
23(6):
2058 - 2068.
[Abstract]
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Z. Xiang and D. A. Prince
Heterogeneous Actions of Serotonin on Interneurons in Rat Visual Cortex
J Neurophysiol,
March 1, 2003;
89(3):
1278 - 1287.
[Abstract]
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H.-J. Yau, H.-F. Wang, C. Lai, and F.-C. Liu
Neural Development of the Neuregulin Receptor ErbB4 in the Cerebral Cortex and the Hippocampus: Preferential Expression by Interneurons Tangentially Migrating from the Ganglionic Eminences
Cereb Cortex,
March 1, 2003;
13(3):
252 - 264.
[Abstract]
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M. C. Angulo, J. F. Staiger, J. Rossier, and E. Audinat
Distinct Local Circuits Between Neocortical Pyramidal Cells and Fast-Spiking Interneurons in Young Adult Rats
J Neurophysiol,
February 1, 2003;
89(2):
943 - 953.
[Abstract]
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A. Bacci, J. R. Huguenard, and D. A. Prince
Functional Autaptic Neurotransmission in Fast-Spiking Interneurons: A Novel Form of Feedback Inhibition in the Neocortex
J. Neurosci.,
February 1, 2003;
23(3):
859 - 866.
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T. M. Korotkova, O. A. Sergeeva, K. S. Eriksson, H. L. Haas, and R. E. Brown
Excitation of Ventral Tegmental Area Dopaminergic and Nondopaminergic Neurons by Orexins/Hypocretins
J. Neurosci.,
January 1, 2003;
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H. A. Swadlow
Fast-spike Interneurons and Feedforward Inhibition in Awake Sensory Neocortex
Cereb Cortex,
January 1, 2003;
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25 - 32.
[Abstract]
[Full Text]
[PDF]
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A. Kitamura, W. Marszalec, J. Z. Yeh, and T. Narahashi
Effects of Halothane and Propofol on Excitatory and Inhibitory Synaptic Transmission in Rat Cortical Neurons
J. Pharmacol. Exp. Ther.,
January 1, 2003;
304(1):
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A. Bacci, J. R. Huguenard, and D. A. Prince
Differential modulation of synaptic transmission by neuropeptide Y in rat neocortical neurons
PNAS,
December 24, 2002;
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[Abstract]
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C. Constantinidis and P. S. Goldman-Rakic
Correlated Discharges Among Putative Pyramidal Neurons and Interneurons in the Primate Prefrontal Cortex
J Neurophysiol,
December 1, 2002;
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[Abstract]
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R. C. Foehring, J. F. M. van Brederode, G. A. Kinney, and W. J. Spain
Serotonergic Modulation of Supragranular Neurons in Rat Sensorimotor Cortex
J. Neurosci.,
September 15, 2002;
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E. Christophe, A. Roebuck, J. F. Staiger, D. J. Lavery, S. Charpak, and E. Audinat
Two Types of Nicotinic Receptors Mediate an Excitation of Neocortical Layer I Interneurons
J Neurophysiol,
September 1, 2002;
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[Abstract]
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Y. Dalezios, R. Lujan, R. Shigemoto, J. D. B. Roberts, and P. Somogyi
Enrichment of mGluR7a in the Presynaptic Active Zones of GABAergic and Non-GABAergic Terminals on Interneurons in the Rat Somatosensory Cortex
Cereb Cortex,
September 1, 2002;
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I. Ferezou, B. Cauli, E. L. Hill, J. Rossier, E. Hamel, and B. Lambolez
5-HT3 Receptors Mediate Serotonergic Fast Synaptic Excitation of Neocortical Vasoactive Intestinal Peptide/Cholecystokinin Interneurons
J. Neurosci.,
September 1, 2002;
22(17):
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A. H. Meyer, I. Katona, M. Blatow, A. Rozov, and H. Monyer
In Vivo Labeling of Parvalbumin-Positive Interneurons and Analysis of Electrical Coupling in Identified Neurons
J. Neurosci.,
August 15, 2002;
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Z. Xiang, J. R. Huguenard, and D. A. Prince
Synaptic Inhibition of Pyramidal Cells Evoked by Different Interneuronal Subtypes in Layer V of Rat Visual Cortex
J Neurophysiol,
August 1, 2002;
88(2):
740 - 750.
[Abstract]
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R. Ruscheweyh and J. Sandkuhler
Lamina-specific membrane and discharge properties of rat spinal dorsal horn neurones in vitro
J. Physiol.,
May 15, 2002;
541(1):
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[Abstract]
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Y. Wang, A. Gupta, M. Toledo-Rodriguez, C. Z. Wu, and H. Markram
Anatomical, Physiological, Molecular and Circuit Properties of Nest Basket Cells in the Developing Somatosensory Cortex
Cereb Cortex,
April 1, 2002;
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395 - 410.
[Abstract]
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D. M. Porcello, C. S. Ho, R. H. Joho, and J. R. Huguenard
Resilient RTN Fast Spiking in Kv3.1 Null Mice Suggests Redundancy in the Action Potential Repolarization Mechanism
J Neurophysiol,
March 1, 2002;
87(3):
1303 - 1310.
[Abstract]
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H. Neuhoff, A. Neu, B. Liss, and J. Roeper
Ih Channels Contribute to the Different Functional Properties of Identified Dopaminergic Subpopulations in the Midbrain
J. Neurosci.,
February 15, 2002;
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[Abstract]
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M. Martina, S. Royer, and D. Pare
Cell-Type-Specific GABA Responses and Chloride Homeostasis in the Cortex and Amygdala
J Neurophysiol,
December 1, 2001;
86(6):
2887 - 2895.
[Abstract]
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[PDF]
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