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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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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] [Full Text] [PDF]


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J. Neurophysiol.Home page
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; 90(5): 2987 - 3000.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
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): 9664 - 9674.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
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] [Full Text] [PDF]


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J. Physiol.Home page
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] [Full Text] [PDF]


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J. Physiol.Home page
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] [Full Text] [PDF]


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J. Physiol.Home page
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): 67 - 78.
[Abstract] [Full Text] [PDF]


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Cereb CortexHome page
Q. Xu, E. de la Cruz, and S. A. Anderson
Cortical Interneuron Fate Determination: Diverse Sources for Distinct Subtypes?
Cereb Cortex, June 1, 2003; 13(6): 670 - 676.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
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] [Full Text] [PDF]


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J. Neurophysiol.Home page
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] [Full Text] [PDF]


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Cereb CortexHome page
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] [Full Text] [PDF]


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J. Neurophysiol.Home page
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] [Full Text] [PDF]


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J. Neurosci.Home page
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.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
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; 23(1): 7 - 11.
[Abstract] [Full Text] [PDF]


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Cereb CortexHome page
H. A. Swadlow
Fast-spike Interneurons and Feedforward Inhibition in Awake Sensory Neocortex
Cereb Cortex, January 1, 2003; 13(1): 25 - 32.
[Abstract] [Full Text] [PDF]


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J. Pharmacol. Exp. Ther.Home page
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): 162 - 171.
[Abstract] [Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
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; 99(26): 17125 - 17130.
[Abstract] [Full Text] [PDF]


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J. Neurophysiol.Home page
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; 88(6): 3487 - 3497.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
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; 22(18): 8238 - 8250.
[Abstract] [Full Text] [PDF]


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J. Neurophysiol.Home page
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; 88(3): 1318 - 1327.
[Abstract] [Full Text] [PDF]


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Cereb CortexHome page
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; 12(9): 961 - 974.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
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): 7389 - 7397.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
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; 22(16): 7055 - 7064.
[Abstract] [Full Text] [PDF]


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J. Neurophysiol.Home page
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] [Full Text] [PDF]


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J. Physiol.Home page
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): 231 - 244.
[Abstract] [Full Text] [PDF]


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Cereb CortexHome page
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; 12(4): 395 - 410.
[Abstract] [Full Text] [PDF]


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J. Neurophysiol.Home page
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] [Full Text] [PDF]


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J. Neurosci.Home page
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; 22(4): 1290 - 1302.
[Abstract] [Full Text] [PDF]


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J. Neurophysiol.Home page
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] [Full Text] [PDF]


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J. Neurosci.Home page
D. Contreras and R. Llinas
Voltage-Sensitive Dye Imaging of Neocortical Spatiotemporal Dynamics to Afferent Activation Frequency
J. Neurosci., December 1, 2001; 21(23): 9403 - 9413.
[Abstract] [Full Text] [PDF]



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