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.

Science 31 July 1992:
Vol. 257. no. 5070, pp. 665 - 669
DOI: 10.1126/science.1496379
Prev | Table of Contents | Next

Articles

Science, Vol 257, Issue 5070, 665-669
Copyright © 1992 by American Association for the Advancement of Science

articles

Neuronal domains in developing neocortex

R Yuste, A Peinado, and LC Katz

Department of Neurobiology, Duke University Medical Center, Durham, NC 27710.

The mammalian neocortex consists of a mosaic of columnar units whose development is poorly understood. Optical recordings of brain slices labeled with the fluorescent calcium indicator fura-2 revealed that the neonatal rat cortex was partitioned into distinct domains of spontaneously coactive neurons. In tangential slices, these domains were 50 to 120 micrometers in diameter; in coronal slices they spanned several cortical layers and resembled columns found in the adult cortex. In developing somatosensory cortex, domains were smaller than, and distinct from, the barrels, which represent sensory input from a single vibrissa. The neurons within each domain were coupled by gap junctions. Thus, nonsynaptic communication during cortical development defines discrete multicellular patterns that could presage adult functional architecture.


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Spontaneous Bursting Activity in the Developing Entorhinal Cortex.
M. G. Sheroziya, O. von Bohlen und Halbach, K. Unsicker, and A. V. Egorov (2009)
J. Neurosci. 29, 12131-12144
   Abstract »    Full Text »    PDF »
Experience-dependent maturation of the glomerular microcircuit.
B. J. Maher, M. J. McGinley, and G. L. Westbrook (2009)
PNAS 106, 16865-16870
   Abstract »    Full Text »    PDF »
Stability of Electrical Coupling despite Massive Developmental Changes of Intrinsic Neuronal Physiology.
P. R. L. Parker, S. J. Cruikshank, and B. W. Connors (2009)
J. Neurosci. 29, 9761-9770
   Abstract »    Full Text »    PDF »
Three Patterns of Oscillatory Activity Differentially Synchronize Developing Neocortical Networks In Vivo.
J.-W. Yang, I. L. Hanganu-Opatz, J.-J. Sun, and H. J. Luhmann (2009)
J. Neurosci. 29, 9011-9025
   Abstract »    Full Text »    PDF »
NMDA Receptors Pattern Early Activity in the Developing Barrel Cortex In Vivo.
M. Minlebaev, Y. Ben-Ari, and R. Khazipov (2009)
Cereb Cortex 19, 688-696
   Abstract »    Full Text »    PDF »
Cellular Mechanisms of Subplate-Driven and Cholinergic Input-Dependent Network Activity in the Neonatal Rat Somatosensory Cortex.
I. L. Hanganu, A. Okabe, V. Lessmann, and H. J. Luhmann (2009)
Cereb Cortex 19, 89-105
   Abstract »    Full Text »    PDF »
Sequential Generation of Two Distinct Synapse-Driven Network Patterns in Developing Neocortex.
C. Allene, A. Cattani, J. B. Ackman, P. Bonifazi, L. Aniksztejn, Y. Ben-Ari, and R. Cossart (2008)
J. Neurosci. 28, 12851-12863
   Abstract »    Full Text »    PDF »
Excitatory GABA in Rodent Developing Neocortex In Vitro.
S. Rheims, M. Minlebaev, A. Ivanov, A. Represa, R. Khazipov, G. L. Holmes, Y. Ben-Ari, and Y. Zilberter (2008)
J Neurophysiol 100, 609-619
   Abstract »    Full Text »    PDF »
Neuronal avalanches organize as nested theta- and beta/gamma-oscillations during development of cortical layer 2/3.
E. D. Gireesh and D. Plenz (2008)
PNAS 105, 7576-7581
   Abstract »    Full Text »    PDF »
Subcolumnar Dendritic and Axonal Organization of Spiny Stellate and Star Pyramid Neurons within a Barrel in Rat Somatosensory Cortex.
V. Egger, T. Nevian, and R. M. Bruno (2008)
Cereb Cortex 18, 876-889
   Abstract »    Full Text »    PDF »
GABA: A Pioneer Transmitter That Excites Immature Neurons and Generates Primitive Oscillations.
Y. Ben-Ari, J.-L. Gaiarsa, R. Tyzio, and R. Khazipov (2007)
Physiol Rev 87, 1215-1284
   Abstract »    Full Text »    PDF »
Rapid Cortical Oscillations and Early Motor Activity in Premature Human Neonate.
M. Milh, A. Kaminska, C. Huon, A. Lapillonne, Y. Ben-Ari, and R. Khazipov (2007)
Cereb Cortex 17, 1582-1594
   Abstract »    Full Text »    PDF »
Identification and Dynamics of Spontaneous Burst Initiation Zones in Unidimensional Neuronal Cultures.
O. Feinerman, M. Segal, and E. Moses (2007)
J Neurophysiol 97, 2937-2948
   Abstract »    Full Text »    PDF »
Giant Spontaneous Depolarizing Potentials in the Developing Thalamic Reticular Nucleus.
S. Pangratz-Fuehrer, U. Rudolph, and J. R. Huguenard (2007)
J Neurophysiol 97, 2364-2372
   Abstract »    Full Text »    PDF »
Network Mechanisms of Spindle-Burst Oscillations in the Neonatal Rat Barrel Cortex In Vivo.
M. Minlebaev, Y. Ben-Ari, and R. Khazipov (2007)
J Neurophysiol 97, 692-700
   Abstract »    Full Text »    PDF »
A Temporal Continuity to the Vertical Organization of the Human Neocortex.
M. F. Casanova, J. Trippe II, and A. Switala (2007)
Cereb Cortex 17, 130-137
   Abstract »    Full Text »    PDF »
Initiation and Propagation of Neuronal Coactivation in the Developing Hippocampus.
S. Bolea, J. V. Sanchez-Andres, X. Huang, and J.-y. Wu (2006)
J Neurophysiol 95, 552-561
   Abstract »    Full Text »    PDF »
Age-dependent Spontaneous Hyperexcitability and Impairment of GABAergic Function in the Hippocampus of Mice Lacking trkB.
M. A. Carmona, E. Pozas, A. Martinez, J. F. Espinosa-Parrilla, E. Soriano, and F. Aguado (2006)
Cereb Cortex 16, 47-63
   Abstract »    Full Text »    PDF »
Signal Propagation Along Unidimensional Neuronal Networks.
O. Feinerman, M. Segal, and E. Moses (2005)
J Neurophysiol 94, 3406-3416
   Abstract »    Full Text »    PDF »
Optical Imaging of Large-Scale Correlated Wave Activity in the Developing Rat CNS.
Y. Momose-Sato, Y. Honda, H. Sasaki, and K. Sato (2005)
J Neurophysiol 94, 1606-1622
   Abstract »    Full Text »    PDF »
Drosophila Mushroom Body Kenyon Cells Generate Spontaneous Calcium Transients Mediated by PLTX-Sensitive Calcium Channels.
S. A. Jiang, J. M. Campusano, H. Su, and D. K. O'Dowd (2005)
J Neurophysiol 94, 491-500
   Abstract »    Full Text »    PDF »
Ion Channel Development, Spontaneous Activity, and Activity-Dependent Development in Nerve and Muscle Cells.
W. J. Moody and M. M. Bosma (2005)
Physiol Rev 85, 883-941
   Abstract »    Full Text »    PDF »
Gq/11-Induced and Spontaneous Waves of Coordinated Network Activation in Developing Frontal Cortex.
D. P. Calderon, N. Leverkova, and A. Peinado (2005)
J. Neurosci. 25, 1737-1749
   Abstract »    Full Text »    PDF »
Monitoring Neural Activity and [Ca2+] with Genetically Encoded Ca2+ Indicators.
T. A. Pologruto, R. Yasuda, and K. Svoboda (2004)
J. Neurosci. 24, 9572-9579
   Abstract »    Full Text »    PDF »
Imaging Calcium Concentration Dynamics in Small Neuronal Compartments.
R. Yasuda, E. A. Nimchinsky, V. Scheuss, T. A. Pologruto, T. G. Oertner, B. L. Sabatini, and K. Svoboda (2004)
Sci. STKE 2004, pl5
   Abstract »    Full Text »    PDF »
Transient Electrical Coupling Delays the Onset of Chemical Neurotransmission at Developing Synapses.
T. M. Szabo, D. S. Faber, and M. J. Zoran (2004)
J. Neurosci. 24, 112-120
   Abstract »    Full Text »    PDF »
Axon Guidance by Growth Cones and Branches: Common Cytoskeletal and Signaling Mechanisms.
E. W. Dent, F. Tang, and K. Kalil (2003)
Neuroscientist 9, 343-353
   Abstract »    PDF »
Segregation and Coactivation of Developing Neocortical Layer 1 Neurons.
T. Soda, R. Nakashima, D. Watanabe, K. Nakajima, I. Pastan, and S. Nakanishi (2003)
J. Neurosci. 23, 6272-6279
   Abstract »    Full Text »    PDF »
NMDA Receptors in Cortical Development are Essential for the Generation of Coordinated Increases in [Ca2+]i in 'Neuronal Domains'.
H. Okada, N. Miyakawa, H. Mori, M. Mishina, Y. Miyamoto, and T. Hisatsune (2003)
Cereb Cortex 13, 749-757
   Abstract »    Full Text »    PDF »
Carbachol-induced Network Oscillations in the Intact Cerebral Cortex of the Newborn Rat.
W. Kilb and H. J. Luhmann (2003)
Cereb Cortex 13, 409-421
   Abstract »    Full Text »    PDF »
BDNF regulates spontaneous correlated activity at early developmental stages by increasing synaptogenesis and expression of the K+/Cl- co-transporter KCC2.
F. Aguado, M. A. Carmona, E. Pozas, A. Aguilo, F. J. Martinez-Guijarro, S. Alcantara, V. Borrell, R. Yuste, C. F. Ibanez, and E. Soriano (2003)
Development 130, 1267-1280
   Abstract »    Full Text »    PDF »
Honeycomb-Like Mosaic at the Border of Layers 1 and 2 in the Cerebral Cortex.
N. Ichinohe, F. Fujiyama, T. Kaneko, and K. S. Rockland (2003)
J. Neurosci. 23, 1372-1382
   Abstract »    Full Text »    PDF »
Spontaneous Calcium Transients in Developing Cortical Neurons Regulate Axon Outgrowth.
F. Tang, E. W. Dent, and K. Kalil (2003)
J. Neurosci. 23, 927-936
   Abstract »    Full Text »    PDF »
Optical Analysis of Depolarization Waves in the Embryonic Brain: A Dual Network of Gap Junctions and Chemical Synapses.
Y. Momose-Sato, N. Miyakawa, H. Mochida, S. Sasaki, and K. Sato (2003)
J Neurophysiol 89, 600-614
   Abstract »    Full Text »    PDF »
Local and Global Spontaneous Calcium Events Regulate Neurite Outgrowth and Onset of GABAergic Phenotype during Neural Precursor Differentiation.
F. Ciccolini, T. J. Collins, J. Sudhoelter, P. Lipp, M. J. Berridge, and M. D. Bootman (2003)
J. Neurosci. 23, 103-111
   Abstract »    Full Text »    PDF »
Spontaneous Development of Synchronous Oscillatory Activity During Maturation of Cortical Networks In Vitro.
T. Opitz, A. D. De Lima, and T. Voigt (2002)
J Neurophysiol 88, 2196-2206
   Abstract »    Full Text »    PDF »
Neuronal Activity Regulates Correlated Network Properties of Spontaneous Calcium Transients in Astrocytes In Situ.
F. Aguado, J. F. Espinosa-Parrilla, M. A. Carmona, and E. Soriano (2002)
J. Neurosci. 22, 9430-9444
   Abstract »    Full Text »    PDF »
Axonal Projection, Input and Output Synapses, and Synaptic Physiology of Cajal-Retzius Cells in the Developing Rat Neocortex.
G. Radnikow, D. Feldmeyer, and J. Lubke (2002)
J. Neurosci. 22, 6908-6919
   Abstract »    Full Text »    PDF »
In Vivo Labeling of Parvalbumin-Positive Interneurons and Analysis of Electrical Coupling in Identified Neurons.
A. H. Meyer, I. Katona, M. Blatow, A. Rozov, and H. Monyer (2002)
J. Neurosci. 22, 7055-7064
   Abstract »    Full Text »    PDF »
Correlated Bursts of Activity in the Neonatal Hippocampus in Vivo.
X. Leinekugel, R. Khazipov, R. Cannon, H. Hirase, Y. Ben-Ari, and G. Buzsaki (2002)
Science 296, 2049-2052
   Abstract »    Full Text »    PDF »
The minicolumn hypothesis in neuroscience.
D. P. Buxhoeveden and M. F. Casanova (2002)
Brain 125, 935-951
   Abstract »    Full Text »    PDF »
Brain-derived Neurotrophic Factor-induced Potentiation of Ca2+ Oscillations in Developing Cortical Neurons.
T. Numakawa, S. Yamagishi, N. Adachi, T. Matsumoto, D. Yokomaku, M. Yamada, and H. Hatanaka (2002)
J. Biol. Chem. 277, 6520-6529
   Abstract »    Full Text »    PDF »
Spontaneous Activity in Developing Ferret Visual Cortex In Vivo.
C. Chiu and M. Weliky (2001)
J. Neurosci. 21, 8906-8914
   Abstract »    Full Text »    PDF »
Spatiotemporal Properties of an Evoked Population Activity in Rat Sensory Cortical Slices.
J.-Y. Wu, L. Guan, L. Bai, and Q. Yang (2001)
J Neurophysiol 86, 2461-2474
   Abstract »    Full Text »    PDF »
Potentiation of L-Type Calcium Channels Reveals Nonsynaptic Mechanisms that Correlate Spontaneous Activity in the Developing Mammalian Retina.
J. H. Singer, R. R. Mirotznik, and M. B. Feller (2001)
J. Neurosci. 21, 8514-8522
   Abstract »    Full Text »    PDF »
Immature Neocortical Neurons Exist as Extensive Syncitial Networks Linked by Dendrodendritic Electrical Connections.
A. Peinado (2001)
J Neurophysiol 85, 620-629
   Abstract »    Full Text »    PDF »
GABAergic Inhibition Suppresses Paroxysmal Network Activity in the Neonatal Rodent Hippocampus and Neocortex.
J. E. Wells, J. T. Porter, and A. Agmon (2000)
J. Neurosci. 20, 8822-8830
   Abstract »    Full Text »    PDF »
Mice Lacking Specific Nicotinic Acetylcholine Receptor Subunits Exhibit Dramatically Altered Spontaneous Activity Patterns and Reveal a Limited Role for Retinal Waves in Forming ON and OFF Circuits in the Inner Retina.
A. Bansal, J. H. Singer, B. J. Hwang, W. Xu, A. Beaudet, and M. B. Feller (2000)
J. Neurosci. 20, 7672-7681
   Abstract »    Full Text »    PDF »
L-Type Calcium Channels Mediate Calcium Oscillations in Early Postnatal Purkinje Neurons.
P. Liljelund, J. G. Netzeband, and D. L. Gruol (2000)
J. Neurosci. 20, 7394-7403
   Abstract »    Full Text »    PDF »
Myelination Defects and Neuronal Hyperexcitability in the Neocortex of Connexin 32-deficient Mice.
B. Sutor, C. Schmolke, B. Teubner, C. Schirmer, and K. Willecke (2000)
Cereb Cortex 10, 684-697
   Abstract »    Full Text »    PDF »
Microcolumns in the cerebral cortex.
E. G. Jones (2000)
PNAS 97, 5019-5021
   Full Text »    PDF »
Gap Junctional Coupling and Patterns of Connexin Expression among Neonatal Rat Lumbar Spinal Motor Neurons.
Q. Chang, M. Gonzalez, M. J. Pinter, and R. J. Balice-Gordon (1999)
J. Neurosci. 19, 10813-10828
   Abstract »    Full Text »    PDF »
Endogenous activation of metabotropic glutamate receptors in neocortical development causes neuronal calcium oscillations.
A. C. Flint, R. S. Dammerman, and A. R. Kriegstein (1999)
PNAS 96, 12144-12149
   Abstract »    Full Text »    PDF »
Propagating Activation during Oscillations and Evoked Responses in Neocortical Slices.
J.-y. Wu, L. Guan, and Y. Tsau (1999)
J. Neurosci. 19, 5005-5015
   Abstract »    Full Text »    PDF »
Retinal Waves Are Governed by Collective Network Properties.
D. A. Butts, M. B. Feller, C. J. Shatz, and D. S. Rokhsar (1999)
J. Neurosci. 19, 3580-3593
   Abstract »    Full Text »    PDF »
Giant Depolarizing Potentials: the Septal Pole of the Hippocampus Paces the Activity of the Developing Intact Septohippocampal Complex In Vitro.
X. Leinekugel, I. Khalilov, Y. Ben-Ari, and R. Khazipov (1998)
J. Neurosci. 18, 6349-6357
   Abstract »    Full Text »    PDF »
Initiation of Spontaneous Epileptiform Activity in the Neocortical Slice.
Y. Tsau, L. Guan, and J.-Y. Wu (1998)
J Neurophysiol 80, 978-982
   Abstract »    Full Text »    PDF »
Patterns of Intracellular Calcium Fluctuation in Precursor Cells of the Neocortical Ventricular Zone.
D. F. Owens and A. R. Kriegstein (1998)
J. Neurosci. 18, 5374-5388
   Abstract »    Full Text »    PDF »
Coordination of Neuronal Activity in Developing Visual Cortex by Gap Junction-Mediated Biochemical Communication.
K. Kandler and L. C. Katz (1998)
J. Neurosci. 18, 1419-1427
   Abstract »    Full Text »    PDF »
Developmental profile and synaptic origin of early network oscillations in the CA1 region of rat neonatal hippocampus.
O. Garaschuk, E. Hanse, and A. Konnerth (1998)
J. Physiol. 507, 219-236
   Abstract »    Full Text »    PDF »
Retrograde Signaling in the Development and Modification of Synapses.
R. M. FITZSIMONDS and M.-M. POO (1998)
Physiol Rev 78, 143-170
   Abstract »    Full Text »    PDF »
Cell Coupling and Uncoupling in the Ventricular Zone of Developing Neocortex.
K. Bittman, D. F. Owens, A. R. Kriegstein, and J. J. LoTurco (1997)
J. Neurosci. 17, 7037-7044
   Abstract »    Full Text »    PDF »
Differential Expression of Connexins during Neocortical Development and Neuronal Circuit Formation.
B. Nadarajah, A. M. Jones, W. H. Evans, and J. G. Parnavelas (1997)
J. Neurosci. 17, 3096-3111
   Abstract »    Full Text »    PDF »
Cell-Cell Signaling in Early Cortical Development.
A. R. Kriegstein (1995)
Neuroscientist 1, 268-276
   Abstract »    PDF »
Requirement for BDNF in activity-dependent survival of cortical neurons.
A Ghosh, J Carnahan, and M. Greenberg (1994)
Science 263, 1618-1623
   Abstract »    PDF »
Regional Differences in the Critical Period Neurodevelopment in the Mouse: Implications for Neonatal Seizures.
M. J. Litzinger, C. L. Mouritsen, B. B. Grover, M. S. Esplin, and J. R. Abbott (1994)
J Child Neurol 9, 77-80
   Abstract »    PDF »
From the Cover: Description of microcolumnar ensembles in association cortex and their disruption in Alzheimer and Lewy body dementias.
S. V. Buldyrev, L. Cruz, T. Gomez-Isla, E. Gomez-Tortosa, S. Havlin, R. Le, H. E. Stanley, B. Urbanc, and B. T. Hyman (2000)
PNAS 97, 5039-5043
   Abstract »    Full Text »    PDF »
Connexin expression in electrically coupled postnatal rat brain neurons.
L. Venance, A. Rozov, M. Blatow, N. Burnashev, D. Feldmeyer, and H. Monyer (2000)
PNAS 97, 10260-10265
   Abstract »    Full Text »    PDF »
Traveling Slow Waves of Neural Activity: A Novel Form of Network Activity in Developing Neocortex.
A. Peinado (2000)
J. Neurosci. 20, RC54
   Abstract »    Full Text »    PDF »


To Advertise     Find Products

Science. ISSN 0036-8075 (print), 1095-9203 (online)