 |
Previous Article | Next Article 
Volume 16, Number 17,
Issue of September 1, 1996
pp. 5290-5300
Copyright ©1996 Society for Neuroscience
Morphology and Physiology of Cortical Neurons in Layer I
Received Feb. 20, 1996; revised June 4, 1996; accepted June 5, 1996.
Shaul Hestrin1, 2 and
William E. Armstrong1
Departments of 1 Anatomy and Neurobiology and
2 Neurology, University of Tennessee, Memphis, Tennessee
38163
The electrophysiological and morphological properties of layer I
neurons were studied in visual cortex slices from 7- to 19-d-old rats
using whole-cell recording and biocytin labeling. A heterogeneous
population of small, nonpyramidal neurons was found. Approximately one
third of the cells we recorded were neurogliaform cells; another third
were multipolar neurons with axons descending out of layer I. The
remaining cells were heterogeneous and were not classified. In slices
from 7- to 10-d-old animals only, we identified Cajal-Retzius
cells.
Neurogliaform neurons had a very dense local axonal field, which was
largely contained within layer I. Cells with descending axons had a
relatively sparse local axonal arbor and projected at least to layer II
and sometimes deeper. Spiking in neurogliaform neurons was followed by
an afterdepolarizing potential, whereas spiking in cells with
descending axons was followed by a slow after-hyperpolarizing potential
(AHP). In addition, neurogliaform cells exhibited less spike broadening
and a larger fast AHP after single spikes than did cells with
descending axons. Generally, cells in layer I received synaptic inputs
characterized as either GABA- or glutamate-mediated, suggesting the
presence of excitatory and inhibitory inputs.
With their output largely limited to layer I, neurogliaform cells could
synapse with other layer I neurons, the most distal dendritic branches
of pyramidal cells, or the dendrites of layer II/III interneurons,
which invade layer I. Cells with descending axons could contact a wide
variety of cortical cells throughout their vertical projection.
Key words:
neurogliaform;
Cajal-Retzius;
afterdepolarization;
afterhyperpolarization;
excitation;
inhibition
This article has been cited by other articles:

|
 |

|
 |
 
A. Young and Q.-Q. Sun
GABAergic Inhibitory Interneurons in the Posterior Piriform Cortex of the GAD67-GFP Mouse
Cereb Cortex,
December 1, 2009;
19(12):
3011 - 3029.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Helmstaedter, B. Sakmann, and D. Feldmeyer
L2/3 Interneuron Groups Defined by Multiparameter Analysis of Axonal Projection, Dendritic Geometry, and Electrical Excitability
Cereb Cortex,
April 1, 2009;
19(4):
951 - 962.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Karagiannis, T. Gallopin, C. David, D. Battaglia, H. Geoffroy, J. Rossier, E. M. C. Hillman, J. F. Staiger, and B. Cauli
Classification of NPY-Expressing Neocortical Interneurons
J. Neurosci.,
March 18, 2009;
29(11):
3642 - 3659.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. Kirmse, A. Dvorzhak, R. Grantyn, and S. Kirischuk
Developmental Downregulation of Excitatory GABAergic Transmission in Neocortical Layer I via Presynaptic Adenosine A1 Receptors
Cereb Cortex,
February 1, 2008;
18(2):
424 - 432.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. Kirmse, A. Dvorzhak, C. Henneberger, R. Grantyn, and S. Kirischuk
Cajal Retzius cells in the mouse neocortex receive two types of pre- and postsynaptically distinct GABAergic inputs
J. Physiol.,
December 15, 2007;
585(3):
881 - 895.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
N. V. Povysheva, A. V. Zaitsev, S. Kroner, O. A. Krimer, D. C. Rotaru, G. Gonzalez-Burgos, D. A. Lewis, and L. S. Krimer
Electrophysiological Differences Between Neurogliaform Cells From Monkey and Rat Prefrontal Cortex
J Neurophysiol,
February 1, 2007;
97(2):
1030 - 1039.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. Shlosberg, Y. Amitai, and R. Azouz
Time-Dependent, Layer-Specific Modulation of Sensory Responses Mediated by Neocortical Layer 1
J Neurophysiol,
December 1, 2006;
96(6):
3170 - 3182.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Z. Chu and S. M. Moenter
Physiologic Regulation of a Tetrodotoxin-Sensitive Sodium Influx That Mediates a Slow Afterdepolarization Potential in Gonadotropin-Releasing Hormone Neurons: Possible Implications for the Central Regulation of Fertility.
J. Neurosci.,
November 15, 2006;
26(46):
11961 - 11973.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. Kirmse and S. Kirischuk
Ambient GABA constrains the strength of GABAergic synapses at Cajal-Retzius cells in the developing visual cortex.
J. Neurosci.,
April 19, 2006;
26(16):
4216 - 4227.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
V. Zsiros and G. Maccaferri
Electrical Coupling between Interneurons with Different Excitable Properties in the Stratum Lacunosum-Moleculare of the Juvenile CA1 Rat Hippocampus
J. Neurosci.,
September 21, 2005;
25(38):
8686 - 8695.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. J. Price, B. Cauli, E. R. Kovacs, A. Kulik, B. Lambolez, R. Shigemoto, and M. Capogna
Neurogliaform Neurons Form a Novel Inhibitory Network in the Hippocampal CA1 Area
J. Neurosci.,
July 20, 2005;
25(29):
6775 - 6786.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Simon, S. Olah, G. Molnar, J. Szabadics, and G. Tamas
Gap-Junctional Coupling between Neurogliaform Cells and Various Interneuron Types in the Neocortex
J. Neurosci.,
July 6, 2005;
25(27):
6278 - 6285.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Wu and J. J. Hablitz
Cooperative Activation of D1 and D2 Dopamine Receptors Enhances a Hyperpolarization-Activated Inward Current in Layer I Interneurons
J. Neurosci.,
July 6, 2005;
25(27):
6322 - 6328.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. B. Merriam, T. I. Netoff, and M. I. Banks
Bistable Network Behavior of Layer I Interneurons in Auditory Cortex
J. Neurosci.,
June 29, 2005;
25(26):
6175 - 6186.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. J. Higley and D. Contreras
Integration of Synaptic Responses to Neighboring Whiskers in Rat Barrel Cortex In Vivo
J Neurophysiol,
April 1, 2005;
93(4):
1920 - 1934.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Zhu and J. J. Zhu
Rapid Arrival and Integration of Ascending Sensory Information in Layer 1 Nonpyramidal Neurons and Tuft Dendrites of Layer 5 Pyramidal Neurons of the Neocortex
J. Neurosci.,
February 11, 2004;
24(6):
1272 - 1279.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Gonchar and A. Burkhalter
Distinct GABAergic Targets of Feedforward and Feedback Connections Between Lower and Higher Areas of Rat Visual Cortex
J. Neurosci.,
November 26, 2003;
23(34):
10904 - 10912.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Soda, R. Nakashima, D. Watanabe, K. Nakajima, I. Pastan, and S. Nakanishi
Segregation and Coactivation of Developing Neocortical Layer 1 Neurons
J. Neurosci.,
July 16, 2003;
23(15):
6272 - 6279.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. Tamas, A. L. A. Simon, and J. Szabadics
Identified Sources and Targets of Slow Inhibition in the Neocortex
Science,
March 21, 2003;
299(5614):
1902 - 1905.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. G. Nowak, R. Azouz, M. V. Sanchez-Vives, C. M. Gray, and D. A. McCormick
Electrophysiological Classes of Cat Primary Visual Cortical Neurons In Vivo as Revealed by Quantitative Analyses
J Neurophysiol,
March 1, 2003;
89(3):
1541 - 1566.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Z. Chu, M. Galarreta, and S. Hestrin
Synaptic Interactions of Late-Spiking Neocortical Neurons in Layer 1
J. Neurosci.,
January 1, 2003;
23(1):
96 - 102.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
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]
|
 |
|

|
 |

|
 |
 
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]
|
 |
|

|
 |

|
 |
 
G. Radnikow, D. Feldmeyer, and J. Lubke
Axonal Projection, Input and Output Synapses, and Synaptic Physiology of Cajal-Retzius Cells in the Developing Rat Neocortex
J. Neurosci.,
August 15, 2002;
22(16):
6908 - 6919.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Peters and C. Sethares
The Effects of Age on the Cells in Layer 1 of Primate Cerebral Cortex
Cereb Cortex,
January 1, 2002;
12(1):
27 - 36.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
W. Kilb and H. J. Luhmann
Characterization of a Hyperpolarization-Activated Inward Current in Cajal-Retzius Cells in Rat Neonatal Neocortex
J Neurophysiol,
September 1, 2000;
84(3):
1681 - 1691.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. S. Dammerman, A. C. Flint, S. Noctor, and A. R. Kriegstein
An Excitatory GABAergic Plexus in Developing Neocortical Layer 1
J Neurophysiol,
July 1, 2000;
84(1):
428 - 434.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Aguilo, T. H. Schwartz, V. S. Kumar, Z. A. Peterlin, A. Tsiola, E. Soriano, and R. Yuste
Involvement of Cajal-Retzius Neurons in Spontaneous Correlated Activity of Embryonic and Postnatal Layer 1 from Wild-Type and Reeler Mice
J. Neurosci.,
December 15, 1999;
19(24):
10856 - 10868.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J.-M. Mienville
Feature Article: Cajal-Retzius Cell Physiology: Just in Time to Bridge the 20th Century
Cereb Cortex,
December 1, 1999;
9(8):
776 - 782.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J.-M. Mienville, I. Maric, D. Maric, and J. R. Clay
Loss of IA Expression and Increased Excitability in Postnatal Rat Cajal-Retzius Cells
J Neurophysiol,
September 1, 1999;
82(3):
1303 - 1310.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. R. Alper
The EEG and Cocaine Sensitization: A Hypothesis
J Neuropsychiatry Clin Neurosci,
May 1, 1999;
11(2):
209 - 221.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
J.-M. Mienville and C. Pesold
Low Resting Potential and Postnatal Upregulation of NMDA Receptors May Cause Cajal-Retzius Cell Death
J. Neurosci.,
March 1, 1999;
19(5):
1636 - 1646.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J.-M. Mienville
Persistent depolarizing action of GABA in rat Cajal-Retzius cells
J. Physiol.,
November 1, 1998;
512(3):
809 - 817.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. Ceranik, R. Bender, J. R. P. Geiger, H. Monyer, P. Jonas, M. Frotscher, and J. Lubke
A Novel Type of GABAergic Interneuron Connecting the Input and the Output Regions of the Hippocampus
J. Neurosci.,
July 15, 1997;
17(14):
5380 - 5394.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. S. Fortune and G. J. Rose
Passive and Active Membrane Properties Contribute to the Temporal Filtering Properties of Midbrain Neurons In Vivo
J. Neurosci.,
May 15, 1997;
17(10):
3815 - 3825.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|

|