 |
Previous Article | Next Article 
The Journal of Neuroscience, May 1, 2000, 20(9):3354-3368
Novel Hippocampal Interneuronal Subtypes Identified Using
Transgenic Mice That Express Green Fluorescent Protein in GABAergic
Interneurons
Anthony A.
Oliva Jr1, 2,
Minghui
Jiang1, 3,
Trang
Lam1, 3,
Karen L.
Smith1, 3, and
John W.
Swann1, 2, 3
1 The Cain Foundation Laboratories,
2 Division of Neuroscience, and 3 Department of
Pediatrics, Baylor College of Medicine Houston, Texas 77030
The chief inhibitory neurons of the mammalian brain, GABAergic
neurons, are comprised of a myriad of diverse neuronal subtypes. To
facilitate the study of these neurons, transgenic mice were generated
that express enhanced green fluorescent protein (EGFP) in
subpopulations of GABAergic neurons. In one of the resulting transgenic
lines, called GIN (GFP-expressing Inhibitory
Neurons), EGFP was found to be expressed in a subpopulation
of somatostatin-containing GABAergic interneurons in the hippocampus
and neocortex. In both live and fixed brain preparations from these
mice, detailed microanatomical features of EGFP-expressing interneurons
were readily observed. In stratum oriens of the hippocampus,
EGFP-expressing interneurons were comprised almost exclusively of
oriens/alveus interneurons with lacunosum-moleculare axon arborization
(O-LM cells). In the neocortex, the somata of EGFP-expressing
interneurons were largely restricted to layers II-IV and upper layer V.
In hippocampal area CA1, two previously uncharacterized subtypes of
interneurons were identified using the GIN mice: stratum pyramidale
interneurons with lacunosum-moleculare axon arborization (P-LM cells)
and stratum radiatum interneurons with lacunosum-moleculare axon
arborization (R-LM cells). These newly identified interneuronal subtypes appeared to be closely related to O-LM cell, as they selectively innervate stratum lacunosum-moleculare. Whole-cell patch-clamp recordings revealed that these cells were fast-spiking and
showed virtually no spike frequency accommodation. The
microanatomical features of these cells suggest that they function
primarily as "input-biasing" neurons, in that synaptic volleys in
stratum radiatum would lead to their activation, which in turn would
result in selective suppression of excitatory input from the entorhinal cortex onto CA1 pyramidal cells.
Key words:
GABAergic neurons; interneurons; green fluorescent
protein; GFP; EGFP; transgenic mice; hippocampus; cortex; somatostatin; metabotropic glutamate receptor; mGluR1; mGluR1a; glutamic acid
decarboxylase; GAD67; Gad1; GABA
Copyright © 2000 Society for Neuroscience 0270-6474/00/2093354-15$05.00/0
This article has been cited by other articles:

|
 |

|
 |
 
A. Caputi, A. Rozov, M. Blatow, and H. Monyer
Two Calretinin-Positive GABAergic Cell Types in Layer 2/3 of the Mouse Neocortex Provide Different Forms of Inhibition
Cereb Cortex,
October 8, 2008;
(2008)
bhn175v1.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. F. Bartley, Z. J. Huang, K. M. Huber, and J. R. Gibson
Differential Activity-Dependent, Homeostatic Plasticity of Two Neocortical Inhibitory Circuits
J Neurophysiol,
October 1, 2008;
100(4):
1983 - 1994.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. Powers-Martin, J. K. Phillip, V. C. Biancardi, and J. E. Stern
Heterogeneous distribution of basal cyclic guanosine monophosphate within distinct neuronal populations in the hypothalamic paraventricular nucleus
Am J Physiol Regulatory Integrative Comp Physiol,
October 1, 2008;
295(4):
R1341 - R1350.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. T. Roberts, K. J. Bender, and L. O. Trussell
Fidelity of Complex Spike-Mediated Synaptic Transmission between Inhibitory Interneurons
J. Neurosci.,
September 17, 2008;
28(38):
9440 - 9450.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
I. Vardya, K. R. Drasbek, Z. Dosa, and K. Jensen
Cell Type-Specific GABAA Receptor-Mediated Tonic Inhibition in Mouse Neocortex
J Neurophysiol,
July 1, 2008;
100(1):
526 - 532.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. H. Gittis and S. du Lac
Similar Properties of Transient, Persistent, and Resurgent Na Currents in GABAergic and Non-GABAergic Vestibular Nucleus Neurons
J Neurophysiol,
May 1, 2008;
99(5):
2060 - 2065.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. W. Bailey, S. M. Appleyard, Y.-H. Jin, and M. C. Andresen
Organization and Properties of GABAergic Neurons in Solitary Tract Nucleus (NTS)
J Neurophysiol,
April 1, 2008;
99(4):
1712 - 1722.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Uematsu, Y. Hirai, F. Karube, S. Ebihara, M. Kato, K. Abe, K. Obata, S. Yoshida, M. Hirabayashi, Y. Yanagawa, et al.
Quantitative Chemical Composition of Cortical GABAergic Neurons Revealed in Transgenic Venus-Expressing Rats
Cereb Cortex,
February 1, 2008;
18(2):
315 - 330.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. Li, H. Adesnik, J. Li, J. Long, R. A. Nicoll, J. L. R. Rubenstein, and S. J. Pleasure
Regional Distribution of Cortical Interneurons and Development of Inhibitory Tone Are Regulated by Cxcl12/Cxcr4 Signaling
J. Neurosci.,
January 30, 2008;
28(5):
1085 - 1098.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Goldin, J. Epsztein, I. Jorquera, A. Represa, Y. Ben-Ari, V. Crepel, and R. Cossart
Synaptic Kainate Receptors Tune Oriens-Lacunosum Moleculare Interneurons to Operate at Theta Frequency
J. Neurosci.,
September 5, 2007;
27(36):
9560 - 9572.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
N. R. Glatzer, A. V. Derbenev, B. W. Banfield, and B. N. Smith
Endomorphin-1 Modulates Intrinsic Inhibition in the Dorsal Vagal Complex
J Neurophysiol,
September 1, 2007;
98(3):
1591 - 1599.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Baude, C. Bleasdale, Y. Dalezios, P. Somogyi, and T. Klausberger
Immunoreactivity for the GABAA Receptor {alpha}1 Subunit, Somatostatin and Connexin36 Distinguishes Axoaxonic, Basket, and Bistratified Interneurons of the Rat Hippocampus
Cereb Cortex,
September 1, 2007;
17(9):
2094 - 2107.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Spampanato and I. Mody
Spike Timing of Lacunosom-Moleculare Targeting Interneurons and CA3 Pyramidal Cells During High-Frequency Network Oscillations In Vitro
J Neurophysiol,
July 1, 2007;
98(1):
96 - 104.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. H. Gittis and S. du Lac
Firing Properties of GABAergic Versus Non-GABAergic Vestibular Nucleus Neurons Conferred by a Differential Balance of Potassium Currents
J Neurophysiol,
June 1, 2007;
97(6):
3986 - 3996.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. M. Wilson, D. A. Dombeck, M. Diaz-Rios, R. M. Harris-Warrick, and R. M. Brownstone
Two-Photon Calcium Imaging of Network Activity in XFP-Expressing Neurons in the Mouse
J Neurophysiol,
April 1, 2007;
97(4):
3118 - 3125.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L.-Y. Fu and A. N. van den Pol
GABA excitation in mouse hilar neuropeptide Y neurons
J. Physiol.,
March 1, 2007;
579(2):
445 - 464.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. W. Bagnall, R. J. Stevens, and S. du Lac
Transgenic Mouse Lines Subdivide Medial Vestibular Nucleus Neurons into Discrete, Neurochemically Distinct Populations
J. Neurosci.,
February 28, 2007;
27(9):
2318 - 2330.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Travers, K Herman, J Yoo, and S. Travers
Taste Reactivity and Fos Expression in GAD1-EGFP Transgenic Mice
Chem Senses,
February 1, 2007;
32(2):
129 - 137.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. Dumitriu, R. Cossart, J. Huang, and R. Yuste
Correlation Between Axonal Morphologies and Synaptic Input Kinetics of Interneurons from Mouse Visual Cortex
Cereb Cortex,
January 1, 2007;
17(1):
81 - 91.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. Schoffnegger, B. Heinke, C. Sommer, and J. Sandkuhler
Physiological properties of spinal lamina II GABAergic neurons in mice following peripheral nerve injury
J. Physiol.,
December 15, 2006;
577(3):
869 - 878.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. I. Verbny, F. Erdelyi, G. Szabo, and M. I. Banks
Properties of a Population of GABAergic Cells in Murine Auditory Cortex Weakly Excited by Thalamic Stimulation
J Neurophysiol,
December 1, 2006;
96(6):
3194 - 3208.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. J. Lawrence, F. Saraga, J. F. Churchill, J. M. Statland, K. E. Travis, F. K. Skinner, and C. J. McBain
Somatodendritic Kv7/KCNQ/M Channels Control Interspike Interval in Hippocampal Interneurons.
J. Neurosci.,
November 22, 2006;
26(47):
12325 - 12338.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. Y. Sun and L. E. Dobrunz
Presynaptic kainate receptor activation is a novel mechanism for target cell-specific short-term facilitation at schaffer collateral synapses.
J. Neurosci.,
October 18, 2006;
26(42):
10796 - 10807.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. Halabisky, F. Shen, J. R. Huguenard, and D. A. Prince
Electrophysiological Classification of Somatostatin-Positive Interneurons in Mouse Sensorimotor Cortex
J Neurophysiol,
August 1, 2006;
96(2):
834 - 845.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. L. Torborg, A. P. Berg, B. W. Jeffries, D. A. Bayliss, and C. J. McBain
TASK-like conductances are present within hippocampal CA1 stratum oriens interneuron subpopulations.
J. Neurosci.,
July 12, 2006;
26(28):
7362 - 7367.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. R. Gibson, A. F. Bartley, and K. M. Huber
Role for the Subthreshold Currents ILeak and IH in the Homeostatic Control of Excitability in Neocortical Somatostatin-Positive Inhibitory Neurons
J Neurophysiol,
July 1, 2006;
96(1):
420 - 432.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Wang, A. G. Teschemacher, J. F. R. Paton, and S. Kasparov
Mechanism of nitric oxide action on inhibitory GABAergic signaling within the nucleus tractus solitarii
FASEB J,
July 1, 2006;
20(9):
1537 - 1539.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. W. Williams and B. N. Smith
Rapid inhibition of neural excitability in the nucleus tractus solitarii by leptin: implications for ingestive behaviour
J. Physiol.,
June 1, 2006;
573(2):
395 - 412.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Ma, H. Hu, A. S. Berrebi, P. H. Mathers, and A. Agmon
Distinct subtypes of somatostatin-containing neocortical interneurons revealed in transgenic mice.
J. Neurosci.,
May 10, 2006;
26(19):
5069 - 5082.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. J. Lawrence, J. M. Statland, Z. M. Grinspan, and C. J. McBain
Cell type-specific dependence of muscarinic signalling in mouse hippocampal stratum oriens interneurones
J. Physiol.,
February 1, 2006;
570(3):
595 - 610.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. J. Dougherty, M. A. Sawchuk, and S. Hochman
Properties of Mouse Spinal Lamina I GABAergic Interneurons
J Neurophysiol,
November 1, 2005;
94(5):
3221 - 3227.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Wu, R. Kawakami, Y. Shinohara, M. Fukaya, K. Sakimura, M. Mishina, M. Watanabe, I. Ito, and R. Shigemoto
Target-Cell-Specific Left-Right Asymmetry of NMDA Receptor Content in Schaffer Collateral Synapses in {epsilon}1/NR2A Knock-Out Mice
J. Neurosci.,
October 5, 2005;
25(40):
9213 - 9226.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. Somogyi and T. Klausberger
Defined types of cortical interneurone structure space and spike timing in the hippocampus
J. Physiol.,
January 1, 2005;
562(1):
9 - 26.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. C. Jung, A. D. Mehta, E. Aksay, R. Stepnoski, and M. J. Schnitzer
In Vivo Mammalian Brain Imaging Using One- and Two-Photon Fluorescence Microendoscopy
J Neurophysiol,
November 1, 2004;
92(5):
3121 - 3133.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. Heinke, R. Ruscheweyh, L. Forsthuber, G. Wunderbaldinger, and J. Sandkuhler
Physiological, neurochemical and morphological properties of a subgroup of GABAergic spinal lamina II neurones identified by expression of green fluorescent protein in mice
J. Physiol.,
October 1, 2004;
560(1):
249 - 266.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Alkondon, E. F. R. Pereira, P. Yu, E. Z. Arruda, L. E. F. Almeida, P. Guidetti, W. P. Fawcett, M. T. Sapko, W. R. Randall, R. Schwarcz, et al.
Targeted Deletion of the Kynurenine Aminotransferase II Gene Reveals a Critical Role of Endogenous Kynurenic Acid in the Regulation of Synaptic Transmission via {alpha}7 Nicotinic Receptors in the Hippocampus
J. Neurosci.,
May 12, 2004;
24(19):
4635 - 4648.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. A. DeFazio, S. Heger, S. R. Ojeda, and S. M. Moenter
Activation of A-Type {gamma}-Aminobutyric Acid Receptors Excites Gonadotropin-Releasing Hormone Neurons
Mol. Endocrinol.,
December 1, 2002;
16(12):
2872 - 2891.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. A. Oliva Jr, T. T. Lam, and J. W. Swann
Distally Directed Dendrotoxicity Induced by Kainic Acid in Hippocampal Interneurons of Green Fluorescent Protein-Expressing Transgenic Mice
J. Neurosci.,
September 15, 2002;
22(18):
8052 - 8062.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
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]
|
 |
|

|
 |

|
 |
 
M. D. McEchron, A. P. Weible, and J. F. Disterhoft
Aging and Learning-Specific Changes in Single-Neuron Activity in CA1 Hippocampus During Rabbit Trace Eyeblink Conditioning
J Neurophysiol,
October 1, 2001;
86(4):
1839 - 1857.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
V. Ramirez-Amaya, I. Balderas, J. Sandoval, M. L. Escobar, and F. Bermudez-Rattoni
Spatial Long-Term Memory Is Related to Mossy Fiber Synaptogenesis
J. Neurosci.,
September 15, 2001;
21(18):
7340 - 7348.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
X. Jin, P. H. Mathers, G. Szabo, Z. Katarova, and A. Agmon
Vertical Bias in Dendritic Trees of Non-pyramidal Neocortical Neurons Expressing GAD67-GFP In Vitro
Cereb Cortex,
July 1, 2001;
11(7):
666 - 678.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|