 |
||||
|
||||
|
||||
|
||||
|
||||
Previous Article | Next Article
The Journal of Neuroscience, November 15, 1999, 19(22):10082-10097
Total Number and Ratio of Excitatory and Inhibitory Synapses Converging onto Single Interneurons of Different Types in the CA1 Area of the Rat Hippocampus
Attila I. Gulyás, Manuel Megías, Zsuzsa Emri, and Tamás F. Freund Institute of Experimental Medicine, Hungarian Academy of Sciences, Budapest, H-1450, Hungary
The least known aspect of the functional architecture of hippocampal microcircuits is the quantitative distribution of synaptic inputs of identified cell classes. The complete dendritic trees of functionally distinct interneuron types containing parvalbumin (PV), calbindin D28k (CB), or calretinin (CR) were reconstructed at the light microscopic level to describe their geometry, total length, and laminar distribution. Serial electron microscopic reconstruction and postembedding GABA immunostaining was then used to determine the density of GABA-negative asymmetrical (excitatory) and GABA-positive symmetrical (inhibitory) synaptic inputs on their dendrites, somata, and axon initial segments. The total convergence and the distribution of excitatory and inhibitory inputs were then calculated using the light and electron microscopic data sets.
The three populations showed characteristic differences in dendritic morphology and in the density and distribution of afferent synapses. PV cells possessed the most extensive dendritic tree (4300 µm) and the thickest dendrites. CR cells had the smallest dendritic tree (2500 µm) and the thinnest shafts. The density of inputs as well as the total number of excitatory plus inhibitory synapses was several times higher on PV cells (on average, 16,294) than on CB (3839) or CR (2186) cells. The ratio of GABAergic inputs was significantly higher on CB (29.4%) and CR (20.71%) cells than on PV cells (6.4%). The density of inhibitory terminals was higher in the perisomatic region than on the distal dendrites.
These anatomical data are essential to understand the distinct behavior and role of these interneuron types during hippocampal activity patterns and represent fundamental information for modeling studies.
Key words: inhibitory neurons; GABA; synaptic convergence; dendrite geometry; serial reconstruction; 3D; electron microscopy; database for modeling
Copyright © 1999 Society for Neuroscience 0270-6474/99/192210082-16$05.00/0
This article has been cited by other articles:
J. Szabadics and I. Soltesz
Functional Specificity of Mossy Fiber Innervation of GABAergic Cells in the Hippocampus
J. Neurosci., April 1, 2009; 29(13): 4239 - 4251.
[Abstract] [Full Text] [PDF]
N. V. Povysheva, A. V. Zaitsev, D. C. Rotaru, G. Gonzalez-Burgos, D. A. Lewis, and L. S. Krimer
Parvalbumin-Positive Basket Interneurons in Monkey and Rat Prefrontal Cortex
J Neurophysiol, October 1, 2008; 100(4): 2348 - 2360.
[Abstract] [Full Text] [PDF]
G. Gonzalez-Burgos and D. A. Lewis
GABA Neurons and the Mechanisms of Network Oscillations: Implications for Understanding Cortical Dysfunction in Schizophrenia
Schizophr Bull, September 1, 2008; 34(5): 944 - 961.
[Abstract] [Full Text] [PDF]
L. L. Glickfeld, B. V. Atallah, and M. Scanziani
Complementary Modulation of Somatic Inhibition by Opioids and Cannabinoids
J. Neurosci., February 20, 2008; 28(8): 1824 - 1832.
[Abstract] [Full Text] [PDF]
X.-M. Ma, Y. Wang, F. Ferraro, R. E. Mains, and B. A. Eipper
Kalirin-7 Is an Essential Component of both Shaft and Spine Excitatory Synapses in Hippocampal Interneurons
J. Neurosci., January 16, 2008; 28(3): 711 - 724.
[Abstract] [Full Text] [PDF]
M. M. Behrens, S. S. Ali, D. N. Dao, J. Lucero, G. Shekhtman, K. L. Quick, and L. L. Dugan
Ketamine-Induced Loss of Phenotype of Fast-Spiking Interneurons Is Mediated by NADPH-Oxidase
Science, December 7, 2007; 318(5856): 1645 - 1647.
[Abstract] [Full Text] [PDF]
R. A. Koene and M. E. Hasselmo
First-In-First-Out Item Replacement in a Model of Short-Term Memory Based on Persistent Spiking
Cereb Cortex, August 1, 2007; 17(8): 1766 - 1781.
[Abstract] [Full Text] [PDF]
G. Kato, Y. Kawasaki, R.-R. Ji, and A. M. Strassman
Differential wiring of local excitatory and inhibitory synaptic inputs to islet cells in rat spinal lamina II demonstrated by laser scanning photostimulation
J. Physiol., May 1, 2007; 580(3): 815 - 833.
[Abstract] [Full Text] [PDF]
S. A. Hart, M. A. Snyder, T. Smejkalova, and C. S. Woolley
Estrogen Mobilizes a Subset of Estrogen Receptor-{alpha}-Immunoreactive Vesicles in Inhibitory Presynaptic Boutons in Hippocampal CA1
J. Neurosci., February 21, 2007; 27(8): 2102 - 2111.
[Abstract] [Full Text] [PDF]
A. Martin-Pena, A. Acebes, J.-R. Rodriguez, A. Sorribes, G. G. de Polavieja, P. Fernandez-Funez, and A. Ferrus
Age-Independent Synaptogenesis by Phosphoinositide 3 Kinase
J. Neurosci., October 4, 2006; 26(40): 10199 - 10208.
[Abstract] [Full Text] [PDF]
I. Oren, E. O. Mann, O. Paulsen, and N. Hajos
Synaptic Currents in Anatomically Identified CA3 Neurons during Hippocampal Gamma Oscillations In Vitro
J. Neurosci., September 27, 2006; 26(39): 9923 - 9934.
[Abstract] [Full Text] [PDF]
C. Gold, D. A. Henze, C. Koch, and G. Buzsaki
On the Origin of the Extracellular Action Potential Waveform: A Modeling Study
J Neurophysiol, May 1, 2006; 95(5): 3113 - 3128.
[Abstract] [Full Text] [PDF]
F. Saraga, L. Ng, and F. K. Skinner
Distal Gap Junctions and Active Dendrites Can Tune Network Dynamics
J Neurophysiol, March 1, 2006; 95(3): 1669 - 1682.
[Abstract] [Full Text] [PDF]
J. W. Kinney, C. N. Davis, I. Tabarean, B. Conti, T. Bartfai, and M. M. Behrens
A Specific Role for NR2A-Containing NMDA Receptors in the Maintenance of Parvalbumin and GAD67 Immunoreactivity in Cultured Interneurons
J. Neurosci., February 1, 2006; 26(5): 1604 - 1615.
[Abstract] [Full Text] [PDF]
J. H. Kotaleski, D. Plenz, and K. T. Blackwell
Using Potassium Currents to Solve Signal-to-Noise Problems in Inhibitory Feedforward Networks of the Striatum
J Neurophysiol, January 1, 2006; 95(1): 331 - 341.
[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]
J. F. Muller, F. Mascagni, and A. J. McDonald
Coupled Networks of Parvalbumin-Immunoreactive Interneurons in the Rat Basolateral Amygdala
J. Neurosci., August 10, 2005; 25(32): 7366 - 7376.
[Abstract] [Full Text] [PDF]
R. E. Campbell, S.-K. Han, and A. E. Herbison
Biocytin Filling of Adult Gonadotropin-Releasing Hormone Neurons in Situ Reveals Extensive, Spiny, Dendritic Processes
Endocrinology, March 1, 2005; 146(3): 1163 - 1169.
[Abstract] [Full Text] [PDF]
L. Wittner, L. Eross, S. Czirjak, P. Halasz, T. F. Freund, and Zs. Magloczky
Surviving CA1 pyramidal cells receive intact perisomatic inhibitory input in the human epileptic hippocampus
Brain, January 1, 2005; 128(1): 138 - 152.
[Abstract] [Full Text] [PDF]
E. O. Mann, C. A. Radcliffe, and O. Paulsen
Hippocampal gamma-frequency oscillations: from interneurones to pyramidal cells, and back
J. Physiol., January 1, 2005; 562(1): 55 - 63.
[Abstract] [Full Text] [PDF]
Y. Fujiwara-Tsukamoto, Y. Isomura, K. Kaneda, and M. Takada
Synaptic interactions between pyramidal cells and interneurone subtypes during seizure-like activity in the rat hippocampus
J. Physiol., June 15, 2004; 557(3): 961 - 979.
[Abstract] [Full Text] [PDF]
B. Rozsa, T. Zelles, E. S. Vizi, and B. Lendvai
Distance-Dependent Scaling of Calcium Transients Evoked by Backpropagating Spikes and Synaptic Activity in Dendrites of Hippocampal Interneurons
J. Neurosci., January 21, 2004; 24(3): 661 - 670.
[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]
K. Lamsa and T. Taira
Use-Dependent Shift From Inhibitory to Excitatory GABAA Receptor Action in SP-O Interneurons in the Rat Hippocampal CA3 Area
J Neurophysiol, September 1, 2003; 90(3): 1983 - 1995.
[Abstract] [Full Text] [PDF]
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]
B. S. Khakh, D. Gittermann, D. A. Cockayne, and A. Jones
ATP Modulation of Excitatory Synapses onto Interneurons
J. Neurosci., August 13, 2003; 23(19): 7426 - 7437.
[Abstract] [Full Text] [PDF]
C. J. Wierenga and W. J. Wadman
Excitatory Inputs to CA1 Interneurons Show Selective Synaptic Dynamics
J Neurophysiol, August 1, 2003; 90(2): 811 - 821.
[Abstract] [Full Text] [PDF]
D. S. Melchitzky and D. A. Lewis
Pyramidal Neuron Local Axon Terminals in Monkey Prefrontal Cortex: Differential Targeting of Subclasses of GABA Neurons
Cereb Cortex, May 1, 2003; 13(5): 452 - 460.
[Abstract] [Full Text] [PDF]
P. M. Baker, P. S. Pennefather, B. A. Orser, and F. K. Skinner
Disruption of Coherent Oscillations in Inhibitory Networks With Anesthetics: Role of GABAA Receptor Desensitization
J Neurophysiol, November 1, 2002; 88(5): 2821 - 2833.
[Abstract] [Full Text] [PDF]
M. Frerking and P. Ohliger-Frerking
AMPA Receptors and Kainate Receptors Encode Different Features of Afferent Activity
J. Neurosci., September 1, 2002; 22(17): 7434 - 7443.
[Abstract] [Full Text] [PDF]
T. Klausberger, J. D. B. Roberts, and P. Somogyi
Cell Type- and Input-Specific Differences in the Number and Subtypes of Synaptic GABAA Receptors in the Hippocampus
J. Neurosci., April 1, 2002; 22(7): 2513 - 2521.
[Abstract] [Full Text] [PDF]
G. Tamas, J. Szabadics, and P. Somogyi
Cell Type- and Subcellular Position-Dependent Summation of Unitary Postsynaptic Potentials in Neocortical Neurons
J. Neurosci., February 1, 2002; 22(3): 740 - 747.
[Abstract] [Full Text] [PDF]
M. Alkondon and E. X. Albuquerque
Nicotinic Acetylcholine Receptor alpha 7 and alpha 4beta 2 Subtypes Differentially Control GABAergic Input to CA1 Neurons in Rat Hippocampus
J Neurophysiol, December 1, 2001; 86(6): 3043 - 3055.
[Abstract] [Full Text] [PDF]
A. Acebes and A. Ferrus
Increasing the Number of Synapses Modifies Olfactory Perception in Drosophila
J. Neurosci., August 15, 2001; 21(16): 6264 - 6273.
[Abstract] [Full Text] [PDF]
F. Pouille and M. Scanziani
Enforcement of Temporal Fidelity in Pyramidal Cells by Somatic Feed-Forward Inhibition
Science, August 10, 2001; 293(5532): 1159 - 1163.
[Abstract] [Full Text] [PDF]
M. Bartos, I. Vida, M. Frotscher, J. R. P. Geiger, and P. Jonas
Rapid Signaling at Inhibitory Synapses in a Dentate Gyrus Interneuron Network
J. Neurosci., April 15, 2001; 21(8): 2687 - 2698.
[Abstract] [Full Text] [PDF]
L. Acsady, I. Katona, F. J. Martinez-Guijarro, G. Buzsaki, and T. F. Freund
Unusual Target Selectivity of Perisomatic Inhibitory Cells in the Hilar Region of the Rat Hippocampus
J. Neurosci., September 15, 2000; 20(18): 6907 - 6919.
[Abstract] [Full Text] [PDF]
D. L. Pettit and G. J. Augustine
Distribution of Functional Glutamate and GABA Receptors on Hippocampal Pyramidal Cells and Interneurons
J Neurophysiol, July 1, 2000; 84(1): 28 - 38.
[Abstract] [Full Text] [PDF]
|
|
|
|
 |
|