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The Journal of Neuroscience, May 1, 1998, 18(9):3386-3403

GABAergic Cells Are the Major Postsynaptic Targets of Mossy Fibers in the Rat Hippocampus

László Acsády1, 2, Anita Kamondi1, Attila Sík2, Tamás Freund2, and György Buzsáki1

1 Center for Molecular and Behavioral Neuroscience, Rutgers, The State University of New Jersey, Newark, New Jersey 07102, and 2 Institute of Experimental Medicine, Hungarian Academy of Sciences, H-1450 Budapest, Hungary

Dentate granule cells communicate with their postsynaptic targets by three distinct terminal types. These include the large mossy terminals, filopodial extensions of the mossy terminals, and smaller en passant synaptic varicosities. We examined the postsynaptic targets of mossy fibers by combining in vivo intracellular labeling of granule cells, immunocytochemistry, and electron microscopy. Single granule cells formed large, complex "mossy" synapses on 11-15 CA3 pyramidal cells and 7-12 hilar mossy cells. In contrast, GABAergic interneurons, identified with immunostaining for substance P-receptor, parvalbumin, and mGluR1a-receptor, were selectively innervated by very thin (filopodial) extensions of the mossy terminals and by small en passant boutons in both the hilar and CA3 regions. These terminals formed single, often perforated, asymmetric synapses on the cell bodies, dendrites, and spines of GABAergic interneurons. The number of filopodial extensions and small terminals was 10 times larger than the number of mossy terminals. These findings show that in contrast to cortical pyramidal neurons, (1) granule cells developed distinct types of terminals to affect interneurons and pyramidal cells and (2) they innervated more inhibitory than excitatory cells. These findings may explain the physiological observations that increased activity of granule cells suppresses the overall excitability of the CA3 recurrent system and may form the structural basis of the target-dependent regulation of glutamate release in the mossy fiber system.

Key words: granule cell; mossy fiber; interneuron; spine; dentate gyrus; in vivo


Copyright © 1998 Society for Neuroscience  0270-6474/98/1893386-18$05.00/0


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I. Vida and M. Frotscher
A hippocampal interneuron associated with the mossy fiber system
PNAS, February 1, 2000; 97(3): 1275 - 1280.
[Abstract] [Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
K. M. Crowder, J. M. Gunther, T. A. Jones, B. D. Hale, H. Z. Zhang, M. R. Peterson, R. H. Scheller, C. Chavkin, and S. M. Bajjalieh
Abnormal neurotransmission in mice lacking synaptic vesicle protein 2A (SV2A)
PNAS, December 21, 1999; 96(26): 15268 - 15273.
[Abstract] [Full Text] [PDF]


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NeurologyHome page
R. Schmid, P. Tandon, C. E. Stafstrom, and G. L. Holmes
Effects of neonatal seizures on subsequent seizure-induced brain injury
Neurology, November 1, 1999; 53(8): 1754 - 1754.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
B. Kocsis, A. Bragin, and G. Buzsaki
Interdependence of Multiple Theta Generators in the Hippocampus: a Partial Coherence Analysis
J. Neurosci., July 15, 1999; 19(14): 6200 - 6212.
[Abstract] [Full Text] [PDF]


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J. Neurophysiol.Home page
S. Bolea, E. Avignone, N. Berretta, J. V. Sanchez-Andres, and E. Cherubini
Glutamate Controls the Induction of GABA-Mediated Giant Depolarizing Potentials Through AMPA Receptors in Neonatal Rat Hippocampal Slices
J Neurophysiol, May 1, 1999; 81(5): 2095 - 2102.
[Abstract] [Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
K. E. Vogt and R. A. Nicoll
Glutamate and gamma -aminobutyric acid mediate a heterosynaptic depression at mossy fiber synapses in the hippocampus
PNAS, February 2, 1999; 96(3): 1118 - 1122.
[Abstract] [Full Text] [PDF]


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J. Neurophysiol.Home page
P. S. Buckmaster and F. E. Dudek
In Vivo Intracellular Analysis of Granule Cell Axon Reorganization in Epileptic Rats
J Neurophysiol, February 1, 1999; 81(2): 712 - 721.
[Abstract] [Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
N. N. Urban and G. Barrionuevo
Active summation of excitatory postsynaptic potentials in hippocampal CA3 pyramidal neurons
PNAS, September 15, 1998; 95(19): 11450 - 11455.
[Abstract] [Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
L. P. Reagan, N. Gorovits, E. K. Hoskin, S. E. Alves, E. B. Katz, C. A. Grillo, G. G. Piroli, B. S. McEwen, and M. J. Charron
Localization and regulation of GLUTx1 glucose transporter in the hippocampus of streptozotocin diabetic rats
PNAS, February 27, 2001; 98(5): 2820 - 2825.
[Abstract] [Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
G. M. G. Shepherd, M. Raastad, and P. Andersen
General and variable features of varicosity spacing along unmyelinated axons in the hippocampus and cerebellum
PNAS, April 30, 2002; 99(9): 6340 - 6345.
[Abstract] [Full Text] [PDF]



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