Journal of Neurophysiology, Vol 72, Issue 5 2167-2180, Copyright © 1994 by APS

ARTICLES

Evidence from simultaneous intracellular recordings in rat hippocampal slices that area CA3 pyramidal cells innervate dentate hilar mossy cells

H. E. Scharfman
Neurology Research Center, Helen Hayes Hospital, New York State Department of Health, West Haverstraw 10993-1195.

1. Simultaneous intracellular recordings of area CA3 pyramidal cells and dentate hilar "mossy" cells were made in rat hippocampal slices to test the hypothesis that area CA3 pyramidal cells excite mossy cells monosynaptically. Mossy cells and pyramidal cells were differentiated by location and electrophysiological characteristics. When cells were impaled near the border of area CA3 and the hilus, their identity was confirmed morphologically after injection of the marker Neurobiotin. 2. Evidence for monosynaptic excitation of a mossy cell by a pyramidal cell was obtained in 7 of 481 (1.4%) paired recordings. In these cases, a pyramidal cell action potential was followed immediately by a 0.40 to 6.75 (mean, 2.26) mV depolarization in the simultaneously recorded mossy cell (mossy cell membrane potentials, -60 to -70 mV). Given that pyramidal cells used an excitatory amino acid as a neurotransmitter (Cotman and Nadler 1987; Ottersen and Storm-Mathisen 1987) and recordings were made in the presence of the GABAA receptor antagonist bicuculline (25 microM), it is likely that the depolarizations were unitary excitatory postsynaptic potentials (EPSPs). 3. Unitary EPSPs of mossy cells were prone to apparent "failure." The probability of failure was extremely high (up to 0.72; mean = 0.48) if the effects of all presynaptic action potentials were examined, including action potentials triggered inadvertently during other spontaneous EPSPs of the mossy cell. Probability of failure was relatively low (as low as 0; mean = 0.24) if action potentials that occurred during spontaneous activity of the mossy cell were excluded. These data suggest that unitary EPSPs produced by pyramidal cells are strongly affected by concurrent synaptic inputs to the mossy cell. 4. Unitary EPSPs were not clearly affected by manipulation of the mossy cell's membrane potential. This is consistent with the recent report that area CA3 pyramidal cells innervate distal dendrites of mossy cells (Kunkel et al. 1993). Such a distal location also may contribute to the high incidence of apparent failures. 5. Characteristics of unitary EPSPs generated by pyramidal cells were compared with the properties of the unitary EPSPs produced by granule cells. In two slices, pyramidal cell and granule cell inputs to the same mossy cell were compared. In other slices, inputs to different mossy cells were compared. In all experiments, unitary EPSPs produced by granule cells were larger in amplitude but similar in time course to unitary EPSPs produced by pyramidal cells. Probability of failure was lower and paired-pulse facilitation more common among EPSPs triggered by granule cells.(ABSTRACT TRUNCATED AT 400 WORDS)

This article has been cited by other articles:

				J.-M. Mangin, A. Kunze, R. Chittajallu, and V. Gallo Satellite NG2 Progenitor Cells Share Common Glutamatergic Inputs with Associated Interneurons in the Mouse Dentate Gyrus J. Neurosci., July 23, 2008; 28(30): 7610 - 7623. [Abstract] [Full Text] [PDF]

				S. P. Schneider Local Circuit Connections Between Hamster Laminae III and IV Dorsal Horn Neurons J Neurophysiol, March 1, 2008; 99(3): 1306 - 1318. [Abstract] [Full Text] [PDF]

				M. P. Witter Intrinsic and extrinsic wiring of CA3: Indications for connectional heterogeneity Learn. Mem., November 15, 2007; 14(11): 705 - 713. [Abstract] [Full Text] [PDF]

				B. Nahir, C. Bhatia, and C. J. Frazier Presynaptic Inhibition of Excitatory Afferents to Hilar Mossy Cells J Neurophysiol, June 1, 2007; 97(6): 4036 - 4047. [Abstract] [Full Text] [PDF]

				A. L. Howard, A. Neu, R. J. Morgan, J. C. Echegoyen, and I. Soltesz Opposing Modifications in Intrinsic Currents and Synaptic Inputs in Post-Traumatic Mossy Cells: Evidence for Single-Cell Homeostasis in a Hyperexcitable Network J Neurophysiol, March 1, 2007; 97(3): 2394 - 2409. [Abstract] [Full Text] [PDF]

				A. M. Kerr and M. Capogna Unitary IPSPs enhance hilar mossy cell gain in the rat hippocampus J. Physiol., January 15, 2007; 578(2): 451 - 470. [Abstract] [Full Text] [PDF]

				S. B. Bausch and J. O. McNamara Contributions of Mossy Fiber and CA1 Pyramidal Cell Sprouting to Dentate Granule Cell Hyperexcitability in Kainic Acid-Treated Hippocampal Slice Cultures J Neurophysiol, December 1, 2004; 92(6): 3582 - 3595. [Abstract] [Full Text] [PDF]

				H. E. Scharfman, A. L. Sollas, R. E. Berger, and J. H. Goodman Electrophysiological Evidence of Monosynaptic Excitatory Transmission Between Granule Cells After Seizure-Induced Mossy Fiber Sprouting J Neurophysiol, October 1, 2003; 90(4): 2536 - 2547. [Abstract] [Full Text] [PDF]

				V. I. Dzhala and K. J. Staley Transition from Interictal to Ictal Activity in Limbic Networks In Vitro J. Neurosci., August 27, 2003; 23(21): 7873 - 7880. [Abstract] [Full Text] [PDF]

				S. B. Bausch and J. O. McNamara Synaptic Connections From Multiple Subfields Contribute to Granule Cell Hyperexcitability in Hippocampal Slice Cultures J Neurophysiol, December 1, 2000; 84(6): 2918 - 2932. [Abstract] [Full Text] [PDF]

				A. K. Shetty and D. A. Turner Fetal Hippocampal Grafts Containing CA3 Cells Restore Host Hippocampal Glutamate Decarboxylase-Positive Interneuron Numbers in a Rat Model of Temporal Lobe Epilepsy J. Neurosci., December 1, 2000; 20(23): 8788 - 8801. [Abstract] [Full Text] [PDF]

				H. E. SCHARFMAN Epileptogenesis in the Parahippocampal Region: Parallels with the Dentate Gyrus Ann. N.Y. Acad. Sci., June 1, 2000; 911(1): 305 - 327. [Abstract] [Full Text] [PDF]

				M. M. Okazaki, P. Molnar, and J. V. Nadler Recurrent Mossy Fiber Pathway in Rat Dentate Gyrus: Synaptic Currents Evoked in Presence and Absence of Seizure-Induced Growth J Neurophysiol, April 1, 1999; 81(4): 1645 - 1660. [Abstract] [Full Text] [PDF]

				Z. Xiang and T. H. Brown Complex Synaptic Current Waveforms Evoked in Hippocampal Pyramidal Neurons by Extracellular Stimulation of Dentate Gyrus J Neurophysiol, May 1, 1998; 79(5): 2475 - 2484. [Abstract] [Full Text] [PDF]

				A. M. Magarinos, J. M. G. Verdugo, and B. S. McEwen Chronic stress alters synaptic terminal structure in hippocampus PNAS, December 9, 1997; 94(25): 14002 - 14008. [Abstract] [Full Text] [PDF]

				N. Kogo and M. Ariel Membrane Properties and Monosynaptic Retinal Excitation of Neurons in the Turtle Accessory Optic System J Neurophysiol, August 1, 1997; 78(2): 614 - 627. [Abstract] [Full Text] [PDF]