 |
||||
|
||||
|
||||
|
||||
Previous Article | Next Article
The Journal of Neuroscience, September 1, 1998, 18(17):6790-6802
Dendrodendritic Inhibition in the Olfactory Bulb Is Driven by NMDA Receptors
Nathan E. Schoppa1, J. Mark Kinzie1, Yoshinori Sahara1, Thomas P. Segerson2, and Gary L. Westbrook1 1 Vollum Institute and 2 Department of Medicine, Oregon Health Sciences University, Portland, Oregon 97201
At many central excitatory synapses, AMPA receptors relay the electrical signal, whereas activation of NMDA receptors is conditional and serves a modulatory function. We show here quite a different role for NMDA receptors at dendrodendritic synapses between mitral and granule cells in the rat olfactory bulb. In whole-cell patch-clamp recordings in bulb slices, stimulation of mitral cells elicited slowly decaying, GABAA receptor-mediated reciprocal IPSCs that reflected prolonged GABA release from granule cells. Although granule cells had a normal complement of AMPA and NMDA receptors, the IPSC was completely blocked by the NMDA receptor antagonist D,L-AP-5, suggesting that NMDA receptor activation is an absolute requirement for dendrodendritic inhibition. The AMPA receptor antagonist 1,2,3,4-tetrahydro-6-nitro-2,3-dioxobenzo[f]quinoxaline-7-sulfonamide (NBQX) had no effect on IPSCs in the absence of extracellular magnesium but modestly reduced IPSCs in 1 mM magnesium, indicating that the primary effect of the AMPA receptor-mediated depolarization was to facilitate the unblocking of NMDA receptors. Granule cell voltage recordings indicated that effective spike stimulation in granule cells depended on the slow NMDA receptor kinetics. Granule cells also showed a pronounced delay between synaptic stimulation and action potential generation, suggesting that their intrinsic membrane properties underlie the ineffectiveness of brief AMPA receptor-mediated EPSPs. NMDA receptors also seem to have a central role in dendrodendritic inhibition in vivo, because intraperitoneal dizocilpine maleate (MK-801) injection in young adult rats resulted in disinhibition of mitral cells as measured by the generation of c-fos mRNA. The unique dependence of dendrodendritic inhibition on slow EPSPs generated by NMDA receptors suggests that olfactory information processing depends on long-lasting reciprocal and lateral inhibition.
Key words: olfactory bulb; dendrodendritic synapses; granule cell; mitral cell; AMPA receptor; NMDA receptor; GABA receptor; synaptic integration; dendrites
Copyright © 1998 Society for Neuroscience 0270-6474/98/18176790-13$05.00/0
This article has been cited by other articles:
Y. Tsuno, H. Kashiwadani, and K. Mori
Behavioral State Regulation of Dendrodendritic Synaptic Inhibition in the Olfactory Bulb
J. Neurosci., September 10, 2008; 28(37): 9227 - 9238.
[Abstract] [Full Text] [PDF]
V. M. Luna and N. E. Schoppa
GABAergic Circuits Control Input-Spike Coupling in the Piriform Cortex
J. Neurosci., August 27, 2008; 28(35): 8851 - 8859.
[Abstract] [Full Text] [PDF]
A. E. Chavez and J. S. Diamond
Diverse Mechanisms Underlie Glycinergic Feedback Transmission onto Rod Bipolar Cells in Rat Retina
J. Neurosci., July 30, 2008; 28(31): 7919 - 7928.
[Abstract] [Full Text] [PDF]
B. J. Maher and G. L. Westbrook
Co-Transmission of Dopamine and GABA in Periglomerular Cells
J Neurophysiol, March 1, 2008; 99(3): 1559 - 1564.
[Abstract] [Full Text] [PDF]
D. J. Brasier and D. E. Feldman
Synapse-Specific Expression of Functional Presynaptic NMDA Receptors in Rat Somatosensory Cortex
J. Neurosci., February 27, 2008; 28(9): 2199 - 2211.
[Abstract] [Full Text] [PDF]
A. M. McNamara, P. D. Magidson, C. Linster, D. A. Wilson, and T. A. Cleland
Distinct neural mechanisms mediate olfactory memory formation at different timescales
Learn. Mem., February 22, 2008; 15(3): 117 - 125.
[Abstract] [Full Text] [PDF]
R. Balu, R. T. Pressler, and B. W. Strowbridge
Multiple Modes of Synaptic Excitation of Olfactory Bulb Granule Cells
J. Neurosci., May 23, 2007; 27(21): 5621 - 5632.
[Abstract] [Full Text] [PDF]
J. B. Castro, K. R. Hovis, and N. N. Urban
Recurrent Dendrodendritic Inhibition of Accessory Olfactory Bulb Mitral Cells Requires Activation of Group I Metabotropic Glutamate Receptors
J. Neurosci., May 23, 2007; 27(21): 5664 - 5671.
[Abstract] [Full Text] [PDF]
T. Heinbockel, K. A. Hamilton, and M. Ennis
Group I Metabotropic Glutamate Receptors Are Differentially Expressed by Two Populations of Olfactory Bulb Granule Cells
J Neurophysiol, April 1, 2007; 97(4): 3136 - 3141.
[Abstract] [Full Text] [PDF]
R. Balu and B. W. Strowbridge
Opposing Inward and Outward Conductances Regulate Rebound Discharges in Olfactory Mitral Cells
J Neurophysiol, March 1, 2007; 97(3): 1959 - 1968.
[Abstract] [Full Text] [PDF]
D. De Saint Jan and G. L. Westbrook
Disynaptic Amplification of Metabotropic Glutamate Receptor 1 Responses in the Olfactory Bulb
J. Neurosci., January 3, 2007; 27(1): 132 - 140.
[Abstract] [Full Text] [PDF]
N. Laaris, A. Puche, and M. Ennis
Complementary Postsynaptic Activity Patterns Elicited in Olfactory Bulb by Stimulation of Mitral/Tufted and Centrifugal Fiber Inputs to Granule Cells
J Neurophysiol, January 1, 2007; 97(1): 296 - 306.
[Abstract] [Full Text] [PDF]
T. Heinbockel, N. Laaris, and M. Ennis
Metabotropic Glutamate Receptors in the Main Olfactory Bulb Drive Granule Cell-Mediated Inhibition
J Neurophysiol, January 1, 2007; 97(1): 858 - 870.
[Abstract] [Full Text] [PDF]
N. E. Schoppa
AMPA/Kainate Receptors Drive Rapid Output and Precise Synchrony in Olfactory Bulb Granule Cells
J. Neurosci., December 13, 2006; 26(50): 12996 - 13006.
[Abstract] [Full Text] [PDF]
V. Kapoor and N. N. Urban
Glomerulus-specific, long-latency activity in the olfactory bulb granule cell network.
J. Neurosci., November 8, 2006; 26(45): 11709 - 11719.
[Abstract] [Full Text] [PDF]
Z. Zhou, W. Xiong, A. V. Masurkar, W. R. Chen, and G. M. Shepherd
Dendritic Calcium Plateau Potentials Modulate Input-Output Properties of Juxtaglomerular Cells in the Rat Olfactory Bulb
J Neurophysiol, November 1, 2006; 96(5): 2354 - 2363.
[Abstract] [Full Text] [PDF]
R. F. Galan, N. Fourcaud-Trocme, G. B. Ermentrout, and N. N. Urban
Correlation-induced synchronization of oscillations in olfactory bulb neurons.
J. Neurosci., April 5, 2006; 26(14): 3646 - 3655.
[Abstract] [Full Text] [PDF]
S. Kim, B. H. Singer, and M. Zochowski
Changing roles for temporal representation of odorant during the oscillatory response of the olfactory bulb.
Neural Comput., April 1, 2006; 18(4): 794 - 816.
[Abstract] [Full Text] [PDF]
B. Bathellier, S. Lagier, P. Faure, and P.-M. Lledo
Circuit Properties Generating Gamma Oscillations in a Network Model of the Olfactory Bulb
J Neurophysiol, April 1, 2006; 95(4): 2678 - 2691.
[Abstract] [Full Text] [PDF]
R. C. Araneda and S. Firestein
Adrenergic enhancement of inhibitory transmission in the accessory olfactory bulb.
J. Neurosci., March 22, 2006; 26(12): 3292 - 3298.
[Abstract] [Full Text] [PDF]
M. J. Lehmkuhle, R. A. Normann, and E. M. Maynard
Trial-by-Trial Discrimination of Three Enantiomer Pairs by Neural Ensembles in Mammalian Olfactory Bulb
J Neurophysiol, March 1, 2006; 95(3): 1369 - 1379.
[Abstract] [Full Text] [PDF]
A. S. Ghatpande, K. Sivaraaman, and S. Vijayaraghavan
Store Calcium Mediates Cholinergic Effects on mIPSCs in the Rat Main Olfactory Bulb
J Neurophysiol, March 1, 2006; 95(3): 1345 - 1355.
[Abstract] [Full Text] [PDF]
L. J. Blakemore, M. Resasco, M. A. Mercado, and P. Q. Trombley
Evidence for Ca2+-permeable AMPA receptors in the olfactory bulb
Am J Physiol Cell Physiol, March 1, 2006; 290(3): C925 - C935.
[Abstract] [Full Text] [PDF]
J. M. Christie and G. L. Westbrook
Lateral excitation within the olfactory bulb.
J. Neurosci., February 22, 2006; 26(8): 2269 - 2277.
[Abstract] [Full Text] [PDF]
J. Vigh and H. von Gersdorff
Prolonged Reciprocal Signaling via NMDA and GABA Receptors at a Retinal Ribbon Synapse
J. Neurosci., December 7, 2005; 25(49): 11412 - 11423.
[Abstract] [Full Text] [PDF]
B. J. Maher and G. L. Westbrook
SK Channel Regulation of Dendritic Excitability and Dendrodendritic Inhibition in the Olfactory Bulb
J Neurophysiol, December 1, 2005; 94(6): 3743 - 3750.
[Abstract] [Full Text] [PDF]
S. B. Dietz and V. N. Murthy
Contrasting short-term plasticity at two sides of the mitral-granule reciprocal synapse in the mammalian olfactory bulb
J. Physiol., December 1, 2005; 569(2): 475 - 488.
[Abstract] [Full Text] [PDF]
A. Hayar, M. T. Shipley, and M. Ennis
Olfactory Bulb External Tufted Cells Are Synchronized by Multiple Intraglomerular Mechanisms
J. Neurosci., September 7, 2005; 25(36): 8197 - 8208.
[Abstract] [Full Text] [PDF]
E. Salcedo, C. Zhang, E. Kronberg, and D. Restrepo
Analysis of Training-Induced Changes in Ethyl Acetate Odor Maps Using a New Computational Tool to Map the Glomerular Layer of the Olfactory Bulb
Chem Senses, September 1, 2005; 30(7): 615 - 626.
[Abstract] [Full Text] [PDF]
V. Egger, K. Svoboda, and Z. F. Mainen
Dendrodendritic Synaptic Signals in Olfactory Bulb Granule Cells: Local Spine Boost and Global Low-Threshold Spike
J. Neurosci., April 6, 2005; 25(14): 3521 - 3530.
[Abstract] [Full Text] [PDF]
D. De Saint Jan and G. L. Westbrook
Detecting Activity in Olfactory Bulb Glomeruli with Astrocyte Recording
J. Neurosci., March 16, 2005; 25(11): 2917 - 2924.
[Abstract] [Full Text] [PDF]
P.-M. Lledo, G. Gheusi, and J.-D. Vincent
Information Processing in the Mammalian Olfactory System
Physiol Rev, January 1, 2005; 85(1): 281 - 317.
[Abstract] [Full Text] [PDF]
T. Heinbockel, P. Heyward, F. Conquet, and M. Ennis
Regulation of Main Olfactory Bulb Mitral Cell Excitability by Metabotropic Glutamate Receptor mGluR1
J Neurophysiol, November 1, 2004; 92(5): 3085 - 3096.
[Abstract] [Full Text] [PDF]
E. Enwere, T. Shingo, C. Gregg, H. Fujikawa, S. Ohta, and S. Weiss
Aging Results in Reduced Epidermal Growth Factor Receptor Signaling, Diminished Olfactory Neurogenesis, and Deficits in Fine Olfactory Discrimination
J. Neurosci., September 22, 2004; 24(38): 8354 - 8365.
[Abstract] [Full Text] [PDF]
I. G. Davison, J. D. Boyd, and K. R. Delaney
Dopamine Inhibits Mitral/Tufted-> Granule Cell Synapses in the Frog Olfactory Bulb
J. Neurosci., September 15, 2004; 24(37): 8057 - 8067.
[Abstract] [Full Text] [PDF]
S. Lagier, A. Carleton, and P.-M. Lledo
Interplay between Local GABAergic Interneurons and Relay Neurons Generates {gamma} Oscillations in the Rat Olfactory Bulb
J. Neurosci., May 5, 2004; 24(18): 4382 - 4392.
[Abstract] [Full Text] [PDF]
G. Pinato and J. Midtgaard
Regulation of Granule Cell Excitability by a Low-Threshold Calcium Spike in Turtle Olfactory Bulb
J Neurophysiol, November 1, 2003; 90(5): 3341 - 3351.
[Abstract] [Full Text] [PDF]
A. P. Davison, J. Feng, and D. Brown
Dendrodendritic Inhibition and Simulated Odor Responses in a Detailed Olfactory Bulb Network Model
J Neurophysiol, September 1, 2003; 90(3): 1921 - 1935.
[Abstract] [Full Text] [PDF]
V. Egger, K. Svoboda, and Z. F. Mainen
Mechanisms of Lateral Inhibition in the Olfactory Bulb: Efficiency and Modulation of Spike-Evoked Calcium Influx into Granule Cells
J. Neurosci., August 20, 2003; 23(20): 7551 - 7558.
[Abstract] [Full Text] [PDF]
F. Debarbieux, E. Audinat, and S. Charpak
Action Potential Propagation in Dendrites of Rat Mitral Cells In Vivo
J. Neurosci., July 2, 2003; 23(13): 5553 - 5560.
[Abstract] [Full Text] [PDF]
J. Cang and J. S. Isaacson
In Vivo Whole-Cell Recording of Odor-Evoked Synaptic Transmission in the Rat Olfactory Bulb
J. Neurosci., May 15, 2003; 23(10): 4108 - 4116.
[Abstract] [Full Text] [PDF]
J. M. Christie and G. L. Westbrook
Regulation of Backpropagating Action Potentials in Mitral Cell Lateral Dendrites by A-Type Potassium Currents
J Neurophysiol, May 1, 2003; 89(5): 2466 - 2472.
[Abstract] [Full Text] [PDF]
D. Friedman and B. W. Strowbridge
Both Electrical and Chemical Synapses Mediate Fast Network Oscillations in the Olfactory Bulb
J Neurophysiol, May 1, 2003; 89(5): 2601 - 2610.
[Abstract] [Full Text] [PDF]
J. S. Isaacson and H. Vitten
GABAB Receptors Inhibit Dendrodendritic Transmission in the Rat Olfactory Bulb
J. Neurosci., March 15, 2003; 23(6): 2032 - 2039.
[Abstract] [Full Text] [PDF]
G. Lowe
Inhibition of Backpropagating Action Potentials in Mitral Cell Secondary Dendrites
J Neurophysiol, July 1, 2002; 88(1): 64 - 85.
[Abstract] [Full Text] [PDF]
Q. Li, S. Clark, D. V. Lewis, and W. A. Wilson
NMDA Receptor Antagonists Disinhibit Rat Posterior Cingulate and Retrosplenial Cortices: A Potential Mechanism of Neurotoxicity
J. Neurosci., April 15, 2002; 22(8): 3070 - 3080.
[Abstract] [Full Text] [PDF]
M. Ennis, F.-M. Zhou, K. J. Ciombor, V. Aroniadou-Anderjaska, A. Hayar, E. Borrelli, L. A. Zimmer, F. Margolis, and M. T. Shipley
Dopamine D2 Receptor-Mediated Presynaptic Inhibition of Olfactory Nerve Terminals
J Neurophysiol, December 1, 2001; 86(6): 2986 - 2997.
[Abstract] [Full Text] [PDF]
P. Heyward, M. Ennis, A. Keller, and M. T. Shipley
Membrane Bistability in Olfactory Bulb Mitral Cells
J. Neurosci., July 15, 2001; 21(14): 5311 - 5320.
[Abstract] [Full Text] [PDF]
P.-A. Salin, P.-M. Lledo, J.-D. Vincent, and S. Charpak
Dendritic Glutamate Autoreceptors Modulate Signal Processing in Rat Mitral Cells
J Neurophysiol, March 1, 2001; 85(3): 1275 - 1282.
[Abstract] [Full Text] [PDF]
J. M. Christie, N. E. Schoppa, and G. L. Westbrook
Tufted Cell Dendrodendritic Inhibition in the Olfactory Bulb Is Dependent on NMDA Receptor Activity
J Neurophysiol, January 1, 2001; 85(1): 169 - 173.
[Abstract] [Full Text] [PDF]
T. W. Margrie, B. Sakmann, and N. N. Urban
Action potential propagation in mitral cell lateral dendrites is decremental and controls recurrent and lateral inhibition in the mammalian olfactory bulb
PNAS, December 14, 2000; (2000) 11523098.
[Abstract] [Full Text]
J. S. Isaacson
Mechanisms governing dendritic gamma -aminobutyric acid (GABA) release in the rat olfactory bulb
PNAS, December 14, 2000; (2000) 21445798.
[Abstract] [Full Text]
D. Friedman and B. W. Strowbridge
Functional Role of NMDA Autoreceptors in Olfactory Mitral Cells
J Neurophysiol, July 1, 2000; 84(1): 39 - 50.
[Abstract] [Full Text] [PDF]
B. Halabisky, D. Friedman, M. Radojicic, and B. W. Strowbridge
Calcium Influx through NMDA Receptors Directly Evokes GABA Release in Olfactory Bulb Granule Cells
J. Neurosci., July 1, 2000; 20(13): 5124 - 5134.
[Abstract] [Full Text] [PDF]
M. Sassoe-Pognetto and O. P. Ottersen
Organization of Ionotropic Glutamate Receptors at Dendrodendritic Synapses in the Rat Olfactory Bulb
J. Neurosci., March 15, 2000; 20(6): 2192 - 2201.
[Abstract] [Full Text] [PDF]
G. C. Carlson, M. T. Shipley, and A. Keller
Long-Lasting Depolarizations in Mitral Cells of the Rat Olfactory Bulb
J. Neurosci., March 1, 2000; 20(5): 2011 - 2021.
[Abstract] [Full Text] [PDF]
P. E. Castillo, A. Carleton, J.-D. Vincent, and P.-M. Lledo
Multiple and Opposing Roles of Cholinergic Transmission in the Main Olfactory Bulb
J. Neurosci., November 1, 1999; 19(21): 9180 - 9191.
[Abstract] [Full Text] [PDF]
G. Laurent
A Systems Perspective on Early Olfactory Coding
Science, October 22, 1999; 286(5440): 723 - 728.
[Abstract] [Full Text]
L. L. Stark and D. J. Perkel
Two-Stage, Input-Specific Synaptic Maturation in a Nucleus Essential for Vocal Production in the Zebra Finch
J. Neurosci., October 15, 1999; 19(20): 9107 - 9116.
[Abstract] [Full Text] [PDF]
H. Zheng, L. Kelly, L. M. Patterson, and H.-R. Berthoud
Effect of brain stem NMDA-receptor blockade by MK-801 on behavioral and Fos responses to vagal satiety signals
Am J Physiol Regulator
