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The Journal of Neuroscience, July 1, 2000, 20(13):5124-5134
Calcium Influx through NMDA Receptors Directly Evokes GABA
Release in Olfactory Bulb Granule Cells
Brian
Halabisky,
Daniel
Friedman,
Milan
Radojicic, and
Ben W.
Strowbridge
Department of Neurosciences, Case Western Reserve University,
Cleveland, Ohio 44106-4975
Recurrent inhibition in olfactory bulb mitral cells is mediated via
reciprocal dendrodendritic synapses with granule cells. Although
GABAergic granule cells express both NMDA and non-NMDA glutamate
receptors, dendrodendritic inhibition (DDI) relies on the activation of
NMDA receptors. Using whole-cell recordings from rat olfactory bulb
slices, we now show that olfactory NMDA receptors have a dual role;
they depolarize granule cell spines, and they provide a source of
calcium that can evoke GABA exocytosis. We demonstrate that exogenous
NMDA can trigger GABA release after blockade of voltage-dependent
calcium channels (VDCCs) with Cd. We also find that postsynaptic
depolarization alone can evoke GABA release via a separate mechanism
that relies on calcium influx through Cd-sensitive VDCCs. By
selectively manipulating postsynaptic responses in granule cells with
high-K or low-Na extracellular solutions, we show that endogenous
glutamate can elicit GABA release via both NMDA receptor- and
VDCC-dependent pathways. Finally, we find that blockade of Na
channels in granule cells with tetrodotoxin enhances DDI, presumably by
reducing the depolarization of granule cells during DDI and thereby
increasing the driving force for Ca entry through NMDA receptors. These
results provide evidence of a novel mechanism for evoked transmitter
release that depends on Ca influx through ionotropic receptors and
provides a new potential site for synaptic plasticity in the olfactory bulb.
Key words:
olfactory bulb; mitral cell; glutamate receptor; EPSP; NMDA receptor; recurrent inhibition
Copyright © 2000 Society for Neuroscience 0270-6474/00/20135124-11$05.00/0
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|

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|
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|

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|
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|

|
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|

|
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|
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|

|
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|
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|
 |
|

|
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|
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[Full Text]
|
 |
|

|
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|
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[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
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[Full Text]
[PDF]
|
 |
|

|
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|
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98(11):
6441 - 6446.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|

|