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Journal of Neuroscience, Vol 15, 8011-8022, Copyright © 1995 by Society for Neuroscience
Two voltage-dependent K+ conductances with complementary functions in postsynaptic integration at a central auditory synapse
HM Brew and ID Forsythe
Department of Cell Physiology and Pharmacology, University of Leicester, United Kingdom.
The medial nucleus of the trapezoid body (MNTB) relays auditory information
important for sound source localization. MNTB neurons faithfully preserve
the temporal patterning of action potentials (APs) occurring in their
single giant input synapse, even at high frequencies. The aim of this work
was to examine the postsynaptic potassium conductances that shape the
transfer of auditory information across this glutamatergic synapse. We used
whole cell patch techniques to record from MNTB neurons in thin slices of
rat brainstem. Two types of potassium conductance were found which had a
strong influence on an MNTB neuron's postsynaptic response. A small low
voltage threshold current, Id, limited the response during each EPSP to a
single brief AP. Id was specifically blocked by dendrotoxin (DTX),
resulting in additional APs during the tail end of the EPSP. Thus DTX
degraded the temporal fidelity of synaptic transmission, since one
presynaptic AP then led to several postsynaptic APs. A second conductance
was a fast delayed rectifier with a high voltage activation threshold, that
rapidly repolarised APs and thus facilitated high frequency AP responses.
Together, these two conductances allow high frequency auditory information
to be passed accurately across the MNTB relay synapse and separately, such
conductances may perform analogous functions elsewhere in the nervous
system.
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[Abstract]
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[PDF]
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[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
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|
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|
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[Abstract]
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[PDF]
|
|
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|
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[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
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[Abstract]
[Full Text]
[PDF]
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|
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|
|
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11019 - 11025.
[Abstract]
[Full Text]
[PDF]
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22(16):
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[Abstract]
[Full Text]
[PDF]
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[Abstract]
[Full Text]
[PDF]
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[Abstract]
[Full Text]
[PDF]
|
|
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[Abstract]
[Full Text]
[PDF]
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[Abstract]
[Full Text]
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[Full Text]
[PDF]
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|
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21(10):
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[Full Text]
[PDF]
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|
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|
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|
|
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85(3):
1017 - 1026.
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[Full Text]
[PDF]
|
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21(4):
1160 - 1168.
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[Full Text]
[PDF]
|
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21(2):
485 - 494.
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[Full Text]
[PDF]
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20(24):
9162 - 9173.
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[Full Text]
[PDF]
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