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Journal of Neuroscience, Vol 16, 572-585, Copyright © 1996 by Society for Neuroscience
Excitatory actions of norepinephrine on multiple classes of hippocampal CA1 interneurons
DE Bergles, VA Doze, DV Madison and SJ Smith
Department of Molecular and Cellular Physiology, Beckman Center for Molecular and Genetic Medicine, Stanford University School of Medicine, California 94305-5426, USA.
Norepinephrine (NE) causes an increase in the frequency of inhibitory
postsynaptic potentials in CA1 pyramidal neurons in vitro. The possibility
that this increase in tonic inhibition is caused by an excitatory effect on
inhibitory interneurons was investigated through whole-cell recordings from
pyramidal cells and both whole-cell and cell- attached patch recordings
from visualized interneurons in acute slices of rat hippocampus. Adrenergic
agonists caused a large increase in the frequency and amplitude of
spontaneous IPSCs recorded from pyramidal cells in the presence of
ionotropic glutamate receptor blockers, but they had no effect on either
the frequency or the amplitude of action potential-independent miniature
IPSCs recorded in tetrodotoxin. This effect was mediated primarily by an
alpha adrenoceptor, although a slight beta adrenoceptor-dependent increase
in IPSCs was also observed. NE caused interneurons located in all strata to
depolarize and begin firing action potentials. Many of these cells had
axons that ramified throughout the stratum pyramidale, suggesting that they
are responsible for the IPSCs observed in pyramidal neurons. This
depolarization was also mediated by an alpha adrenoceptor and was blocked
by a selective alpha 1- but not a selective alpha 2-adrenoceptor
antagonist. However, a slight beta adrenoceptor-dependent depolarization
was detected in those interneurons that displayed time-dependent inward
rectification. In the presence of a beta antagonist, NE induced an inward
current that reversed near the predicted K+ equilibrium potential and was
not affected by changes in intracellular Cl- concentration. In the presence
of an alpha 1 antagonist, NE induced an inwardly rectifying current at
potentials negative to approximately -70 mV that did not reverse (between
-130 and -60 mV), characteristics similar to the
hyperpolarization-activated current (lh). However, the depolarizing action
of NE is attributable primarily to the alpha 1 adrenoceptor- mediated
decrease in K+ conductance and not the beta adrenoceptor- dependent
increase in lh. These results provide evidence that NE increases action
potential-dependent IPSCs in pyramidal neurons by depolarizing surrounding
inhibitory interneurons. This potent excitatory action of NE on multiple
classes of hippocampal interneurons may contribute to the NE-induced
decrease in the spontaneous activity of pyramidal neurons and the
antiepileptic effects of NE observed in vivo.
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77(6):
3013 - 3020.
[Abstract]
[Full Text]
[PDF]
|
|
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16(23):
7566 - 7573.
[Abstract]
[Full Text]
[PDF]
|
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