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The Journal of Neurophysiology Vol. 82 No. 4 October 1999, pp. 1895-1901
Copyright ©1999 by the American Physiological Society
Neuroscience Center, Louisiana State University Medical Center, New Orleans, Louisiana 70112
Magee, Jeffrey C. and
Michael Carruth.
Dendritic Voltage-Gated Ion Channels Regulate the Action
Potential Firing Mode of Hippocampal CA1 Pyramidal Neurons. J. Neurophysiol. 82: 1895-1901, 1999. The
role of dendritic voltage-gated ion channels in the generation of
action potential bursting was investigated using whole cell patch-clamp
recordings from the soma and dendrites of CA1 pyramidal neurons located
in hippocampal slices of adult rats. Under control conditions somatic
current injections evoked single action potentials that were associated
with an afterhyperpolarization (AHP). After localized application of
4-aminopyridine (4-AP) to the distal apical dendritic arborization, the
same current injections resulted in the generation of an
afterdepolarization (ADP) and multiple action potentials. This burst
firing was not observed after localized application of 4-AP to the
soma/proximal dendrites. The dendritic 4-AP application allowed
large-amplitude Na+-dependent action potentials, which were
prolonged in duration, to backpropagate into the distal apical
dendrites. No change in action potential backpropagation was seen with
proximal 4-AP application. Both the ADP and action potential bursting
could be inhibited by the bath application of nonspecific
concentrations of divalent Ca2+ channel blockers (NiCl and
CdCl). Ca2+ channel blockade also reduced the dendritic
action potential duration without significantly affecting spike
amplitude. Low concentrations of TTX (10-50 nM) also reduced the
ability of the CA1 neurons to fire in the busting mode. This effect was
found to be the result of an inhibition of backpropagating dendritic action potentials and could be overcome through the coordinated injection of transient, large-amplitude depolarizing current into the
dendrite. Dendritic current injections were able to restore the burst
firing mode (represented as a large ADP) even in the presence of high
concentrations of TTX (300-500 µM). These data suggest the role of
dendritic Na+ channels in bursting is to allow
somatic/axonal action potentials to backpropagate into the dendrites
where they then activate dendritic Ca2+ channels. Although
it appears that most Ca2+ channel subtypes are important in
burst generation, blockade of T- and R-type Ca2+ channels
by NiCl (75 µM) inhibited action potential bursting to a greater
extent than L-channel (10 µM nimodipine) or N-, P/Q-type (1 µM
-conotoxin MVIIC) Ca2+ channel blockade. This suggest
that the Ni-sensitive voltage-gated Ca2+ channels have the
most important role in action potential burst generation. In summary,
these data suggest that the activation of dendritic voltage-gated
Ca2+ channels, by large-amplitude backpropagating spikes,
provides a prolonged inward current that is capable of generating an
ADP and burst of multiple action potentials in the soma of CA1
pyramidal neurons. Dendritic voltage-gated ion channels profoundly
regulate the processing and storage of incoming information in CA1
pyramidal neurons by modulating the action potential firing mode from
single spiking to burst firing.
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