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The Journal of Neuroscience, July 1, 2000, 20(13):4878-4884
Calcium-Dependent Persistent Facilitation of Spike
Backpropagation in the CA1 Pyramidal Neurons
Hiroshi
Tsubokawa1,
Stefan
Offermanns4,
Melvin
Simon4, and
Masanobu
Kano2, 3
1 National Institute for Physiological Sciences,
Okazaki 444-8585, Japan, 2 Core Research for Evolutional
Science and Technology, Japan Science Technology Corporation, Kawaguchi
332-0012, Japan, 3 Department of Physiology, Kanazawa
University School of Medicine, Kanazawa 920-8640, Japan, and
4 Division of Biology, California Institute of Technology,
Pasadena, California 91125
Sodium-dependent action potentials initiated near the soma are
known to backpropagate over the dendrites of CA1 pyramidal neurons in
an activity-dependent manner. Consequently, later spikes in a train
have smaller amplitude when recorded in the apical dendrites. We found
that depolarization and resultant Ca2+ influx into
dendrites caused a persistent facilitation of spike backpropagation.
Dendritic patch recordings were made from CA1 pyramidal neurons in
mouse hippocampal slices under blockade of fast excitatory and
inhibitory synaptic inputs. Trains of 10 backpropagating action
potentials induced by antidromic stimulation showed a clear decrement
in the amplitude of later spikes when recorded in the middle apical
dendrites. After several depolarizing current pulses, the amplitude of
later spikes increased persistently, and all spikes in a train became
almost equal in size. BAPTA (10 mM) contained in the
pipette or low-Ca2+ perfusing solution abolished
this depolarization-induced facilitation, indicating that
Ca2+ influx is required. This facilitation was
present in G q knock-out mice that lack the previously
reported muscarinic receptor-mediated enhancement of spike
backpropagation. Therefore, these two forms of facilitation are clearly
distinct in their intracellular mechanisms. Intracellular injection of
either calmodulin binding domain (100 µM) or
Ca2+/calmodulin-kinase II (CaMKII) inhibitor
281-301 (10 µM) blocked the depolarization-induced
facilitation. Bath application of a membrane-permeable CaMKII inhibitor
KN-93 (10 µM) also blocked the facilitation, but KN-92
(10 µM), an inactive isomer of KN-93, had no effect.
These results suggest that increases in
[Ca2+]i cause persistent facilitation
of spike backpropagation in the apical dendrite of CA1 pyramidal neuron
by CaMKII-dependent mechanisms.
Key words:
hippocampus; pyramidal neuron; dendrite; action
potential; backpropagation; Ca2+/calmodulin-dependent protein kinase II; neuronal excitability; neural plasticity; intracellular signaling
Copyright © 2000 Society for Neuroscience 0270-6474/00/20134878-07$05.00/0
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