The Journal of Neuroscience, November 15, 1998, 18(22):9171-9180
Heterologous Expression of the Kv3.1 Potassium
Channel Eliminates Spike Broadening and the Induction of a Depolarizing
Afterpotential in the Peptidergic Bag Cell Neurons
Matthew D.
Whim and
Leonard K.
Kaczmarek
Department of Pharmacology, Yale University School of Medicine, New
Haven, Connecticut 06520-8066
The bag cell neurons of Aplysia are a cluster of
cells that control egg laying behavior. After brief synaptic
stimulation, they depolarize and fire spontaneously for up to 30 min.
During the first few seconds of this afterdischarge, the action
potentials of the bag cell neurons undergo pronounced broadening.
Single bag cell neurons in culture also show spike broadening in
response to repeated depolarizations. This broadening is
frequency-dependent and associated with the induction of a depolarizing
afterpotential lasting minutes. In some neurons the depolarizing
afterpotential is sufficient to trigger spontaneous firing. To test the
possibility that spike broadening during stimulation is required to
trigger the depolarizing afterpotential, we eliminated
frequency-dependent broadening by heterologous expression of the Kv3.1
potassium channel. This channel has rapid activation and deactivation
kinetics and no use-dependent inactivation. Expression of Kv3.1
prevented spike broadening and also eliminated the depolarizing
afterpotential. Measurements of the integral of calcium current during
voltage commands, which simulated the action potentials of the control neurons and those expressing Kv3.1, indicate that spike broadening produces up to a fivefold increase in calcium entry. Manipulations that
limit calcium entry during action potentials or chelation of
intracellular calcium using BAPTA AM prevented the induction of the
depolarizing afterpotential. We conclude that spike broadening is
essential for the induction of the depolarizing afterpotential probably
by regulating calcium influx and suggest that one of the physiological
roles of spike broadening may be to regulate long-term changes in
neuronal excitability.
Key words:
Kv3.1; depolarizing afterpotential; spike broadening; afterdischarge; long-term excitability; potassium channel; expression
vector
Copyright © 1998 Society for Neuroscience 0270-6474/98/18229171-10$05.00/0
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