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The Journal of Neurophysiology Vol. 82 No. 6 December 1999, pp. 2914-2935
Copyright ©1999 by the American Physiological Society
1Laboratories of Origin, Department of Neurobiology and Anatomy, W. M. Keck Center for the Neurobiology of Learning and Memory, The University of Texas-Houston Medical School, Houston, 77225; and 2Department of Electrical and Computer Engineering, Rice University, Houston, Texas 77251
Baxter, Douglas A.,
Carmen C. Canavier,
John W. Clark Jr., and
John H. Byrne.
Computational Model of the Serotonergic Modulation of Sensory
Neurons in Aplysia. J. Neurophysiol. 82: 2914-2935, 1999. Serotonergic modulation of the
sensory neurons that mediate the gill- and tail-withdrawal reflexes of
Aplysia is a useful model system for studies of neuronal
plasticity that contributes to learning and memory. The effects of
serotonin (5-HT) are mediated, in part, via two protein kinases
(protein kinase A, PKA, and protein kinase C, PKC), which in turn,
modulate at least four membrane currents, including a S
("serotonin-sensitive") K+ current
(IK,S), a steeply voltage-dependent
K+ current (IK-V), a slow
component of the Ca2+-activated K+ current
(IK,Ca-S), and a L-type Ca2+
current (ICa-L). The present study
investigated how the modulation of these currents altered the spike
duration and excitability of sensory neurons and examined the relative
contributions of PKA- and PKC-mediated effects to the actions of 5-HT.
A Hodgkin-Huxley type model was developed that described the ionic
conductances in the somata of sensory neurons. The descriptions of
these currents and their modulation were based largely on voltage-clamp
data from sensory neurons. Simulations were preformed with the program SNNAP (Simulator for Neural Networks and Action Potentials). The model
was sufficient to replicate empirical data that describes the membrane
currents, action potential waveform and excitability as well as their
modulation by application of 5-HT, increased levels of adenosine cyclic
monophosphate or application of active phorbol esters. In the model,
modulation of IK-V by PKC played a dominate
role in 5-HT-induced spike broadening, whereas the concurrent
modulation of IK,S and
IK,Ca-S by PKA primarily accounted for
5-HT-induced increases in excitability. Finally, simulations indicated
that a PKC-induced increase in excitability resulted from decreases of
IK,S and IK,Ca-S,
which was likely the indirect result of cross-talk between the PKC and
PKA systems. The results provide several predictions that warrant
additional experimental investigation and illustrate the importance of
considering indirect as well as direct effects of modulatory agents on
the modulation of membrane currents.
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