Quantitative aspects of ionic conductance mechanisms contributing to firing pattern of motor cells mediating inking behavior in Aplysia californica

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Abstract
The release of ink occurs selectively to long-lasting stimuli. A good correspondence exists between the features of the behavior and the firing pattern of the ink motor cells since the initial synaptic input is ineffective in firing the ink gland motor neurons. The features of the firing pattern of these cells were attributed to a fast K+ current that shunts the initial excitatory input and a late buildup of synaptic input. These features were examined quantitatively using a kinetic model of the ink gland motor neurons. A modified Hodgkin-Huxley model was developed which includes 7 membrane currents: a fast inward Na+ current, a slow inward Ca2+ current, a fast outward K+ current, a slow (delayed) outward K+ current, a synaptic current, a leakage current and a capacitative current. The 3 ink gland motor neurons are electrically coupled to each other. The model includes the features of this electronic coupling. The Na+ current underlies the spike initiation; the delayed K+ current accounts for spike repolarization. The fast transient K+ current contributes to the repolarization process and slows the rate of rise of the membrane potential during the interspike interval. The slow Ca2+ current makes only a small contribution to the generation of the action potential, but contributes to the rise of the membrane potential during the interspike interval. A depolarizing current pulse to 1 ink gland motor neuron yields an initial rapid depolarization followed by a slower component, which after a several-second period results in a burst of action potentials. The activation and inactivation sequence of a fast transient K+ current contributes to the cell''s selective response to long-lasting depolarizing current pulses. If the suprathreshold current pulse is preceded by a small subthreshold pulse, spikes are elicited immediately with the application of the suprathreshold pulse, since the subthreshold pulse inactivates the transient outward current. The ink gland motor neurons show a selective response to long-lasting trains of synaptic input. A train of synaptic input causes an initial large depolarization, but the initial synaptic input is ineffective in firing the cell. A several-second silent period or pause results before an accelerating brust of spikes is produced. The fast transient K+ current shunts the initial synaptic input, preventing the cell from reaching spike threshold. Over a several-second period this current inactivates and the synaptic current is more effective in firing the cell. During the fast outward current inactivation, the synaptic current builds up and contributes to the accelerating burst of spikes. The results indicate the feasibility of quantitatively relating the biophysical features of individual neurons to the features of the behavior that those cells mediate.