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The Journal of Neuroscience, October 8, 2003, 23(27):9059-9067

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Cellular/Molecular
Overexpression of a Hyperpolarization-Activated Cation Current (I_h) Channel Gene Modifies the Firing Activity of Identified Motor Neurons in a Small Neural Network

Ying Zhang,¹ Ricardo Oliva,² Günter Gisselmann,³ Hanns Hatt,³ John Guckenheimer,² and Ronald M. Harris-Warrick¹

Departments of ¹Neurobiology and Behavior, and ²Mathematics, Cornell University, Ithaca, New York 14853, and ³Department of Cell Physiology, Ruhr University Bochum, D-44780 Bochum, Germany

The hyperpolarization-activated cation current (I_h) is widely distributed in excitable cells. I_h plays important roles in regulation of cellular excitability, rhythmic activity, and synaptic function. We previously showed that, in pyloric dilator (PD) neurons of the stomatogastric ganglion (STG) of spiny lobsters, I_h can be endogenously upregulated to compensate for artificial overexpression of the Shal transient potassium channel; this maintains normal firing properties of the neuron despite large increases in potassium current. To further explore the function of I_h in the pyloric network, we injected cRNA of PAIH, a lobster gene that encodes I_h, into rhythmically active PD neurons. Overexpression of PAIH produced a fourfold increase in I_h, although with somewhat different biophysical properties than the endogenous current. Compared with the endogenous I_h, the voltage for half-maximal activation of the PAIH-evoked current was depolarized by 10 mV, and its activation kinetics were significantly faster. This increase in I_h did not affect the expression of I_A or other outward currents. Instead, it significantly altered the firing properties of the PD neurons. Increased I_h depolarized the minimum membrane potential of the cell, reduced the oscillation amplitude, decreased the time to the first spike, and increased the duty cycle and number of action potentials per burst. We used both dynamic-clamp experiments, injecting the modeled PAIH currents into PD cells in a functioning STG, and a theoretical model of a two-cell network to demonstrate that the increased I_h was sufficient to cause the observed changes in the PD activity.

Key words: I_h; I_A; STG; computational modeling; gene expression; neuronal network

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Received June 24, 2003; revised July 29, 2003; accepted August 1, 2003.

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