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The Journal of Neuroscience, July 6, 2005, 25(27):6322-6328; doi:10.1523/JNEUROSCI.1405-05.2005

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Cellular/Molecular
Cooperative Activation of D₁ and D₂ Dopamine Receptors Enhances a Hyperpolarization-Activated Inward Current in Layer I Interneurons

JianPing Wu and John J. Hablitz

Department of Neurobiology and Civitan International Research Center, University of Alabama at Birmingham, Birmingham, Alabama 35294

Layer I of the neocortex comprises axonal processes from widespread regions of the brain and a unique population of GABAergic interneurons. Dopamine is known to directly depolarize layer I interneurons, but the underlying mechanism is unclear. Using whole-cell recording techniques in neocortical brain slices, we have examined how dopamine increases excitability of layer I interneurons in postnatal day 7-11 rats. Dopamine (30 µM) caused a 10 mV depolarization of layer I neurons. Paradoxically, neither the D₁-like receptor agonist 6-chloro-2,3,4,5-tetrahydro-1-phenyl-1H-3-benzazepine hydrobromide (SKF81297 (1-10 µM) nor the D₂-like agonist quinpirole (10 µM) produced a significant depolarization. Depolarization was observed when SKF81297and quinpirole were coapplied. When G-protein subunits were included in the recording pipette, D₁ but not D₂ agonists depolarized layer I neurons. Bath application of 4-ethylphenylamino-1,2-dimethyl-6-methylaminopyrimidinium chloride, a specific blocker of inwardly rectifying hyperpolarization-activated current (I_h) channels, hyperpolarized the neurons and occluded the action of dopamine. Voltage-clamp analysis demonstrated that dopamine increased the amplitude and shifted the voltage dependence of activation of I_h. These results indicate that I_h contributes to the resting potential of layer I interneurons and is subject to modulation by dopamine.

Key words: neocortex; dopamine; layer I; interneuron; modulation; I_h

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Received April 11, 2005; revised May 17, 2005; accepted May 24, 2005.

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