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The Journal of Neuroscience, November 22, 2006, 26(47):12251-12259; doi:10.1523/JNEUROSCI.3693-06.2006

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Cellular/Molecular
Distinct Populations of Spinal Cord Lamina II Interneurons Expressing G-Protein-Gated Potassium Channels

Cheryl L. Marker,¹ Rafael Luján,² José Colón,¹ and Kevin Wickman¹

¹Department of Pharmacology, University of Minnesota, Minneapolis, Minnesota 55455, and ²Facultad de Medicina, Centro Regional de Investigaciones Biomédicas, Universidad de Castilla-La Mancha, 02006 Albacete, Spain

Correspondence should be addressed to Kevin Wickman, Department of Pharmacology, University of Minnesota, 6-120 Jackson Hall, 321 Church Street South East, Minneapolis, MN 55455. Email: wickm002{at}umn.edu

Noxious stimuli are sensed and carried to the spinal cord dorsal horn by A and C primary afferent fibers. Some of this input is relayed directly to supraspinal sites by projection neurons, whereas much of the input impinges on a heterogeneous population of interneurons in lamina II. Previously, we demonstrated that G-protein-gated inwardly rectifying potassium (GIRK) channels are expressed in lamina II of the mouse spinal cord and that pharmacologic ablation of spinal GIRK channels selectively blunts the analgesic effect of high but not lower doses of intrathecal µ-opioid receptor (MOR) agonists. Here, we report that GIRK channels formed by GIRK1 and GIRK2 subunits are found in two large populations of lamina II excitatory interneurons. One population displays relatively large apparent whole-cell capacitances and prominent GIRK-dependent current responses to the MOR agonist [D-Ala²,N-MePhe⁴,Gly-ol⁵] -enkephalin (DAMGO). A second population shows smaller apparent capacitance values and a GIRK-dependent response to the GABA_B receptor agonist baclofen, but not DAMGO. Ultrastructural analysis revealed that GIRK subunits preferentially label type I synaptic glomeruli, suggesting that GIRK-containing lamina II interneurons receive prominent input from C fibers, while receiving little input from A fibers. Thus, excitatory interneurons in lamina II of the mouse spinal cord can be subdivided into different populations based on the neurotransmitter system coupled to GIRK channels. This important distinction will afford a unique opportunity to characterize spinal nociceptive circuitry with defined physiological significance.

Key words: knock-out; opioid; GABA; baclofen; Kir3; substantia gelatinosa

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Received Aug. 24, 2006; revised Oct. 12, 2006; accepted Oct. 14, 2006.

Correspondence should be addressed to Kevin Wickman, Department of Pharmacology, University of Minnesota, 6-120 Jackson Hall, 321 Church Street South East, Minneapolis, MN 55455. Email: wickm002{at}umn.edu

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				T. Nakatsuka, T. Fujita, K. Inoue, and E. Kumamoto Activation of GIRK channels in substantia gelatinosa neurones of the adult rat spinal cord: a possible involvement of somatostatin J. Physiol., May 15, 2008; 586(10): 2511 - 2522. [Abstract] [Full Text] [PDF]

				H. G. Cruz, F. Berton, M. Sollini, C. Blanchet, M. Pravetoni, K. Wickman, and C. Luscher Absence and Rescue of Morphine Withdrawal in GIRK/Kir3 Knock-out Mice J. Neurosci., April 9, 2008; 28(15): 4069 - 4077. [Abstract] [Full Text] [PDF]

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