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The Journal of Neuroscience, December 19, 2007, 27(51):13938-13948; doi:10.1523/JNEUROSCI.3055-07.2007

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Development/Plasticity/Repair
Topographic Specificity within Membranes of a Single Muscle Detected In Vitro

Srinivas Rao Chadaram,^1,2 Michael B. Laskowski,¹ and Roger D. Madison^2,3,4

¹WWAMI Medical Education Program and Department of Biological Sciences, University of Idaho, Moscow, Idaho 83843, Departments of ²Surgery and ³Neurobiology, Duke University Medical Center, Durham, North Carolina 27710, and ⁴Research Service of the Veterans Affairs Medical Center, Durham Veterans Affairs Medical Center, Durham, North Carolina 27705

Correspondence should be addressed to Dr. Michael B. Laskowski, WWAMI Medical Education Program, University of Idaho, P.O. Box 444207, Moscow, ID 83844-4207. Email: mlaskow{at}uidaho.edu

Spinal motor pools project to target muscles forming distinct rostrocaudal topographic maps during development and regeneration. To define the mechanisms underlying these neuromuscular maps we studied the preferential outgrowth of embryonic spinal cord neurites on muscle membranes from different axial positions and explored the role of ephrin A ligands. We found all five ephrin As (EphAs) expressed in serratus anterior, gluteus maximus and diaphragm muscles. In the diaphragm, four of the five ephrin As are expressed as a caudal to rostral gradient. When ephrin A function is disrupted in muscle membranes by deletion of glycosyl-phosphatidylinositol anchored ephrin A ligands with phosphatidylinositol-specific phospholipase C enzyme treatment or by blocking of ephrin A ligands with EphA fusion proteins, or by genetic manipulation leading to ephrin A2/A5 mutant mice, the spinal cord neurites loose their preference for the membranes of corresponding axial position; suggesting a significant role for ephrins in topographic choices made by growing motor neurons. To closely approximate topographic choices presented to embryonic neurites in vivo, neurites within the phrenic motor pool were challenged to make outgrowth choices on membranes of their normal target, the diaphragm muscle. We observed that neurites from rostral cervical segments (C₁ and C₂) prefer to grow on rostral diaphragm membranes; caudal cervical neurites (C₆–C₈) choose caudal diaphragm membranes; a transition of positional preference occurs at C₄ and this ability is lost in ephrin A2/A5 mutant mice. These results demonstrate for the first time topographical outgrowth of axons from within a motor pool onto a single target muscle in vitro.

Key words: diaphragm; neuromuscular; topography; muscle; ephrins; spinal cord; axon guidance

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Received July 5, 2007; revised Sept. 20, 2007; accepted Oct. 12, 2007.

Correspondence should be addressed to Dr. Michael B. Laskowski, WWAMI Medical Education Program, University of Idaho, P.O. Box 444207, Moscow, ID 83844-4207. Email: mlaskow{at}uidaho.edu

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