Development, Vol 125, Issue 6 995-1004, Copyright © 1998 by Company of Biologists

JOURNAL ARTICLES

The spatial relationships among cutaneous, muscle sensory and motoneuron axons during development of the chick hindlimb

MG Honig, PA Frase and SJ Camilli
Department of Anatomy and Neurobiology, University of Tennessee, College of Medicine, Memphis, Tennessee 38163, USA. mhonig@utmen1.utmem.edu

Previous studies have suggested that interactions with other axons are important in sensory axon pathfinding in the developing chick hindlimb. Yet the nature of these interactions remains unknown, in part because information about the spatial relationships among the different kinds of axons is lacking. To obtain this information, we combined retrograde axonal tracing with an immunofluorescent labelling approach that distinguishes between sensory and motoneuron axons. This allowed us to follow the trajectories of sensory axons having a known destination, while also identifying their neighbors. We found that as sensory and motoneuron axons meet in the spinal nerves and travel into the limb, sensory axons remain bundled together. The large bundles that are present proximally gradually split into smaller bundles as the axons course distally in the spinal nerves; more distally, some bundles join to again form large bundles. Younger, later-growing sensory axons appear to grow primarily along bundles of older sensory axons that grew out earlier. Starting from very proximal levels, axons projecting along an individual cutaneous nerve are found together in bundles that are situated in characteristic regions of each spinal nerve. Some of these bundles are initially interspersed with bundles of axons projecting along other nerves, thereby indicating that the initial position of a cutaneous axon in the spinal nerves does not strictly determine its subsequent trajectory. As they travel distally, bundles of axons projecting along one cutaneous nerve gradually join one another, becoming increasingly separated from axons having different destinations. In contrast, muscle sensory axons are situated adjacent to motoneuron axons innervating the same muscle for much of their course. This suggests that muscle sensory axons may be guided to the appropriate muscles by fasciculating along motoneuron axons. Taken together, the results show that sensory axons projecting along different nerves are different from one another and respond to cues in their environment to navigate through the spinal nerves and plexus. Thus, sensory neurons must be intrinsically specified with respect to their peripheral targets. Sensory axons appear to respond differentially to the axons they encounter, segregating from axons that project along different nerves and often growing with axons destined for the same nerve, suggesting that fasciculation may aid pathfinding.
CiteULike    Complore    Connotea    Del.icio.us    Digg    Reddit    Technorati    Twitter    What's this?

This article has been cited by other articles:

				B. W. Gallarda, D. Bonanomi, D. Muller, A. Brown, W. A. Alaynick, S. E. Andrews, G. Lemke, S. L. Pfaff, and T. Marquardt Segregation of Axial Motor and Sensory Pathways via Heterotypic Trans-Axonal Signaling Science, April 11, 2008; 320(5873): 233 - 236. [Abstract] [Full Text] [PDF]

				W. Guan, M. A. Puthenveedu, and M. L. Condic Sensory Neuron Subtypes Have Unique Substratum Preference and Receptor Expression before Target Innervation J. Neurosci., March 1, 2003; 23(5): 1781 - 1791. [Abstract] [Full Text] [PDF]

				A. Levinsson, H. Holmberg, J. Broman, M. Zhang, and J. Schouenborg Spinal Sensorimotor Transformation: Relation between Cutaneous Somatotopy and a Reflex Network J. Neurosci., September 15, 2002; 22(18): 8170 - 8182. [Abstract] [Full Text] [PDF]

				H.-H. Chen, J. W. Yip, A. F. R. Stewart, and E. Frank Differential expression of a transcription regulatory factor, the LIM domain only 4 protein Lmo4, in muscle sensory neurons Development, January 11, 2002; 129(21): 4879 - 4889. [Abstract] [Full Text] [PDF]

				G. Wang and S. A. Scott The "Waiting Period" of Sensory and Motor Axons in Early Chick Hindlimb: Its Role in Axon Pathfinding and Neuronal Maturation J. Neurosci., July 15, 2000; 20(14): 5358 - 5366. [Abstract] [Full Text] [PDF]

				J. C. Glover Development of Specific Connectivity Between Premotor Neurons and Motoneurons in the Brain Stem and Spinal Cord Physiol Rev, April 1, 2000; 80(2): 615 - 647. [Abstract] [Full Text] [PDF]

				S. Perez, S Rebelo, and D. Anderson Early specification of sensory neuron fate revealed by expression and function of neurogenins in the chick embryo Development, January 4, 1999; 126(8): 1715 - 1728. [Abstract] [PDF]