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The Journal of Neuroscience, January 11, 2006, 26(2):355-364; doi:10.1523/JNEUROSCI.3221-05.2006

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Development/Plasticity/Repair
Axonal Growth and Guidance Defects in Frizzled3 Knock-Out Mice: A Comparison of Diffusion Tensor Magnetic Resonance Imaging, Neurofilament Staining, and Genetically Directed Cell Labeling

Yanshu Wang,^1 * Jiangyang Zhang,^2,3 * Susumu Mori,^2,4 and Jeremy Nathans^1,5

¹Department of Molecular Biology and Genetics, Howard Hughes Medical Institute, ²Department of Radiology, Division of Nuclear Magnetic Resonance Research, ³Department of Biomedical Engineering, ⁴F. M. Kirby Research Center for Functional Brain Imaging, Kennedy Krieger Institute, and ⁵Departments of Neuroscience and Ophthalmology, Johns Hopkins University School of Medicine, Baltimore, Maryland 21205

Previous work has identified axonal outgrowth and/or guidance defects in the brain and spinal cord of prenatal Frizzled3 (Fz3)^–/– mice. To systematically explore the axonal defects in Fz3^–/– mice and to compare techniques for the global assessment of axon tracts in the developing mouse, we have analyzed wild-type and Fz3^–/– brains using (1) diffusion tensor magnetic resonance imaging (µDTI), (2) neurofilament staining, and (3) two genetically directed neuronal labeling methods. Confirming and extending the previous work of Wang et al. (2002), we find that the following structures/tracts are absent or greatly reduced in the Fz3^–/– brain: the anterior commissure, cerebral peduncle (corticospinal tract), corpus callosum, fornix, internal capsule (thalamocortical and corticothalamic tracts), stria medullaris, stria terminalis, and hippocampal commissure. An aberrant U-shaped fiber bundle immediately caudal to the optic tract connects the left and right sides of the Fz3^–/– thalamus and likely represents a default pathway for thalamic axons that failed to enter the internal capsule. At embryonic day 18, labeling of cortical pyramidal cells with a yellow fluorescent protein reporter reveals widespread fragmentation of axons with no apparent loss of pyramidal cell bodies. Fragmentation likely represents one stage in the process that normally eliminates stalled or mistargeted axons. This work demonstrates the usefulness of µDTI and genetically directed neuronal labeling for the analysis of nervous system defects in the mouse.

Key words: brain development; Frizzled3; axon guidance; fiber tracts; cre recombinase; YFP; knock-out mice; magnetic resonance imaging; diffusion tensor; axonal fragmentation

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Received Aug 2, 2005; revised November 9, 2005; accepted November 10, 2005.

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