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Ephrins regulate the formation of terminal axonal arbors during the development of thalamocortical projections

Fanny Mann^1,*,, Christiane Peuckert², Frank Dehner², Renping Zhou³ and Jürgen Bolz²

¹ Institut National de la Santé et de la Recherche Médicale Unité 371, 18 avenue du Doyen Lépine, 69500 Bron, France
² Universität Jena, Institut Allgemeine Zoologie, Erberstrasse 1, 07743 Jena, Germany
³ Laboratory for Cancer Research, Department of Chemical Biology, College of Pharmacy, Rutgers University, Piscataway, NJ 08855, USA
^* Present address: University of Cambridge, Department of Anatomy, Downing Street, Cambridge CB2 3DY, UK

Author for correspondence (e-mail: fm222{at}cam.ac.uk)

Accepted 21 May 2002

The development of connections between thalamic afferents and their cortical target cells occurs in a highly precise manner. Thalamic axons enter the cortex through deep cortical layers, then stop their growth in layer 4 and elaborate terminal arbors specifically within this layer. The mechanisms that underlie target layer recognition for thalamocortical projections are not known. We compared the growth pattern of thalamic explants cultured on membrane substrates purified from cortical layer 4, the main recipient layer for thalamic axons, and cortical layer 5, a non-target layer. Thalamic axons exhibited a reduced growth rate and an increased branching density on their appropriate target membranes compared with non-target substrate. When confronted with alternating stripes of both membrane substrates, thalamic axons grew preferentially on their target membrane stripes. Enzymatic treatment of cortical membranes revealed that growth, branching and guidance of thalamic axons are independently regulated by attractive and repulsive cues differentially expressed in distinct cortical layers. These results indicate that multiple membrane-associated molecules collectively contribute to the laminar targeting of thalamic afferents. Furthermore, we found that interfering with the function of Eph tyrosine kinase receptors and their ligands, ephrins, abolished the preferential branching of thalamic axons on their target membranes, and that recombinant ephrin-A5 ligand elicited a branch-promoting activity on thalamic axons. We conclude that interactions between Eph receptors and ephrins mediate branch formation of thalamic axons and thereby may play a role in the establishment of layer-specific thalamocortical connections.

Key words: Wiring molecules, Cortical development, Thalamocortical projection, Ephrin, Eph receptor, Target recognition, Axon guidance, Branch formation, Mouse

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