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The Journal of Neuroscience, January 18, 2006, 26(3):862-872; doi:10.1523/JNEUROSCI.3385-05.2006

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Development/Plasticity/Repair
Requirement of Adenylate Cyclase 1 for the Ephrin-A5-Dependent Retraction of Exuberant Retinal Axons

Xavier Nicol, Aude Muzerelle, Jean Paul Rio, Christine Métin, and Patricia Gaspar

Institut National de la Santé et de la Recherche Médicale, U616, and University Paris 06, Hôpital Pitié Salpêtrière, Institut Féderatif Neurosciences, F-75013 Paris, France

The calcium-stimulated adenylate cyclase 1 (AC1) has been shown to be required for the refinement of the retinotopic map, but the mechanisms involved are not known. To investigate this question, we devised a retinotectal coculture preparation that reproduces the gradual acquisition of topographic specificity along the rostrocaudal axis of the superior colliculus (SC). Temporal retinal axons invade the entire SC at 4 d in vitro (DIV) and eliminate exuberant branches caudally by 12 DIV. Temporal and nasal axons form branches preferentially in the rostral or caudal SC, respectively. Retinal explants from AC1-deficient mice, AC1^brl/brl, maintain exuberant branches and lose the regional selectivity of branching when confronted with wild-type (WT) SC. Conversely, WT retinas correctly target AC1^brl/brl collicular explants. The effects of AC1 loss of function in the retina are mimicked by the blockade of ephrin-A5 signaling in WT cocultures. Video microscopic analyses show that AC1^brl/brl axons have modified responses to ephrin-A5: the collapse of the growth cones occurs, but the rearward movement of the axon is arrested. Our results demonstrate a presynaptic, cell autonomous role of AC1 in the retina and further indicate that AC1 is necessary to enact a retraction response of the retinal axons to ephrin-A5 during the refinement of the retinotopic map.

Key words: adenylate cyclase; ephrin; retinal map; axon branching; presynaptic mechanisms; knock-out mice; development; retraction; retinotectal; retina; growth cone; cAMP

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Received Aug 11, 2005; revised November 22, 2005; accepted November 23, 2005.

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