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The Journal of Neuroscience, July 16, 2008, 28(29):7376-7386; doi:10.1523/JNEUROSCI.1135-08.2008

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Development/Plasticity/Repair
Functional Topography and Integration of the Contralateral and Ipsilateral Retinocollicular Projections of Ephrin-A^–/– Mice

Daniel J. Haustead,^1,2 Sherralee S. Lukehurst,¹ Genevieve T. Clutton,¹ Carole A. Bartlett,¹ Sarah A. Dunlop,^1,3 Catherine A. Arrese,¹ Rachel M. Sherrard,^4,5 and Jennifer Rodger^1,3

¹School of Animal Biology, ²Faculty of Medicine and Dentistry, ³Western Australian Institute for Medical Research, and ⁴School of Anatomy and Human Biology, University of Western Australia, Crawley, WA 6009, Australia, and ⁵Université Pierre et Marie Curie-Paris 6 and Centre National de la Recherche Scientifique, Unité Mixte de Recherche 7102, Neurobiologie des Processus Adaptatifs, 75005 Paris, France

Correspondence should be addressed to Dr. Jennifer Rodger, School of Animal Biology M092, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia. Email: jrodger{at}cyllene.uwa.edu.au

Topographically ordered projections are established by molecular guidance cues and refined by neuronal activity. Retinal input to a primary visual center, the superior colliculus (SC), is bilateral with a dense contralateral projection and a sparse ipsilateral one. Both projections are topographically organized, but in opposing anterior–posterior orientations. This arrangement provides functionally coherent input to each colliculus from the binocular visual field, supporting visual function. When guidance cues involved in contralateral topography (ephrin-As) are absent, crossed retinal ganglion cell (RGC) axons form inappropriate terminations within the SC. However, the organization of the ipsilateral projection relative to the abnormal contralateral input remains unknown, as does the functional capacity of both projections. We show here that in ephrin-A^–/– mice, the SC contains an expanded, diffuse ipsilateral projection. Electrophysiological recording demonstrated that topography of visually evoked responses recorded from the contralateral superior colliculus of ephrin-A^–/– mice displayed similar functional disorder in all genotypes, contrasting with their different degrees of anatomical disorder. In contrast, ipsilateral responses were retinotopic in ephrin-A2^–/– but disorganized in ephrin-A2/A5^–/– mice. The lack of integration of binocular input resulted in specific visual deficits, which could be reversed by occlusion of one eye. The discrepancy between anatomical and functional topography in both the ipsilateral and contralateral projections implies suppression of inappropriately located terminals. Moreover, the misalignment of ipsilateral and contralateral visual information in ephrin-A2/A5^–/– mice suggests a role for ephrin-As in integrating convergent visual inputs.

Key words: ephrin-A; topography; ipsilateral; retina; neuronal activity; visuomotor response; knock-out mouse

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Received Dec. 20, 2007; revised May 9, 2008; accepted June 3, 2008.

Correspondence should be addressed to Dr. Jennifer Rodger, School of Animal Biology M092, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia. Email: jrodger{at}cyllene.uwa.edu.au

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