Abstract

The visual system is characterized by precise retinotopic mapping of each eye, together with exquisitely matched binocular projections. In many species, the inputs that represent the eyes are segregated into ocular dominance columns in primary visual cortex (V1), whereas in rodents, this does not occur. Ten-m3, a member of the Ten-m/Odz/Teneurin family, regulates axonal guidance in the retinogeniculate pathway. Significantly, ipsilateral projections are expanded in the dorsal lateral geniculate nucleus and are not aligned with contralateral projections in Ten-m3 knockout (KO) mice. Here, we demonstrate the impact of altered retinogeniculate mapping on the organization and function of V1. Transneuronal tracing and c-fos immunohistochemistry demonstrate that the subcortical expansion of ipsilateral input is conveyed to V1 in Ten-m3 KOs: Ipsilateral inputs are widely distributed across V1 and are interdigitated with contralateral inputs into eye dominance domains. Segregation is confirmed by optical imaging of intrinsic signals. Single-unit recording shows ipsilateral, and contralateral inputs are mismatched at the level of single V1 neurons, and binocular stimulation leads to functional suppression of these cells. These findings indicate that the medial expansion of the binocular zone together with an interocular mismatch is sufficient to induce novel structural features, such as eye dominance domains in rodent visual cortex.

Highlights

  • A key organizing principle of the nervous system is topography

  • Our data demonstrate that deletion of Ten-m3 induces a medial expansion of the binocular zone and an interocular mismatch

  • This is associated with ocular segregation

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Summary

Introduction

A key organizing principle of the nervous system is topography. In the visual pathway, intrinsic guidance and activity-dependent mechanisms interact to generate a faithful representation of the sensory periphery (Huberman et al 2006, 2008; Cang et al 2008; Leamey et al 2009; Triplett et al 2009). The generation of a cohesive visual map requires the precise mapping of each retina as well as the visuotopic alignment of the inputs from the 2 eyes. This is first observed in the dorsal lateral geniculate nucleus (dLGN), where retinal inputs are segregated (Grubb et al 2003) but topographically in register (Malpeli and Baker 1975; Reese and Jeffery 1983). In carnivorans and primates visuotopically overlapping geniculocortical inputs representing the ipsilateral and contralateral eyes are typically segregated into ocular dominance columns (ODCs) (Hubel and Wiesel 1962, 1968, 1972; Wiesel et al 1974; Shatz et al 1977), whereas in rodents, no segregation is apparent.

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