Asymmetrical Interhemispheric Connections Develop in Cat Visual Cortex after Early Unilateral Convergent Strabismus: Anatomy, Physiology, and Mechanisms

Abstract

In the mammalian primary visual cortex, the corpus callosum contributes to the unification of the visual hemifields that project to the two hemispheres. Its development depends on visual experience. When this is abnormal, callosal connections must undergo dramatic anatomical and physiological changes. However, data concerning these changes are sparse and incomplete. Thus, little is known about the impact of abnormal postnatal visual experience on the development of callosal connections and their role in unifying representation of the two hemifields. Here, the effects of early unilateral convergent strabismus (a model of abnormal visual experience) were fully characterized with respect to the development of the callosal connections in cat visual cortex, an experimental model for humans. Electrophysiological responses and 3D reconstruction of single callosal axons show that abnormally asymmetrical callosal connections develop after unilateral convergent strabismus, resulting from an extension of axonal branches of specific orders in the hemisphere ipsilateral to the deviated eye and a decreased number of nodes and terminals in the other (ipsilateral to the non-deviated eye). Furthermore this asymmetrical organization prevents the establishment of a unifying representation of the two visual hemifields. As a general rule, we suggest that crossed and uncrossed retino-geniculo-cortical pathways contribute successively to the development of the callosal maps in visual cortex.

Interhemispheric Connections between the Primary Visual Cortical Areas via the Anterior Commissure in Human Callosal Agenesis

“…Bilateral connections of the primary visual cortices through the corpus callosum were found to be asymmetrical in cats with induced early unilateral strabismus. Callosal terminals were found to be expanded in the primary visual cortex ipsilateral to the deviated (convergent) eye and almost normal in the contralateral hemisphere (Milleret and Houzel, 2001; Bui Quoc et al, 2012). Using DTI, we recently corroborated these results in humans with infantile strabismus in which we found that visual callosal pathways lack normal pruning (submitted).…”

Reorganization of Visual Callosal Connections Following Alterations of Retinal Input and Brain Damage

“…Reconstruction (3D) of single callosal axons shows that unilateral convergent strabismus triggers abnormalities in callosal connections (Bui Quoc et al, 2012). Specifically, strabismus induces an extension of interhemispheric terminals into the hemisphere ipsilateral to the deviated eye.…”

Does dominance of crossing retinal ganglion cells make the eyes cross? The temporal retina in the origin of infantile esotropia – a neuroanatomical and evolutionary analysis

“…Unilateral strabismus appeared to cause asymmetrical development of callosal connections (Quoc et al. 2011). This asymmetry possibly precludes the imposition of the central vertical meridian onto the ‘central vertical’, relayed directly from the lateral geniculate nucleus.…”

“…In cats, the callosal visual field subserving fusional convergence subtends twice the angle of the field subserving divergence, similar to the fusional convergence/divergence ratio in humans (Quoc et al. 2011). …”