Functional Specificity of Long-Range Intrinsic and Interhemispheric Connections in the Visual Cortex of Strabismic Cats

Abstract

The development of both long-range intracortical and interhemispheric connections depends on visual experience. Previous experiments showed that in strabismic but not in normal cats, clustered horizontal axon projections preferentially connect cell groups activated by the same eye. This indicates that there is selective stabilization of fibers between neurons exhibiting correlated activity. Extending these experiments, we investigated in strabismic cats: (1) whether tangential connections remain confined to columns of similar orientation preference within the subsystems of left and right eye domains; and (2) whether callosal connections also extend predominantly between neurons activated by the same eye and preferring similar orientations. To this end, we analyzed in strabismic cats the topographic relationships between orientation preference domains and both intrinsic and callosal connections of area 17. Red and green latex microspheres were injected into monocular iso-orientation domains identified by optical imaging of intrinsic signals. Additionally, domains sharing the ocular dominance and orientation preference of the neurons at the injection sites were visualized by 2-deoxyglucose (2-DG) autoradiography. Quantitative analysis revealed that 56% of the retrogradely labeled cells within the injected area 17 and 60% of the transcallosally labeled neurons were located in the 2-DG-labeled iso-orientation domains. This indicates: (1) that strabismus does not interfere with the tendency of long-range horizontal fibers to link predominantly neurons of similar orientation preference; and (2) that the selection mechanisms for the stabilization of callosal connections are similar to those that are responsible for the specification of the tangential intrinsic connections.

The layout of orientation and ocular dominance domains in area 17 of strabismic cats

“…These resembled closely the activation patterns revealed with 2-DG after similar stimulation conditions (Schmidt et al, 1997b). As expected for strabismic animals (e.g.…”

“…Consist-ent with previous electrophysiological and anatomical experiments (i.e. Hubel & Wiesel, 1965;Löwel & Singer, 1992;König et al, 1993;Schmidt et al, 1997b) our optical imaging data thus give no indication of a disadvantage of the deviated compared with the non-deviated eye in divergently squinting cats (Figs 1-4).…”

“…Iso-orientation columns were visualized with [ 14 C]2-DG autoradiography after binocular stimulation with contours of either horizontal (BO1) or vertical orientation (BO2) and ocular dominance columns were labelled with the transneuronal tracer [ 3 H]proline injected in either the squinting (BO1) or the non-squinting eye (BO2). The 2-DG labelled binocular orientation domains extended in columns through the entire cortical thickness and resembled those of autoradiographically labelled binocular iso-orientation domains of normal cats (Albus, 1979;Singer, 1981;Löwel & Singer, 1993a;Schmidt et al, 1997b). As in normals, the orientation domains appeared as beaded continuous bands indicating that orientation columns of the left and the right eye are not isolated from each other (Fig.…”

“…Distinction between these alternatives is of particular importance because of the squint-induced restriction of tangential connections to domains of like ocular preference (Löwel & Singer, 1992). In normal and strabismic animals, these connections link selectively columns with similar orientation preference (Gilbert & Wiesel, 1989;Schmidt et al, 1997b) and have been assigned an important role in the development of iso-orientation maps. If orientation maps remain continuous across the segregated ocular dominance domains of strabismic animals this implies that tangential connections are not required for the maintenance of the sequence regularity of iso-orientation maps.…”

Visual interhemispheric transfer to areas 17 and 18 in cats with convergent strabismus

“…Therefore, our study reveals that functional characteristics of visual callosal transfer might be affected differentially by early strabismus, depending on the rule governing the connections subserving them. Based on a series of elegant experiments combining optical recording, deoxyglucose labelling and retrograde tracing, Schmidt et al (1997aSchmidt et al ( , 1997b concluded that long-range corticocortical connections ± intrahemispheric as well as interhemispheric ± are selected during development according to perceptual grouping criteria and thereafter link domains of similar ocularity or orientation selectivity. These connections are considered to be the substrate for long-range, stimulus-speci®c synchronization of visual responses, a phenomenon that is proposed to serve as a mechanism for dynamic tagging of visual responses, as belonging to neuronal assemblies (reviewed in Singer & Gray, 1995).…”