Effect of sensory disuse on geniculate afferents to cat visual cortex

Abstract

In the kitten, as little as a week of monocular lid suture during early life causes a remarkable remodeling of the geniculocortical projections serving the deprived eye (Antonini & Stryker, 1993a, 1996). While the physiological effects of monocular deprivation have been shown to be due to competitive interactions between the projections serving the two eyes, it is not known whether these morphological changes are due to competitive interactions or to sensory disuse. We addressed this question by analyzing the morphology of geniculocortical arbors in kittens deprived of patterned vision by binocular lid suture for 1 week or 2 weeks ending at 6 weeks of age. Such deprivation would be expected to affect the afferents serving the two eyes equally, giving neither eye a competitive advantage. The arbors were anterogradely filled with Phaseolus lectin iontophoretically injected into lamina A of the lateral geniculate nucleus. The lectin was visualized immunohistochemically, and single geniculocortical arbors were serially reconstructed in three dimensions. Arbors reconstructed in binocularly deprived animals were compared with arbors serving the deprived and nondeprived eye in animals monocularly deprived by lid suture of one eye for a week and with arbors obtained in age-matched normal controls. Geniculocortical arbors in binocularly deprived animals did not suffer the drastic remodeling of the deprived arbors in monocularly deprived animals. Indeed, arbors in binocularly deprived animals were indistinguishable from arbors in normal kittens or nondeprived arbors in short-term monocularly deprived animals. These results support the notion that competitive mechanisms rather than sensory disuse are responsible for gross morphological remodeling of geniculocortical arbors.

Fig. 1

Computer reconstructions of PHA-L immunostained axonal arbors in area 17 in a normal P40 animal. Row A shows the arbors as originally reconstructed in the coronal plane, and row B shows the arbors from a surface view after a 90-deg rotation along the dorsoventral axis. The total length of the terminal arborization in layer IV has been computed distally to the small gap in the main axonal trunk, well visible in arbor NN22 (see Materials and methods). The arrowheads indicate the boundaries of the layer IV. VD and AP: ventrodorsal and anteroposterior direction along the lateral gyrus.

Fig. 2

Computer reconstructions of PHA-L immunostained geniculocortical arbors reconstructed in animals binocularly deprived for 1 week. Arbors are shown in coronal view (A), and in surface view (B). Abbreviations and symbols are as in Fig. 1.

Fig. 3

Computer reconstructions of PHA-L immunostained geniculocortical arbors reconstructed in animals binocularly deprived for 2 weeks. Arbors are shown in coronal view (A), and in surface view (B). Abbreviations and symbols are as in Fig. 1.

Fig. 4

Scattergram of the total length (A) and number of branch points (B) of the terminal arborization in layer IV (see Materials and methods) for arbors reconstructed in animals binocularly deprived for 1 and 2 weeks. For comparison, data from arbors serving the deprived (D) and nondeprived (ND) eye in animals deprived for 6/7 days (6/7dD) and from arbors reconstructed in normal (N) animals at P30/31 and P40 are also plotted.

Fig. 5

Density analysis of the terminal arborization in layer IV expressed as μm/1000 μm². (A) Scattergram of the maximal density of arbors reconstructed from 1-week and 2-week binocularly deprived animals, of arbors serving the deprived (D) and nondeprived (ND) eye in 6/7dD animals, and of arbors reconstructed in normal animals at P30/31 and P40. (B) Scattergram of the cumulative area of the standard patches (see Results) of the terminal arborizations in all groups of animals. Note that the values for one arbor in 1-week BD group and four deprived arbors in 6/7dD are equal to 0, as they did not reach the threshold density of 38 μm/1000 μm².