Synapse maturation is enhanced in the binocular region of the retinocollicular map prior to eye opening

In the developing visual system of mammals, retinal axons from the two eyes compete for postsynaptic partners. After eye opening, this process is regulated in part by homeostatically constrained competition for synaptic connectivity with target neurons. However, prior to eye opening, the functional and synaptic basis of binocular map development is unclear. To examine the role of binocular interactions during early stages of visual map development, we performed in vitro patch-clamp recordings from the superior colliculus (SC) of neonatal mice. Using newly designed slice preparations, we compared retinocollicular synapse development in the medial SC, which receives binocular input, and the lateral SC, which is predominantly monocular. Surprisingly, we found that at P6–7, when eye-specific segregation has just emerged, retinocollicular synapses were stronger and more mature and dendritic arbors were more elaborate in the medial than the lateral SC. Furthermore, monocular enucleation of the ipsilateral eye at P0 selectively reduced synaptic strength and dendritic branching in the medial SC and abolished the differences normally observed between the two slices at P6–7. This specifically implicates binocular interactions in the development of retinocollicular connectivity prior to eye opening. Our findings contrast with the predictions of a constrained-connectivity model of binocular map development and suggest instead that binocular competition prior to eye opening enhances retinocollicular synaptic strength and the morphological development of retino-recipient neurons.

Experience-dependent changes in NMDAR1 expression in the visual cortex of an animal model for amblyopia

When normal binocular visual experience is disrupted during postnatal development, it affects the maturation of cortical circuits and often results in the development of poor visual acuity known as amblyopia. Two main factors contribute to the development of amblyopia: visual deprivation and reduced binocular competition. We investigated the affect of these two amblyogenic factors on the expression of the NMDAR1 subunit in the visual cortex because activation of the NMDA receptor is a key mechanism of developmental neural plasticity. We found that disruption of binocular correlations by monocular deprivation promoted a topographic loss of NMDAR1 expression within the cortical representations of the central visual field and the vertical and horizontal meridians. In contrast, binocular deprivation, which primarily affects visual deprivation, promoted an increase in NMDAR1 expression throughout the visual cortex. These different changes in NMDAR1 expression can be described as topographic and homeostatic plasticity of NMDA expression, respectively. In addition, the changes in NMDA expression in the visual cortex provide a greater understanding of the neural mechanisms that underlie the development of amblyopia and the potential for visual recovery.

Does early enucleation affect the decussation pattern of alpha cells in the ferret?

Naturally occurring cell death has been hypothesized to sculpt various features of the organization of the mature visual pathways, including the recent proposal that the selective elimination of ganglion cells in the temporal retina shapes the formation of decussation patterns. Through a class-specific interocular competition, ganglion cells in the two temporal hemiretinae are selectively lost to produce the decussation patterns characteristic of each individual cell class (Leventhal et al., 1988). The present study has tested this hypothesis by asking whether the removal of one retina in newborn ferrets, which should disrupt binocular interactions at the level of the terminals, alters the decussation pattern of the alpha cells, a cell class that is entirely decussating in the normal adult ferret. Enucleation on the day of birth was found to increase the uncrossed projection by ≈50%, but not a single uncrossed alpha cell was found in the temporal retina. Either alpha cells never project ipsilaterally during development, or if they do, they cannot be rescued by early enucleation. While naturally occurring cell death plays many roles during development, creating the decussation pattern of the ferreth's alpha cell class via a binocular competition at the level of the targets is unlikely to be one of them.

Binocular competition affects the pattern and intensity of ocular activation columns in the visual cortex of cats

The effect of binocular competition on the development of ocular activation columns in areas 17 and 18 of cats was studied using the 14C-2-deoxyglucose (14C-2DG) technique to visualize the regions of cortex activated by one eye in cats reared with equal alternating monocular exposure (equal AME), unequal AME, or monocular deprivation (MD). The average size of the ocular activation columns of the eye stimulated during administration of 2DG was positively correlated with the competitive advantage during rearing. In order of increasing percentage of visual cortex activated, the eyes were (1) deprived eye of MD cats, (2) less experienced eye of unequal AME cats, (3) either eye of equal AME cats, (4) more experienced eye of unequal AME cats, and (5) experienced eye of MD cats. In area 17, the shape of the activation columns also was affected by the relative experience of the eye. The columns of the deprived eye of MD cats were widest in layer IV, where they were about the same width as those of the less experienced eye of the unequal AME cats; in other layers they were narrower, sometimes disappearing altogether. In contrast, the activation columns of the less experienced eye of the unequal AME cats were about the same width in all layers. These results suggest that when one eye is placed at a severe disadvantage and receives no patterned input, as in MD, both geniculocortical connections and intracortical connections may be disrupted, but when the disadvantage is less, as in unequal AME, only the geniculocortical connections are disrupted.Binocular competition also affected the intensity of activation within columns in area 17. We used video densitometry to determine ratios of the amount of label in cortical and thalamic structures. Both the ratio of label in area 17 to that in the lateral geniculate nucleus (LGN) and the ratio of label in the binocular segment of area 17 to that in the monocular segment were significantly less for the deprived eye of MD cats than for any other group. These results suggest that even within the smaller activation columns, deprived geniculocortical afferents are relatively ineffective at driving cortical cells. This finding is consistent with earlier reports that the synapses from the deprived pathway are both morphologically abnormal and reduced in number. The cortical labeling for the less experienced eye of the unequal AME cats and the experienced eye of the MD cats were also significantly less than that in equal AME cats. The decreased labeling for the experienced eye activation columns suggests that, in order to cover an abnormally large area, afferents representing the experienced eye must make fewer synaptic contacts within that area and that there are intrinsic limits on the number of synapses that one axon can make.