Introduction

In the adult visual system of higher mammals, information from the two eyes is kept separate through the early stages of visual processing. In the lateral geniculate nucleus (LGN), retinal ganglion cell axons from the two eyes project to separate eye-specific layers, and all LGN cells respond only to visual stimulation through one or the other eye. In primary visual cortex, LGN afferents serving the two eyes are segregated into eye-specific patches or stripes in cortical layer IV, forming the anatomical basis for ocular dominance columns (radial columns of cells throughout the depth of the cortex that tend to respond better to visual stimuli presented to one or the other eye). The development of this eye-specific segregation has been widely studied and is used extensively as a model system for the development of specific neuronal connections throughout the nervous system.

Historically, the development of eye-specific segregation was first studied using electrophysiological recordings in primary visual cortex. The pioneering work of Hubel and Wiesel showed that ocular dominance columns can be drastically modified by visual experience during a critical period early in development. Raising an animal with one eye closed (monocular deprivation) results in a primary visual cortex where cells can no longer respond to visual stimuli through the eye that was closed and are driven almost exclusively by the eye that had remained open (Hubel and Wiesel, 1970; Wiesel and Hubel, 1965). Transneuronal labeling with radioactive amino acids injected into one eye confirmed that this physiological response to monocular deprivation is associated with a profound reduction in the size of the geniculocortical projection from the closed eye (Hubel et al., 1977; Fig. 8.1). The first hints of the mechanisms underlying the development of eye-specific segregation came from comparing the results of monocular deprivation experiments with those of binocular deprivation experiments in which animals were raised with both eyes closed. In binocularly deprived animals, ocular dominance columns develop normally, with equal inputs to cortex from the two eyes (Wiesel and Hubel, 1965). This result, together with the fact that ocular dominance columns are present in some species at birth (Horton and Hocking, 1996; Rakic, 1976) clearly indicates that visual experience is not needed for the normal development of ocular dominance columns. Comparison of the results of monocular and binocular deprivation also suggests that development of ocular dominance columns might occur through a competitive process: when neuronal activity in the two eyes is equal, either because both eyes are open (as in normal animals) or both eyes are closed (as in binocularly deprived animals), normal ocular dominance columns form, whereas when the activity in the two eyes is not equal (in monocularly deprived animals), the more active eye has a competitive advantage in maintaining or expanding its LGN afferent connections to the cortex.

Figure 8.1..  

Ocular dominance columns from a normal monkey (left) and a monkey subjected to monocular deprivation during the critical period (right). In the normal monkey the ipsilateral eye was injected with [³H]proline, which was transported transneuronally through the LGN and can be seen as the white stripes in the figure. In the normal monkey, the ocular dominance columns from the injected eye (white stripes) and the uninjected eye (dark stripes) are equal in width. In the monocularly deprived monkey, [³H]proline was injected into the deprived eye. The white stripes, representing the ocular dominance columns from this deprived eye, are much narrower than those seen in the normal animal or than those from the nondeprived eye (dark stripes) in this animal. (From LeVay et al., 1980.)

This chapter will discuss some of the large number of experiments that have been performed since the groundbreaking work described above. Many of these experiments have been designed to answer the following questions: (1) does the development of eye-specific layers in the LGN follow the same rules as the development of ocular dominance columns? (2) Are there two separate stages of development, an initial phase in which ocular dominance columns are established and a second phase in which they are maintained or undergo plasticity? (3) Is the role of activity in the development and plasticity of eye-specific segregation instructive (patterns of activity actually guide the development of specific neuronal connections) or merely permissive (activity is necessary only to enable other developmental cues that guide connections)?