Patterns of synaptic connections in the visual system are remarkably precise. These connections dictate the receptive field properties of individual visual neurons and ultimately determine the quality of visual perception. Spontaneous neural activity is necessary for the development of various receptive field properties and visual feature maps. In recent years, attention has shifted to understanding the mechanisms by which spontaneous activity in the developing retina, lateral geniculate nucleus, and visual cortex instruct the axonal and dendritic refinements that give rise to orderly connections in the visual system. Axon guidance cues and a growing list of other molecules, including immune system factors, have also recently been implicated in visual circuit wiring. A major goal now is to determine how these molecules cooperate with spontaneous and visually evoked activity to give rise to the circuits underlying precise receptive field tuning and orderly visual maps.

The orientation selectivity of cells in ferret primary visual cortex was studied during normal development and in animals deprived of vision or of visual cortical activity. In normal animals from the age when visual responses were first recorded (postnatal day 23) through postnatal week 5, only about 25% of cells showed orientation-selective responses. By postnatal week 7, cortical responses had matured to an adult-like state, with approximately 75% of cells clearly selective for orientation. This development of orientation selectivity was not merely a reflection of the development of cortical cell responsiveness: at all ages studied, there was no correlation between responsiveness and selectivity. Infusion of TTX into visual cortex to silence neuronal activity completely blocked the maturation of orientation selectivity. Visual deprivation by bilateral lid suture impaired but did not completely block the normal development of orientation selectivity. We conclude that the maturation of orientation-selective responses in ferret primary visual cortex requires cortical neuronal activity, and that normal development requires visually driven activity.

The development of orientation preference maps was studied in ferret primary visual cortex using chronic optical imaging of intrinsic signals. The emergence and maturation of the maps were examined over time in single animals. The earliest age at which cortical domains selectively responsive to particular stimulus orientations were observed varied considerably between individuals, from postnatal day 31 to 36. In all cases, the earliest maps seen were low-contrast, with regions of orientation-specific activity that were difficult to distinguish from noise. These early maps matured over a period of several days into the high-contrast, patchy maps typical of adult animals. The structure of the orientation maps was remarkably constant over time. The indistinct features in the earliest maps were always patches of the same sizes and shapes and at the same locations as in the maps obtained in subsequent recording sessions. Details of the more mature maps, including the relative intensities of individual iso-orientation domains, were also constant from one recording session to another over periods of several weeks. The patterning of iso-orientation domains in ferret primary visual cortex thus is established early in development and remains stable over time, unaffected by either normal visual experience or the anatomical rearrangements of geniculocortical afferents into eye-specific domains.