An analysis of orientation and ocular dominance patterns in the visual cortex of cats and ferrets.

We report an analysis of orientation and ocular dominance maps that were recorded optically from area 17 of cats and ferrets. Similar to a recent study performed in primates (Obermayer & Blasdel, 1997), we find that 80% (for cats and ferrets) of orientation singularities that are nearest neighbors have opposite sign and that the spatial distribution of singularities deviates from a random distribution of points, because the average distances between nearest neighbors are significantly larger than expected for a random distribution. Orientation maps of normally raised cats and ferrets show approximately the same typical wavelength; however, the density of singularities is higher in ferrets than in cats. Also, we find the well-known overrepresentation of cardinal versus oblique orientations in young ferrets (Chapman & Bonhoeffer, 1998; Coppola, White, Fitzpatrick, & Purves, 1998) but only a weak, not quite significant overrepresentation of cardinal orientations in cats, as has been reported previously (Bonhoeffer & Grinvald, 1993). Orientation and ocular dominance slabs in cats exhibit a tendency of being orthogonal to each other (Hubener, Shoham, Grinvald, & Bonhoeffer, 1997), albeit less pronounced, as has been reported for primates (Obermayer & Blasdel, 1993). In chronic recordings from single animals, a decrease of the singularity density and an increase of the ocular dominance wavelength with age but no change of the orientation wavelengths were found. Orientation maps are compared with two pattern models for orientation preference maps: bandpass-filtered white noise and the field analogy model. Bandpass-filtered white noise predicts sign correlations between orientation singularities, but the correlations are significantly stronger (87% opposite sign pairs) than what we have found in the data. Also, bandpass-filtered noise predicts a deviation of the spatial distribution of singularities from a random dot pattern. The field analogy model can account for the structure of certain local patches but not for the whole orientation map. Differences between the predictions of the field analogy model and experimental data are smaller than what has been reported for primates (Obermayer & Blasdel, 1997), which can be explained by the smaller size of the imaged areas in cats and ferrets.

Cortical cell orientation selectivity fails to develop in the absence of ON-center retinal ganglion cell activity.

Neuronal activity is necessary for the normal development of visual cortical cell receptive fields. When neuronal activity is blocked, cortical cells fail to develop normal ocular dominance and orientation selectivity. Patterned activity has been shown to play an instructive, rather than merely permissive, role in the segregation of geniculocortical afferents into ocular dominance columns. To test whether normal patterns of activity are necessary to instruct the development of cortical orientation selectivity, we studied ferrets raised without ON-center retinal ganglion cell activity. The ON-center blockade was produced by daily intravitreal injections of DL-2-amino-4-phosphonobutyric acid (APB). Effects of this treatment on the development of orientation selectivity in primary visual cortex were assessed using extracellular electrode recordings and optical imaging. In animals raised with an ON-center blockade starting after visual cortical cells are visually driven but still poorly tuned for orientation, cortical cell responsivity was maintained, but no maturation of orientation selectivity was seen. No recovery of orientation tuning was seen in animals treated with APB during the normal period of orientation development and then allowed several months of development without treatment. These results suggest that patterns of neuronal activity carried in the separate ON- and OFF-center visual pathways are necessary for the development of orientation selectivity in visual cortical neurons of the ferret and that there is a critical period for this development.

Development of orientation preference in the mammalian visual cortex.

Recent experiments have studied the development of orientation selectivity in normal animals, visually deprived animals, and animals where patterns of neuronal activity have been altered. Results of these experiments indicate that orientation tuning appears very early in development, and that normal patterns of activity are necessary for its normal development. Visual experience is not needed for early development of orientation, but is crucial for maintaining orientation selectivity. Neuronal activity and vision thus seem to play similar roles in the development of orientation selectivity as they do in the development of eye-specific segregation in the visual system.

Intrinsic and environmental factors in the development of functional maps in cat visual cortex.

In the mammalian visual cortex, key neuronal response properties such as orientation preference and ocular dominance (OD) are mapped in an orderly fashion across the cortical surface. It has been known for some time that manipulating early postnatal visual experience can change the appearance of the OD map. Similar evidence for developmental plasticity of the orientation map has been scarce. We employed optical imaging of intrinsic signals to examine the contribution of intrinsic and environmental factors to the development of cortical maps, using the paradigms of strabismus, reverse occlusion and rearing in a single-orientation environment ('stripe-rearing'). For several weeks after induction of strabismus, the pattern of OD domains remained stable in young kittens. The isotropic magnification of the OD map matched the postnatal growth of the visual cortical surface during the same period. In reverse-occluded and in stripe-reared kittens, orientation preference maps obtained through the left and the right eye were very similar, although the two eyes had never shared any visual experience. We suggest that the geometry of functional maps in the visual cortex is intrinsically determined, while the relative strength of representation of different response properties can be modified through visual experience.

Development of orientation preference maps in area 18 of kitten visual cortex.

We investigated the development of orientation preference maps in the visual cortex of kittens by repeated optical imaging from the same animal. Orientation maps became detectable for the first time around postnatal day (P) 17 and improved continuously in strength unitl P30, the time at which their appearance became adultlike. During this developmental period the overall geometry of the maps remained unchanged, suggesting that the layout of the orientation map is specified prior to P17. Hence, before the visual cortex becomes susceptible to experience-dependent modifications its functional architecture is largely specified. This suggests that the initial development and layout of orientation preference maps are determined by intrinsic processes that are independent of visual experience. This conclusion is further supported by the result that orientation maps were well expressed at P24 in binocularly deprived kittens. Because the appearance of the first orientation-selective neurons and the subsequent development of orientation preference maps correlated well with the time course of the expression and refinement of clustered horizontal connections, we propose that these connections might contribute to the specification of orientation preference maps.

Orientation selectivity in pinwheel centers in cat striate cortex.

In primary visual cortex of higher mammals neurons are grouped according to their orientation preference, forming "pinwheels" around "orientation centers." Although the general structure of orientation maps is largely resolved, the microscopic arrangement of neuronal response properties in the orientation centers has remained elusive. The tetrode technique, enabling multiple single-unit recordings, in combination with intrinsic signal imaging was used to reveal the fine-grain structure of orientation maps in these locations. The results show that orientation centers represent locations where orientation columns converge containing normal, sharply tuned neurons of different orientation preference lying in close proximity.

Development of identical orientation maps for two eyes without common visual experience.

In the mammalian visual cortex, many neurons are driven binocularly and response properties such as orientation preference or spatial frequency tuning are virtually identical for the two eyes. A precise match of orientation is essential in order to detect disparity and is therefore a prerequisite for stereoscopic vision. It is not clear whether this match is accomplished by activity-dependent mechanisms together with the common visual experience normally received by the eyes, or whether the visual system relies on other, perhaps even innate, cues to achieve this task. Here we test whether visual experience is responsible for the match in a reverse-suturing experiment in which kittens were raised so that both eyes were never able to see at the same time. A comparison of the layout of the two maps formed under these conditions showed them to be virtually identical. Considering that the two eyes never had common visual experience, this indicates that correlated visual input is not required for the alignment of orientation preference maps.