The brain’s visual cortex processes information concerning form, pattern, and motion within functional maps that reflect the layout of neuronal circuits. We analyzed functional maps of orientation preference in the ferret, tree shrew, and galago—three species separated since the basal radiation of placental mammals more than 65 million years ago—and found a common organizing principle. A symmetry-based class of models for the self-organization of cortical networks predicts all essential features of the layout of these neuronal circuits, but only if suppressive long-range interactions dominate development. We show mathematically that orientation-selective long-range connectivity can mediate the required interactions. Our results suggest that self-organization has canalized the evolution of the neuronal circuitry underlying orientation preference maps into a single common design.

Sensory experience begins when neural circuits in the cerebral cortex are still immature; however, the contribution of experience to cortical maturation remains unclear. In the visual cortex, the selectivity of neurons for oriented stimuli at the time of eye opening is poor and increases dramatically after the onset of visual experience. Here we investigate whether visual experience has a significant role in the maturation of orientation selectivity and underlying cortical circuits using two forms of deprivation: dark rearing, which completely eliminates experience, and binocular lid suture, which alters the pattern of sensory driven activity. Orientation maps were present in dark-reared ferrets, but fully mature levels of tuning were never attained. In contrast, only rudimentary levels of orientation selectivity were observed in lid-sutured ferrets. Despite these differences, horizontal connections in both groups were less extensive and less clustered than normal, suggesting that long-range cortical processing is not essential for the expression of orientation selectivity, but may be needed for the full maturation of tuning. Thus, experience is beneficial or highly detrimental to cortical maturation, depending on the pattern of sensory driven activity.

In both humans and experimental animals, the ability to perceive contours that are vertically or horizontally oriented is superior to the perception of oblique angles. There is, however, no consensus about the developmental origins or functional basis of this phenomenon. Here, we report the analysis of a large library of digitized scenes using image processing with orientation-sensitive filters. Our results show a prevalence of vertical and horizontal orientations in indoor, outdoor, and even entirely natural settings. Because visual experience is known to inf luence the development of visual cortical circuitry, we suggest that this real world anisotropy is related to the enhanced ability of humans and other animals to process contours in the cardinal axes, perhaps by stimulating the development of a greater amount of visual circuitry devoted to processing vertical and horizontal contours.Humans and other animals process information at or near the vertical and horizontal meridians more efficiently than information projected onto the retina at oblique angles. This phenomenon-called the ''oblique effect''-has been documented by differences in acuity, contrast sensitivity, orientation discrimination, and recognition rate (1, 2). In addition to humans, species as diverse as octopuses, goldfish, rats, cats, and chimpanzees show the oblique effect to some degree (2). Despite the prevalence of this perceptual bias, there is little or no consensus about how or why it occurs or what significance it has for human vision (see, for example, ref.3).Although contours in the visual environment obviously are distributed across the full range of orientations, it is possible that the visual system has been biased functionally and structurally by a predominance of visible contours near the cardinal axes. In fact, natural vistas have predictable frequency and chromatic characteristics (4, 5), and an earlier study using optical Fourier analysis has shown that a variety of scenes have anisotropic frequency spectra, with more power near the cardinal axes (6; see also ref. 7). Despite these intriguing reports, the distribution of oriented feature contours projected onto the retina by representative objects has never been determined in a way that would allow ready comparison of the distribution of orientations within and between different visual environments. Accordingly, we have examined a large number of real world scenes, taking advantage of recent advances in image analysis to measure the distribution of oriented projections that the visual system must process. METHODSTo ensure an unbiased selection of scenes, we employed two naive subjects to collect representative images. The images were obtained with an automatic digital camera while the subjects walked about in three different settings: (i) indoor environments at Duke University; (ii) outdoor environments on the Duke University campus; and (iii) natural environments at Duke University (different regions of the Duke Forest, which comprises a variety of completely undevelo...