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...

Eye position was recorded in different viewing conditions to assess whether the temporal and spatial characteristics of saccadic eye movements in different individuals are idiosyncratic. Our aim was to determine the degree to which oculomotor control is based on endogenous factors. A total of 15 naive subjects viewed five visual environments: (1) The absence of visual stimulation (i.e. a dark room); (2) a repetitive visual environment (i.e. simple textured patterns); (3) a complex natural scene; (4) a visual search task; and (5) reading text. Although differences in visual environment had significant effects on eye movements, idiosyncrasies were also apparent. For example, the mean fixation duration and size of an individual's saccadic eye movements when passively viewing a complex natural scene covaried significantly with those same parameters in the absence of visual stimulation and in a repetitive visual environment. In contrast, an individual's spatio-temporal characteristics of eye movements during active tasks such as reading text or visual search covaried together, but did not correlate with the pattern of eye movements detected when viewing a natural scene, simple patterns or in the dark. These idiosyncratic patterns of eye movements in normal viewing reveal an endogenous influence on oculomotor control. The independent covariance of eye movements during different visual tasks shows that saccadic eye movements during active tasks like reading or visual search differ from those engaged during the passive inspection of visual scenes.

We have measured the amount of cortical space activated by differently oriented gratings in 25 adult ferrets by optical imaging of intrinsic signal. On average, 7% more area of the exposed visual cortex was preferentially activated by vertical and horizontal contours than by contours at oblique angles. This anisotropy may ref lect the real-world prevalence of contours in the cardinal axes and could explain the greater sensitivity of many animals to vertical and horizontal stimuli.

Fetal alcohol syndrome is a major cause of learning and sensory deficits. These disabilities may result from disruption of neocortex development and plasticity. Alcohol exposure during the third trimester equivalent of human gestation may have especially severe and long-lasting consequences on learning and sensory processing, because this is when the functional properties and connectivity of neocortical neurons start to develop. To address this issue, we used the monocular deprivation model of neural plasticity, which shares many common mechanisms with learning. Ferrets were exposed to ethanol (3.5 mg/kg, i.p.) on alternate days for 3 weeks starting on postnatal day (P) 10. Animals were then monocularly deprived at the peak of ocular dominance plasticity after a prolonged alcohol-free period (15-20 d). Quantitative single-unit electrophysiology revealed that alcohol exposure disrupted ocular dominance plasticity while preserving robust visual responses. Moreover, optical imaging of intrinsic signals revealed that the reduction in visual cortex area driven by the deprived eye was much less pronounced in ethanol-treated than in control animals. Alcohol exposure starting at a later age (P20) did not disrupt ocular dominance plasticity, indicating that timing of exposure is crucial for the effects on visual plasticity. In conclusion, alcohol exposure during a brief period of development impairs ocular dominance plasticity at a later age. This model provides a novel approach to investigate the consequences of fetal alcohol exposure and should contribute to elucidate how alcohol disrupts neural plasticity.

Unilateral naris occlusion has long been the method of choice for effecting stimulus deprivation in studies of olfactory plasticity. A significant body of literature speaks to the myriad consequences of this manipulation on the ipsilateral olfactory pathway. Early experiments emphasized naris occlusion's deleterious and age-critical effects. More recent studies have focused on life-long vulnerability, particularly on neurogenesis, and compensatory responses to deprivation. Despite the abundance of empirical data, a theoretical framework in which to understand the many sequelae of naris occlusion on olfaction has been elusive. This paper focuses on recent data, new theories, and underappreciated caveats related to the use of this technique in studies of olfactory plasticity.

It has been known for more than 40 years that images fade from perception when they are kept at the same position on the retina by abrogating eye movements. Although aspects of this phenomenon were described earlier, the use of close-fitting contact lenses in the 1950s made possible a series of detailed observations on eye movements and visual continuity. In the intervening decades, many investigators have studied the role of image motion on visual perception. Although several controversies remain, it is clear that images deteriorate and in some cases disappear following stabilization; eye movements are, therefore, essential to sustained exoptic vision. The time course of image degradation has generally been reported to be a few seconds to a minute or more, depending upon the conditions. Here we show that images of entoptic vascular shadows can disappear in less than 80 msec. The rapid vanishing of these images implies an active mechanism of image erasure and creation as the basis of normal visual processing.J. E. Purkinje (1) was the first to describe the rich variety of perceptual phenomena that arise from objects within the eye (called entoptic images; see also refs. 2-5). As can be readily demonstrated with an ordinary penlight, a source of illumination applied to the sclera through the closed eyelid will, when moved, elicit a striking image created by the shadows of the larger retinal vessels (Fig. 1). A much more detailed entoptic image of retinal vessels is obtained by illuminating the pupil with a point source of light, as described by Helmholtz (ref. 3; see also ref. 6). When light is presented through a pinhole held at the focal point of the eye, the cornea and lens collimate the rays, which, therefore, cast well-defined shadows of the foveal capillaries onto the underlying retina (Fig. 2). Because of their close and constant relationship to the photoreceptor sheet, such shadows can move only slightly across the retina compared with exoptic images, and, like other stabilized images, disappear when their movement is stopped. Entoptic vascular shadows, therefore, provide a simple means of studying the effect of retinal image motion on the continuity of vision, a relationship that remains controversial despite several decades of study (10)(11)(12)(13)(14)(15)(16)(17).To determine how long these entoptic images persist in the absence of motion, we constructed two devices that translated a light source to produce moving shadows of the retinal vessels that could be readily stilled. To observe the larger vessels, a light guide was held in a conical collar that was moved back and forth in the horizontal plane by an oscillating motor (Fig. 1A).When the collar was drawn gently across the closed eyelid, the shadows of the major retinal vessels and their branches (save the capillaries) were easily seen. The second apparatus moved a smaller light guide back and forth over a similar horizontal path in front of the open eye, allowing visualization of the foveal capillary shadows (Fig. 2). Both devices were i...