Sparse coding on the spot: Spontaneous retinal waves suffice for orientation selectivity

Ohshiro, Hussain, and Weliky (2011) recently showed that ferrets reared with exposure to flickering spot stimuli, in the absence of oriented visual experience, develop oriented receptive fields. They interpreted this as refutation of efficient coding models, which require oriented input in order to develop oriented receptive fields. Here we show that these data are compatible with the efficient coding hypothesis if the influence of spontaneous retinal waves is considered. We demonstrate that independent component analysis learns predominantly oriented receptive fields when trained on a mixture of spot stimuli and spontaneous retinal waves. Further, we show that the efficient coding hypothesis provides a compelling explanation for the contrast between the lack of receptive field changes seen in animals reared with spot stimuli and the significant cortical reorganisation observed in stripe-reared animals

Optimizing the representation of orientation preference maps in visual cortex

The colorful representation of orientation preference maps in primary visual cortex has become iconic. However, the standard representation is misleading because it uses a color mapping to indicate orientations based on the HSV (hue, saturation, value) color space, for which important perceptual features such as brightness, and not just hue, vary among orientations. This means that some orientations stand out more than others, conveying a distorted visual impression. This is particularly problematic for visualizing subtle biases caused by slight overrepresentation of some orientations due to, for example, stripe rearing. We show that displaying orientation maps with a color mapping based on a slightly modified version of the HCL (hue, chroma, lightness) color space, so that primarily only hue varies between orientations, leads to a more balanced visual impression. This makes it easier to perceive the true structure of this seminal example of functional brain architecture

A theory for the alignment of cortical feature maps during\ud development

We present a developmental model of ocular dominance column formation that takes into account the existence of an array of intrinsically specified cytochrome oxidase blobs. We assume that there is some molecular substrate for the blobs early in development, which generates a spatially periodic modulation of experience–dependent plasticity. We determine the effects of such a modulation on a competitive Hebbian mechanism for the modification of the feedforward afferents from the left and right eyes. We show how alternating left and right eye dominated columns can develop, in which the blobs are aligned with the centers of the ocular dominance columns and receive a greater density of feedforward connections, thus becoming defined extrinsically. More generally, our results suggest that the presence of periodically distributed anatomical markers early in development could provide a mechanism for the alignment of cortical feature maps

Natural scene statistics and the development of the primary visual cortex

Vision is the dominant human sensory modality. Due to the relative ease with which both visual input and visual brain areas can be studied and manipulated, vision has become an important window for enlarging our understanding of the biological sensory processing. Whether artificial or biological, visual processing systems must quickly and efficiently make sense of a large volume of noisy, high-dimensional input. To do this they construct statistical models of the input and utilise these models to efficiently encode visual scenes, detect features and construct a model of the world. In this thesis, we combine the study of natural scene statistics with mathematical models, experimental analysis and visual psychophysics to glean a deeper understanding of the development and function of the mammalian primary visual cortex. We start by considering functional models of receptive field development. We find, in agreement with previous work, that unsupervised learning models trained on natural scenes consistently learn that oriented ``edges'' (Gabor-like filters) are the basic features of natural scenes. The similarity between these filters and primary visual cortex receptive fields is strong evidence that primary visual cortex receptive fields are optimal encoders of visual input. We then significantly extend this work by comparing the prediction of unsupervised learning models with the receptive fields of animals reared in unusual visual environments. We find good agreement, which is evidence that aspects of receptive fields are learned during development, rather than innate. We also show that applying such unsupervised learning models to binocular visual input is not a simple extension of monocular visual input. Inter-ocular correlations change the optimal encoding strategy of binocular input so that it depends on edge orientation. Such functional models intriguingly predict an over-representation of vertically oriented receptive fields. After establishing that oriented edges are the basic feature of natural scenes and the unit of primary visual cortex receptive fields, we consider the statistics of edge arrangements in natural scenes. \citet{Sigman2001} showed that edges in natural scenes over short distances tend to be tangent to a common circle, or co-circular. Edge arrangements which contain a dependence between edge position and orientation may be said to have ``reduced symmetry'' as they lack a symmetry in that the edge position and orientation cannot be rotated independently without modifying the statistics of the arrangement. Co-circularity is one specific type of reduced symmetry. We extend previous work on natural scene co-circularity using a noise-resistant measure of co-circularity we develop and show that natural scenes contain significant co-circularity over extremely large angular distances ($>14\degree$). We also discuss preliminary work into variations in co-circularity statistics by scene type. After establishing that co-circularity is found pervasively in natural scenes, even over large distances, we then return to the structure of the primary visual cortex, but this time at the network level. Previous work has shown that, like edges in natural scenes, V1 orientation preferences maps also have reduced symmetry. However, the details of this dependence between orientation and position have not been examined in detail. We examine cat orientation preference maps from normal, stripe and blind-reared animals and find that, although orientation preference maps do contain reduced symmetry, it is not co-circularity. Moreover, the statistics of reduced symmetry in the maps are not affected by changes to visual input during development. Continuing our examination of V1 network structure, we consider the statistics of lateral connectivity in tree shrew V1. Previous work demonstrated that long-range V1 lateral connections are more common between regions with similar orientation preferences \citep{Bosking1997}. We re-examine this connectivity data using our noise-resistance measure of co-circularity. We find evidence that lateral connections between cells in the primary visual cortex may use two opposite wiring strategies which simultaneously facilitate quick processing of co-circular visual input while increasing the salience of the less expected deviations from co-circularity. Finally, we use the psychophysics of binocular rivalry to test whether co-circularity statistics can affect the functional processing of visual input in humans. We show, using binocular rivalry dominance as an objective measure of salience, that randomly arranged edges are more salient than edge arrangements which contain co-circularity. This is evidence that early visual processing may be functionally utilising edge arrangement statistics. In concurrence with our findings about lateral connections, this may indicate a general strategy of increasing the salience of unexpected visual input. Overall, we demonstrate that early visual coding uses natural scene statistics extensively. We show that oriented edges are a key currency in early visual processing. We find that the arrangement of edges in natural scenes contain rich statistical structure which influences wiring in the primary visual cortex during development and produces measurable changes in the salience of visual stimuli

Imaging plasticity and structure of cortical maps in cat and mouse visual cortex

The study reported in the first part of this thesis utilized optical imaging of intrinsic signals to visualize changes in orientation maps in cat visual cortex induced by pairing a visual stimulus with an intracortical electrical stimulation. We found that the direction of plasticity within orientation maps depends critically on the relative timing between visual and electrical stimulation on a millisecond time scale: a shift in orientation preference towards the paired orientation was observed if the cortex was first visually and then electrically stimulated. In contrast, the cortical response to the paired orientation was diminished if the electrical preceded the visual cortical stimulation. Spike-time-dependent plasticity has been observed in single cell studies; however, our results demonstrate an analogous effect at the systems level in the live animal. Thus, timing-dependent plasticity needs to be incorporated into our conception of cortical map development. While the pairing paradigm induced pronounced shifts in orientation preference, the general setup of the orientation preference map remained unaltered. In order to unravel potential factors contributing to this overall stability, we determined the distribution of plasticity across the cortical surface. We found that pinwheel centers, points were domains of all orientation meet, exhibited less plasticity than other regions of the orientation map. The resistance of pinwheel centers to changes in orientation preference may support maintenance of the general structure of the orientation map. The study that forms the second part employs optical imaging to visualize the retinotopy in mouse visual cortex. We were able to resolve the pattern of retinotopic activity with high precision and reliability in the primary visual cortex (area 17). Functional imaging of the position, size and shape of area 17 corresponded exactly to the location of this area in stained histological sections. The imaged maps were also confirmed with electrophysiological recordings. The retinotopic structure of area 17 showed very low inter-animal variability, thus allowing averaging maps across animals and therefore statistical analysis. These averaged maps greatly facilitated the identification of at least four extrastriate visual areas. In addition, we detected decreases in the intrinsic signal below baseline with a shape and location reminiscent of lateral inhibition. This decrease of the intrinsic signal was shown to be correlated with a decrease in neuronal firing rate below baseline. Both studies were facilitated by the development of a signal analysis technique (part III), which improves the quality of optical imaging data. Intrinsic signal fluctuations originating from blood vessels were minimized based on their correlation with the actual superficial blood vessel pattern. These fluctuation components were then extracted from images obtained during sensory stimulation. This method increases the reproducibility of functional maps from cat, rat, and mouse visual cortex significantly and might also be applied to high resolution imaging using voltage sensitve dyes or functional magnetic resonance

Synapse Plasticity in Motor, Sensory, and Limbo-Prefrontal Cortex Areas as Measured by Degrading Axon Terminals in an Environment Model of Gerbils (Meriones unguiculatus)

Still little is known about naturally occurring synaptogenesis in the adult neocortex and related impacts of epigenetic influences. We therefore investigated (pre)synaptic plasticity in various cortices of adult rodents, visualized by secondary lysosome accumulations (LA) in remodeling axon terminals. Twenty-two male gerbils from either enriched (ER) or impoverished rearing (IR) were used for quantification of silver-stained LA. ER-animals showed rather low LA densities in most primary fields, whereas barrel and secondary/associative cortices exhibited higher densities and layer-specific differences. In IR-animals, these differences were evened out or even inverted. Basic plastic capacities might be linked with remodeling of local intrinsic circuits in the context of cortical map adaptation in both IR- and ER-animals. Frequently described disturbances due to IR in multiple corticocortical and extracortical afferent systems, including the mesocortical dopamine projection, might have led to maladaptations in the plastic capacities of prefronto-limbic areas, as indicated by different LA densities in IR- compared with ER-animals

Supranormal orientation selectivity of visual neurons in orientation-restricted animals

Altered sensory experience in early life often leads to remarkable adaptations so that humans and animals can make the best use of the available information in a particular environment. By restricting visual input to a limited range of orientations in young animals, this investigation shows that stimulus selectivity, e.g., the sharpness of tuning of single neurons in the primary visual cortex, is modified to match a particular environment. Specifically, neurons tuned to an experienced orientation in orientation-restricted animals show sharper orientation tuning than neurons in normal animals, whereas the opposite was true for neurons tuned to non-experienced orientations. This sharpened tuning appears to be due to elongated receptive fields. Our results demonstrate that restricted sensory experiences can sculpt the supranormal functions of single neurons tailored for a particular environment. The above findings, in addition to the minimal population response to orientations close to the experienced one, agree with the predictions of a sparse coding hypothesis in which information is represented efficiently by a small number of activated neurons. This suggests that early brain areas adopt an efficient strategy for coding information even when animals are raised in a severely limited visual environment where sensory inputs have an unnatural statistical structure

VOLTAGE-SENSITIVE DYE IMAGING OF RAT PIRIFORM CORTEX BEFORE AND AFTER KINDLING

To determine the role of inhibitory cells in the propagation of activity in the rat piriform cortex (PC) before and after kindling, we used voltage-sensitive dye imaging technique to follow the membrane potential changes in three layers of the PC after stimulating the lateral olfactory tract (LOT) with beta and gamma frequencies. Stimulation of LOT was followed by propagation of excitatory (in layer II) and inhibitory responses (in layer III) through the PC. Decreasing the inhibition by applying gabazine, a GABAa- receptor antagonist, decreased the inhibitory responses and increased the excitatory responses in the control rats; however, it did not affect the excitatory and inhibitory responses in the kindled rats. Furthermore, cutting the slice below the layer II decreased the both responses. Thus, we concluded that disinhibition of layer III intemeurons is necessary for principle cells firing and kindling can result in seizures by increasing disinhibition in layer III of PC

Diffusion Tensor Imaging Detects Early Cerebral Cortex Abnormalities in Neuronal Architecture Induced by Bilateral Neonatal Enucleation: An Experimental Model in the Ferret

Diffusion tensor imaging (DTI) is a technique that non-invasively provides quantitative measures of water translational diffusion, including fractional anisotropy (FA), that are sensitive to the shape and orientation of cellular elements, such as axons, dendrites and cell somas. For several neurodevelopmental disorders, histopathological investigations have identified abnormalities in the architecture of pyramidal neurons at early stages of cerebral cortex development. To assess the potential capability of DTI to detect neuromorphological abnormalities within the developing cerebral cortex, we compare changes in cortical FA with changes in neuronal architecture and connectivity induced by bilateral enucleation at postnatal day 7 (BEP7) in ferrets. We show here that the visual callosal pattern in BEP7 ferrets is more irregular and occupies a significantly greater cortical area compared to controls at adulthood. To determine whether development of the cerebral cortex is altered in BEP7 ferrets in a manner detectable by DTI, cortical FA was compared in control and BEP7 animals on postnatal day 31. Visual cortex, but not rostrally adjacent non-visual cortex, exhibits higher FA than control animals, consistent with BEP7 animals possessing axonal and dendritic arbors of reduced complexity than age-matched controls. Subsequent to DTI, Golgi-staining and analysis methods were used to identify regions, restricted to visual areas, in which the orientation distribution of neuronal processes is significantly more concentrated than in control ferrets. Together, these findings suggest that DTI can be of utility for detecting abnormalities associated with neurodevelopmental disorders at early stages of cerebral cortical development, and that the neonatally enucleated ferret is a useful animal model system for systematically assessing the potential of this new diagnostic strategy