A Neural Model of How the Cortical Subplate Coordinates the Laminar Development of Orientation and Ocular Dominance Maps

Air Force Office of Scientific Research (F49620-98-1-0108, F49620-0 1-1-0397); Defense Advanced Research Projects Agency and the Office of Naval Research (N00014-95-1-0409); National Science Foundation (IIS-97-20333); Office of Naval Research (N00014-01-1-0624

The influence of restricted orientation rearing on map structure in primary visual cortex

Visual experience is critical to the development of the structure of the primary visual cortex and, in turn, normal functional vision. The primary visual cortex contains maps of multiple features of the visual input, and these maps are characterised by specific types of geometric relationships. Manipulations of the visual environment during development in animals such as ferrets, cats and monkeys provide an opportunity to probe the rules governing map formation via their effect on these relationships. Here we use a computational model of map formation based on dimension-reduction principles to predict the effect on map relationships of presenting only a single orientation to one eye and the orthogonal orientation to the other eye. Since orientation preference and ocular dominance are now tightly coupled one might expect orientation and ocular dominance contours to lose their normally orthogonal relationship and instead run parallel to each other. However, surprisingly, the model predicts that orthogonal intersection can sometimes be preserved in this case. The model also predicts that orientation pinwheels can migrate from the centre to the borders of ocular dominance columns, and that the wavelengths of the ocular dominance and orientation maps can become coupled. These predictions provide a way to further test the adequacy of dimension reduction principles for explaining map structure under perturbed as well as normal rearing conditions, and thus allow us to deepen our understanding of the effect of the visual environment on visual cortical development

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

Principles underlying the development and organization of feature maps in the visual cortex

Thesis (Ph. D.)--Massachusetts Institute of Technology, Dept. of Brain and Cognitive Sciences, February 2007.This electronic version was submitted by the student author. The certified thesis is available in the Institute Archives and Special Collections.Includes bibliographical references (leaves 139-142).A fundamental question in neuroscience is how sensory information is represented in the brain. In particular, what principles guide the spatial organization of neurons with regard to their receptive field properties, and how is this organization established mechanistically? The visual cortex serves as a model area to address these questions, but whether general principles can explain the layouts of cortical maps, such as those of visual space and of specific response features, remains unresolved. We find that in primary visual cortex of ferret, the layout of each map is inter-dependent with that of the others. First, we find a strong anisotropy in the visual map, such that receptive field positions change more rapidly along one axis of cortex; and importantly, along the axis where visual space changes rapidly, the feature maps of orientation, ocular dominance, and spatial frequency change slowly. Second, orientation, ocular dominance, and spatial frequency maps have local spatial relationships with each other: in areas of cortex where one feature changes rapidly, the other features change more slowly. Each of these relationships are well-explained by a dimension-reduction model of cortex.(cont.) This suggests that the constraints which drive map formation in the model, continuity (representing each feature smoothly across cortex) and coverage uniformity (representing each feature combination to an equal extent), may play a central role in determining the functional organization of visual cortex. To explore the mechanisms giving rise to the map relationships, we alter the expression of one feature map early in development and measure the impact on the layouts of the remaining maps. We find that alteration of the ocular dominance map, due to neonatal monocular enucleation, does not prevent the formation of the orientation and spatial frequency maps, but it does alter their spatial relationships. The highest gradient regions of the spatial frequency map have a stronger tendency to avoid high gradient orientation regions, and the contours of the two maps have a greater tendency to cross orthogonally. The results are consistent with the predictions of a dimension-reduction model for removing a feature map, suggesting that as a result of altered input patterns, the cortex can rearrange over the time scale of development according to a dimension-reduction strategy.by Brandon J. Farley.Ph.D

Genetic determination and layout rules of visual cortical architecture

The functional architecture of the primary visual cortex is set up by neurons that preferentially respond to visual stimuli with contours of a specific orientation in visual space. In primates and placental carnivores, orientation preference is arranged into continuous and roughly repetitive (iso-) orientation domains. Exceptions are pinwheels that are surrounded by all orientation preferences. The configuration of pinwheels adheres to quantitative species-invariant statistics, the common design. This common design most likely evolved independently at least twice in the course of the past 65 million years, which might indicate a functionally advantageous trait. The possible acquisition of environment-dependent functional traits by genes, the Baldwin effect, makes it conceivable that visual cortical architecture is partially or redundantly encoded by genetic information. In this conception, genetic mechanisms support the emergence of visual cortical architecture or even establish it under unfavorable environments. In this dissertation, I examine the capability of genetic mechanisms for encoding visual cortical architecture and mathematically dissect the pinwheel configuration under measurement noise as well as in different geometries. First, I theoretically explore possible roles of genetic mechanisms in visual cortical development that were previously excluded from theoretical research, mostly because the information capacity of the genome appeared too small to contain a blueprint for wiring up the cortex. For the first time, I provide a biologically plausible scheme for quantitatively encoding functional visual cortical architecture by genetic information that circumvents the alleged information bottleneck. Key ingredients for this mechanism are active transport and trans-neuronal signaling as well as joined dynamics of morphogens and connectome. This theory provides predictions for experimental tests and thus may help to clarify the relative importance of genes and environments on complex human traits. Second, I disentangle the link between orientation domain ensembles and the species-invariant pinwheel statistics of the common design. This examination highlights informative measures of pinwheel configurations for model benchmarking. Third, I mathematically investigate the susceptibility of the pinwheel configuration to measurement noise. The results give rise to an extrapolation method of pinwheel densities to the zero noise limit and provide an approximated analytical expression for confidence regions of pinwheel centers. Thus, the work facilitates high-precision measurements and enhances benchmarking for devising more accurate models of visual cortical development. Finally, I shed light on genuine three-dimensional properties of functional visual cortical architectures. I devise maximum entropy models of three-dimensional functional visual cortical architectures in different geometries. This theory enables the examination of possible evolutionary transitions between different functional architectures for which intermediate organizations might still exist

Coordinated optimization of visual cortical maps : 2. Numerical studies

In the juvenile brain, the synaptic architecture of the visual cortex remains in a state of flux for months after the natural onset of vision and the initial emergence of feature selectivity in visual cortical neurons. It is an attractive hypothesis that visual cortical architecture is shaped during this extended period of juvenile plasticity by the coordinated optimization of multiple visual cortical maps such as orientation preference (OP), ocular dominance (OD), spatial frequency, or direction preference. In part (I) of this study we introduced a class of analytically tractable coordinated optimization models and solved representative examples, in which a spatially complex organization of the OP map is induced by interactions between the maps. We found that these solutions near symmetry breaking threshold predict a highly ordered map layout. Here we examine the time course of the convergence towards attractor states and optima of these models. In particular, we determine the timescales on which map optimization takes place and how these timescales can be compared to those of visual cortical development and plasticity. We also assess whether our models exhibit biologically more realistic, spatially irregular solutions at a finite distance from threshold, when the spatial periodicities of the two maps are detuned and when considering more than 2 feature dimensions. We show that, although maps typically undergo substantial rearrangement, no other solutions than pinwheel crystals and stripes dominate in the emerging layouts. Pinwheel crystallization takes place on a rather short timescale and can also occur for detuned wavelengths of different maps. Our numerical results thus support the view that neither minimal energy states nor intermediate transient states of our coordinated optimization models successfully explain the architecture of the visual cortex. We discuss several alternative scenarios that may improve the agreement between model solutions and biological observations

Functional Organization of Visual Cortex in the Owl Monkey

In this study, we compared the organization of orientation preference in visual areas V1, V2, and V3. Within these visual areas, we also quantified the relationship between orientation preference and cytochrome oxidase (CO) staining patterns. V1 maps of orientation preference contained both pinwheels and linear zones. The location of CO blobs did not relate in a systematic way to maps of orientation; although, as in other primates, there were approximately twice as many pinwheels as CO blobs. V2 contained bands of high and low orientation selectivity. The bands of high orientation selectivity were organized into pinwheels and linear zones, but iso-orientation domains were twice as large as those in V1. Quantitative comparisons between bands containing high or low orientation selectivity and CO dark and light bands suggested that at least four functional compartments exist in V2, CO dense bands with either high or low orientation selectivity, and CO light bands with either high or low selectivity. We also demonstrated that two functional compartments exist in V3, with zones of high orientation selectivity corresponding to CO dense areas and zones of low orientation selectivity corresponding to CO pale areas. Together with previous findings, these results suggest that the modular organization of V1 is similar across primates and indeed across most mammals. V2 organization in owl monkeys also appears similar to that of other simians but different from that of prosimians and other mammals. Finally, V3 of owl monkeys shows a compartmental organization for orientation selectivity that remains to be demonstrated in other primates

Insights into activity-dependent map formation from the retinotectal system: a middle-of-the-brain perspective

ABSTRACT: The development of orderly topographic maps in the central nervous system (CNS) results from a collaboration of chemoaffinity cues that establish the coarse organization of the projection and activity-dependent mechanisms that fine-tune the map. Using the retinotectal projection as a model system, we describe evidence that biochemical tags and patterned neural activity work in parallel to produce topographically ordered axonal projections. Finally, we review recent experiments in other CNS projections that support the proposition that cooperation between molecular guidance cues and activity-dependent processes constitutes a general paradigm for CNS map formation