Orientation Preference Maps Research Articles

Topological analysis of point singularities in stimulus preference maps of the prim ary visual cortex

A large population of neurons in the primary visual cortex optimally respond to the orientation and phase of a grating stimulus in luminance. I demonstrate here that the topology of the stimulus space spanned by these parameters is equivalent to that of the Klein bottle, which has a characteristic feature that there is no distinction between the inside and outside of the bottle. The assumption that these stimulus parameters are continuously arranged almost everywhere on the visual cortical surface enables us to map from a loop on the cortical surface to a loop on the Klein bottle. This leads to a systematic categorization of possible point singularities in the arrangements of the optimal orientation and phase in the cortex. Two types of point singularities have been observed in the orientation preference map, according to clockwise or counterclockwise rotation in optimal orientation around the points. The present analysis predicts that each type of orientation centre is subdivided into two types, around which neurons exhibit separately ONcentre and OFF-flank or OFF-centre ON-flank receptive fields. It is also predicted that point singularities about the optimal phase are allowed to exist on the cortical surface. Finally, these predictions are tested by computer simulation based on the author’s thermodynamic model for neural network selforganization

Neural network model for the coordinated formation of orientation preference and orientation selectivity maps.

Earlier models for the self-organization of orientation preference and orientation selectivity maps are explicitly designed to reproduce the functional structures observed in cortical tissue. They mostly use formal though biologically motivated implementations and artifical assumptions to achieve this result. In particular, orientation selective cells are usually encoded by doubling the orientation preference angle, which introduces an ad hoc 180\ifmmode^\circ\else\textdegree\fi{} symmetry to the models. This symmetry is then reflected by the emerging \ifmmode\pm\else\textpm\fi{}180\ifmmode^\circ\else\textdegree\fi{} vortices, which parallel physiological findings. In this work a linear feed-forward neural network model is presented that is not designed to reproduce orientation maps but instead is designed to parallel the anatomical architecture of the early visual pathway. The network is trained using a general Hebb-type unsupervised learning rule and uncorrelated white noise as input. Arguments will be given that on average even strong intracortical interactions have only a weak influence on the learning dynamics of the afferent weights. An approximate description of the learning dynamics of these weights is then developed which strongly reduces computational expense without predetermining the receptive field properties, as earlier approaches do. For parameter regimes, where the most stable receptive fields form within the given model network, vortex structures containing singularities and fractures are observed. In addition, for strong lateral interactions, regions of reduced orientation selectivity appear, which coincide with these singularities. Thus, the present model suggests an implicit and biologically plausible coupling mechanism for the coordinated development of orientation preference and orientation selectivity maps.

Reverse occlusion leads to a precise restoration of orientation preference maps in visual cortex.

In the visual system of young kittens, the layout of the cortical maps for ocular dominance and orientation preference converges to an equilibrium state within the first few weeks of life and normally remains largely unchanged. If during the critical period, however, patterned visual experience is restricted to only one eye for a few days, cortical neurons lose their ability to respond to stimulation of the deprived eye. We used the 'reverse occlusion' protocol together with chronical optical imaging to investigate how the profound anatomical changes accompanying monocular deprivation affect the spatial pattern of the cortical orientation preference map. We report here that after 1 week of monocular deprivation, cortical orientation maps for the deprived eye had vanished. But we also discovered that after subsequent reverse occlusion the restored orientation maps were very similar to the original maps. This demonstrates that in spite of functional disconnection of one eye after monocular deprivation, the layout of cortical orientation maps, when re-established for this eye, is not formed from scratch but is strongly influenced by previous experience.

Cortical column design: a link between the maps of preferred orientation and orientation tuning strength?

We demonstrate that the map of the preferred orientations and the corresponding map of the orientation tuning strengths as measured with optical imaging are not independent, but that band-pass filtering of the preferred orientation map at each location yields a good approximation of the orientation tuning strength. Band-pass filtering is performed by convolving the map of orientation preference with its own autocorrelation function. We suggest an interpretation of the autocorrelation function of the preferred orientations as synaptic coupling function, i.e., synaptic strength as a function of intracortical distance between cortical cells. In developmental models it has been shown previously that a Mexican hat-shaped synaptic coupling function (with a shape similar to that of the autocorrelation function) can produce a realistical-looking pattern of preferred orientations. Since optical imaging performs surface averaging, we discuss the possibility that the connection between the two maps is a measurement artifact of optical imaging. Whether this is the case can only be decided by combining electrode penetrations with optical imaging techniques for which we suggest experiments. We present a model for the generation of both maps from a single computational concept. The model is based on inverse Fourier transform of rather simple two-dimensional annulus-shaped spectra which will produce a column structure very similar to real data. Thus, our approach shows that the complex appearance of cortical orientation columns has a rather simple description in the Fourier domain. Our theoretical analysis explains why singularities in the cortex do not have vorticities other than ±1/2, a result which corresponds to recent experimental findings. This study combines the results from several modeling approaches with recently available optical imaging data to construct a model of both aspects (angle and strength) of the cortical orientation column system. This could alter ideas about cortical development if the link between the two maps can be established as a physiological result.

The layout of iso-orientation domains in area 18 of cat visual cortex: optical imaging reveals a pinwheel-like organization

In this study we used optical imaging based on activity-dependent intrinsic signals to determine the distribution of cells responding to gratings of various orientations moving in different directions in area 18 of cat visual cortex. To test directional-selective clustering of neurons, we compared cortical activity maps obtained by stimulation with two gratings of identical orientation but moving in opposite directions. We found those maps to be almost identical, suggesting that neurons are not notably clustered into directionality columns. We also compared activity maps obtained with gratings of different orientations. Each of the orientation maps was similar to the 2-deoxyglucose maps previously reported. Having compiled the information obtained from the different orientations into one "orientation preference map," we found, in contrast to earlier reports, that iso-orientation domains are not elongated parallel bands but are small patches organized in "pinwheels" around points that we refer to as "orientation centers." We furthermore show that the only locations at which orientation preference changes rapidly are these orientation centers and not lines or loops. In addition, this report clarifies that our observations on the functional architecture of cat area 18, although at first sight at variance with earlier observations, are actually fully consistent with them. We therefore propose that in cat visual cortex pinwheel-like patterns of orientation preference form an irregular mosaic of modular units with an average density of 1.2 pinwheels per square millimeter.

Optical imaging of bipolar cortical stimulation.

In order to better understand the degree of cortical activation that occurs during bipolar surface stimulation, the authors stimulated monkey visual cortex while monitoring the degree of activation with optical imaging. Optical imaging of intrinsic signals in monkey visual cortex during visual stimulation resulted in functional maps of ocular dominance and orientation selectivity. After functional maps of ocular dominance and orientation preference were obtained, bipolar surface stimulation was applied to activate just the cortical areas around the bipolar electrodes. Graded responses to changes in the stimulation intensity and duration were found. These findings demonstrate the reliability of bipolar cortical surface stimulation in localizing functional regions of cortex. The area of activation, at least in the region around the bipolar stimulating electrodes, did not appear to activate nearby ocular dominance columns or orientation patches. Intraoperative bipolar surface stimulation continues to be a consistently reliable technique for localizing rolandic cortex and essential language sites.

Orientation selectivity, preference, and continuity in monkey striate cortex

Maps of orientation preference and selectivity, inferred from differential images of orientation (Blasdel, 1992), reveal linear organizations in patches, 0.5-1.0 mm across, where orientation selectivities are high, and where preferred orientations rotate linearly along one axis while remaining constant along the other. Most of these linear zones lie between the centers of adjacent ocular dominance columns, with their short iso-orientation slabs oriented perpendicular, in regions enjoying the greatest binocular overlap. These two-dimensional linear zones are segregated by one- and zero-dimensional discontinuities that are particularly abundant in the centers of ocular dominance columns, and that are also correlated with cytochrome oxidase-rich zones within them. Discontinuities smaller than 90 degrees extend in one dimension, as fractures, while discontinuities greater than 90 degrees are confined to points, in the form of singularities, that are generated when orientation preferences rotate continuously through +/- 180 degrees along circular paths. The continuous rotations through 180 degrees imply that direction preferences are not organized laterally in striate cortex. And they also ensure that preferences for all orientations converge at each singularity, with perpendicular orientations represented uniquely close together on opposite sides. The periodic interspersing of linear zones and singularities suggests that orientation preferences are organized by at least two competing schemes. They are optimized for linearity, along with selectivity and binocularity, in the linear zones, and they are optimized for density near singularities. Since upper-layer neurons are likely to have similarly sized dendritic fields in all regions (Lund and Yoshioka, 1991), those in the linear zones should receive precise information about narrowly constrained orientations, while those near singularities should receive coarse information about all orientations--very different inputs that suggest different perceptual functions.

Surface organization of orientation and direction selectivity in cat area 18

Two-dimensional maps of orientation and direction preference were made in area 18 of the cat's visual cortex using multiple electrode penetrations 150-300 micron apart. The maps were then analyzed by autocorrelation and Fourier transformation. The power spectrum of the orientation map was sharply peaked below the theoretical cutoff frequency for the sampling function (the pattern of electrode penetrations) used to obtain the map. This suggested that it would be possible to interpolate orientation values between the sample points in the cortex. This was done and the resulting fine-grain maps of orientation preference were studied. Empirical testing showed that the interpolated orientation values were accurate to within +/- 30 degrees. Study of the fine-grain maps showed that iso-orientation domains for broad orientation ranges (0 degrees-90 degrees) were branching bands running from an anterolateral to a posteromedial direction across the surface of the cortex with a periodicity of 1.25 +/- 0.13 mm. Domains for smaller orientation ranges (0 degrees-30 degrees) were periodically spaced, but somewhat irregularly shaped patches. The orientation maps contained numerous point singularities where orientation changed discontinuously. These were spaced about 750 micron apart and most were surrounded by a single 180 degrees cycle of orientations. Autocorrelation analysis of the maps of preferred direction revealed local clustering that extended over a distance of 250-300 micron, but spectral analysis failed to reveal any evidence of periodicity. The absence of periodicity was probably due to a relatively large number of 180 degrees reversals in the map of direction preference, which do not affect the continuity of the orientation map and are not sufficiently numerous to destroy local continuity in the direction map. It is shown that the direction map, if it is to be as continuous as possible, must nevertheless contain lines across which direction preference reverses by 180 degrees. These lines run from one orientation singularity to another. Evidence that the direction map approaches this degree of continuity is presented.

Functional topography in cat area 18

Using closely spaced microelectrode penetrations, we have mapped the representation of the visual field and of several functional response properties on the surface of cat area 18. The representation of the visual field was anisotropic, with the magnification factor for vertical visual space being about 2-5 times greater than that for horizontal. The topographic anisotropy was paralleled by an anisotropy in the cortical point-spread function, a measure of the distribution in the cortex of cells with overlapping receptive-field centers. The spread of this distribution (measured as twice the standard deviation) was positively correlated with the magnification factor anisotropy, averaging about 0.6 mm along the mediolateral (M-L) axis and 1.2 mm along the anteroposterior (A-P) axis. Units with similar response properties were clustered across the cortical surface, but different response features were laid out in different ways. For units with orientations within a 90 degrees range, the clusters took the form of branching bands, with a center to center spacing of 1.25 +/- 0.13 mm. These bands ran from postero-medial to anterolateral across the cortical surface, roughly perpendicular to the 17/18 border. Units with similar preferred eye input were laid out in patches without a well-defined direction of elongation, and with a less well-defined periodicity that averaged 1.86 +/- 0.75 mm. Local correlations in direction preference extending over distances of 300 micron were found, together with frequent 180 degrees differences in the direction preferences of units close together. The organization of the map of orientation preference, and the way in which direction selectivity is overlaid on this map, is discussed in more detail in the accompanying paper (Swindale et al., 1987). No obvious structural relationships between the ocular dominance patches and the pattern of iso-orientation domains were observed. There were, however, obvious interrelationships between the topographic map and other functional response properties. The iso-orientation bands ran approximately perpendicular to the direction in which both the point-spread function and magnification factor were elongated. This will have the effect of maximizing the allocation of a full range of orientations by the cortex to each location in visual space.