Whither the hypercolumn?

Abstract

Among the crowning achievements of Hubel and Wiesel's highly influential studies on primary visual cortex is the description of the cortical hypercolumn, a set of cortical columns with functional properties spanning a particular parameter space. This fundamental concept laid the groundwork for the notion of a modular sensory cortex, canonical cortical circuits and an understanding of visual field coverage beyond simple retinotopy. Surprisingly, the search for and description of analogous hypercolumnar organizations in other cortical areas to date has been limited. In the present work, we have applied the hypercolumn concept to the functional organization of the second visual area, V2. We found it important to separate out the original definition of the hypercolumn from other associated observations and concepts, not all of which are applicable to V2. We present results indicating that, as in V1, the V2 hypercolumns for orientation and binocular interaction (disparity) run roughly orthogonal to each other. We quantified the 'nearest neighbour' periodicities for the hypercolumns for ocular dominance, orientation, colour and disparity, and found a marked similarity in the periodicities of all of these hypercolumns, both across hypercolumn type and across visual areas V1 and V2. The results support an underlying common mechanism that constrains the anatomical extent of hypercolumn systems, and highlight the original definition of the cortical hypercolumn.

Figure 1. The Hubel and Wiesel ‘ice cube’ model of primate V1, and a hypothetical analogue in V2

The ice cube model in V1, showing the hypothesized relationship between the orientation hypercolumns and the ocular dominance hypercolumns, running orthogonal to each other and both completing a full cycle in (i.e. having a periodicity of) about 1 mm (Hubel & Wiesel, 1977). Shown with the CO blobs (hatched patches) lying in the centre of the ocular dominance columns (after Livingstone & Hubel, 1984), which may be the locus of V1 colour hypercolumns. In V2, CO staining helped delineate the striped organization, with thick CO stripes containing oriented, disparity cells, thin CO stripes containing colour cells but no net orientation organization, and pale stripes containing columns of oriented cells. Evidence also suggests further functional clustering of other receptive field properties in the stripes of V2. Note that the colour ‘system’ in V1 (the CO blobs) is embedded in the same cortical territory as columns co-representing orientation and ocular dominance, whereas in V2 the colour system (the CO thin stripes) exists as separate cortical territory, apart from the co-representation of orientation and disparity, found in the CO thick stripes.

Figure 2. The relationship between the V1 orientation and ocular dominance maps, as revealed by optical imaging methods

A, a ‘polar’ map of orientation from a portion of primate V1, pseudo-colour coded such that: horizontal/0 deg = blue, 45 deg = red, vertical/90 deg = yellow, 135 deg = green. Iso-orientation contours (thin black lines) have been overlaid on the map, as well as the pattern of the ocular dominance columns from the same cortical sample (thick black lines). B, the ocular dominance map from the same cortical sample, with dark areas responding preferentially to the left eye. The pattern of the iso-orientation contours (thin red lines) from Fig. 2A has also been overlaid on this map, as well as the pattern of the ocular dominance columns (thick black lines). The iso-contour lines for orientation can be seen to often run roughly orthogonal to the ocular dominance bands.

Figure 3. The activation in primate V1 and V2 to a small spot stimulus – an estimate of the cortical point image (point spread function)

Top row, left, activation in V2 reveals the location of the thin stripes (dark patches, red arrows) and thick stripes (light patches, green arrows) due to general activation and disparity cell suppression (see Ts'o et al. 2001). Top row, right, an orientation map confirms the location of the thick and pale stripes as regions of marked orientation organization in V2. Bottom row: V1/V2 activation due to a monocular small spot (0.25 deg) stimulus. A restricted patch of activation approximately 2 mm in extent can be seen in V1. The activation in V2 extends across at least two stripe cycles, 8 mm or more (out of the field of view of the camera). Recall that the V1–V2 border represents the vertical meridian. The spot stimulus was placed on the vertical meridian, yielding the expected reflection of activation areas across the V1–V2 border. The prediction from Hubel & Wiesel (1974) is that a small spot stimulus would activate between 1.5 and 2 mm of V1, matching the observation in this imaging data. However, the same spot stimulus activates a much greater extent of V2. This result is consistent with reduction of retinotopic precision in V2, and with the notion that roughly two ‘point sets’ are required to represent a given point in visual space (just as in V1), but is not consistent with the notion that a V2 point set equals a V2 hypercolumn.

Figure 7. The orthogonal relationship between orientation and disparity maps in a thick stripe region of primate V2

A, disparity maps from two thick stripes in V2, with iso-disparity contours overlaid. B, orientation maps from the same two thick stripes (and adjacent pale stripes) in V2, with iso-orientation contours overlaid. C, the overlaying of the iso-disparity and iso-orientation contour lines. D, post mortem cytochrome oxidase histology of the imaged V2 region, confirming the location of the thick, thin and pale stripes. E, a close-up of the overlaid iso-disparity and iso-orientation contour lines from C, showing the frequent occurrence of roughly orthogonal inter-contour crossing angles, for example, in the upper left-hand corner.

Figure 6. Orientation and disparity maps in primate V1 and V2

A, optical imaging of orientation and disparity in V2, showing the distribution of orientation in the thick and pale stripes of V2 (ORI) and the disparity subcompartments in the thick stripes of V2 (DISP). The non-oriented zones are the thin stripes. The four images on the right are ‘polar’-analysed images of disparity responses at a particular orientation. Disparity presented was orthogonal to axis of orientation. For each orientation, non-disparity selective activation at that orientation is seen as white and suppression as black. Disparity specific activation at that orientation is colour coded according to the scale, with green as near and red as far. Note the paucity of disparity information in the horizontal component image (upper right), which is virtually colourless. In general vertical bars and gratings provide the strongest disparity signal. The DISP image in the lower left is simply the sum of all the component disparity polar images on the right, yielding an image of disparity across all orientations. Yellow regions indicate tuned inhibitory responses (depression of blue/zero disparity). B, electrophysiological confirmation of the disparity maps in A, using multiple single unit recordings, showing the resulting disparity tuning curves at each site. C reiterates the behaviour of the ‘polar’ analysis given the canonical disparity tuning curves: near yields green, far yields red, tuned excitatory near zero yields blue, tuned inhibitory near zero yields yellow, no disparity tuning yields neutral (grey to white).

Figure 5. Construction of orientation and disparity maps from optically imaged responses to orientation and disparity stimuli

A, optically imaged response of a portion of a V2 disparity (thick) stripe to a stimulus set composed of 4 orientations and 7 disparities. Note that for horizontal (0 deg) orientations, each of the 7 disparities yielded a very similar response (no disparity tuning). Whereas for each of the other orientations, the response was quite disparity dependent, particularly around 0 deg disparity. B, orientation sums (top row) are produced by summing these responses across all disparities. Disparity partials (middle row) are computed by applying the polar analysis (see Methods) for each of the 4 orientations, encoding any disparity information in pseudocolour (red = far, blue = zero, green = near). The orientation sums were then used to compute a standard orientation map (Fig. 6A ORI), while the disparity partials were combined to yield a disparity map free of orientation-specific information (Fig. 6A DISP). The disparity partial for each orientation can be seen to the right in Fig. 6A. B, the close ups of the relationship and contribution to disparity at each orientation. The top orientation sums are shown as reflectance maps (dark = activation), whereas the disparity sums are polar activation maps (colour or white = activation).

Figure 4. Optical imaging of orientation in V1 and V2, analysed by the ‘polar’ algorithm

For every pixel, the response to each of four oriented luminance gratings is turned into a vector, with the response signalled as the vector magnitude, and the vector direction is a mapping from orientation to a direction in RGB colour space. The pixel is then assigned an RGB triplet based on the summing of these vectors in RGB space. A, the familiar patterns of orientation maps in V1 and V2 are interspersed with regions showing poor colour saturation, both in V1 and V2 – these cortical sites have poor net orientation tuning. B, the orientation map in A is overlaid with contour lines derived from the ocular dominance map from the same cortical region. C, red crosses have been placed in V1 sites showing poor net orientation tuning. They generally are located in the centres of ocular dominance columns and are likely to correspond to the CO blobs.

Figure 8. A second example of the orthogonal relationship between the orientation maps and disparity maps within a V2 disparity (thick) stripe

Iso-orientation and iso-disparity contours were derived from optical imaging maps of orientation and disparity (as in Fig. 6). The iso-orientation and iso-disparity contours were then overlaid. As can be seen, the two contours often run orthogonal to each other. The plot/histogram above depicts a tabulation of the crossing angles of the iso-orientation and iso-disparity contours. The crossing angle of the two maps is most often close to orthogonal.

Figure 9. The observation that V1 and V2 hypercolumn periodicities may both be approximately 1 mm, at least for orientation and ocular dominance

A, a ‘polar’ orientation map, showing the pattern of the orientation ‘modules’ in the CO thick and pale stripes of V2, as well as some orientation structure in V1. Although the iso-orientation modules in V2 are 6–10 times larger in area than in V1, the ‘near neighbour’ periodicity of like V2 orientation modules (i.e. the V2 orientation hypercolumn periodicity) appears to also be about 1 mm, like orientation and ocular dominance (B) in V1. Note the ellipsoidal shape of many V2 iso-orientation domains.

Figure 11. Population data by functional domain, showing marked similarity between hypercolumn periodicity across all tested classes of functional maps in V1 and V2

Each data point represents the periodicity value obtained from a single cortical sample, for the given functional map and visual area. Filled circles represent median values, pointed to with arrowheads. OD: ocular dominance; Orient: orientation.

Figure 10. Method for quantifying periodicity of functional maps

A, an ocular dominance (OD) map in V1. B and C, the orientation and disparity maps from the same cortical region. The dashed line outlines the region of interest (ROI). D, the unbiased autocorrelogram of the ROI of the OD map. The dashed line outlines the region of the autocorrelogram that was used to compute the periodicity. The redundant portion is discarded due to the antisymmetric nature of the autocorrelogram. E, the FFT of the selected region of the autocorrelogram. The frequency resolution of each pixel is 0.18 cycles mm⁻¹ in the horizontal direction and 0.26 cycles mm⁻¹ in the vertical direction. The centre represents zero cycles mm⁻¹; the peak is located at 1.206 cycles mm⁻¹, corresponding to a period of 0.83 mm. F, a table of periodicities for the OD, orientation and disparity maps from this cortical region is also shown. Scale bars: 1 mm.

Figure 12. Paired periodicity values of two V1 hypercolumn systems, and of V1/V2 orientation hypercolumns

A, scatter plot demonstrating a weak correlation between the two hypercolumn systems, V1 orientation and ocular dominance, in the same cortical sample (and therefore the same animal). Each data point corresponds to an individual cortical sample in which ocular dominance and orientation periodicity values were obtained in V1. B, each data point corresponds to an individual cortical sample in which orientation periodicity values were obtained in both V1 and V2. There appears to be somewhat less of a match between periodicities in V1 vs. V2 in the same animal, than between the two hypercolumn types within V1 in the same animal. The correlation coefficients are also shown.