Elsevier

NeuroImage

Volume 30, Issue 1, March 2006, Pages 228-238
NeuroImage

The specificity of cortical region KO to depth structure

https://doi.org/10.1016/j.neuroimage.2005.09.067Get rights and content

Abstract

Functional MRI studies have identified a cortical region designated as KO between retinotopic areas V3A/B and motion area V5 in human cortex as particularly responsive to motion-defined or kinetic borders. To determine the response of the KO region to more general aspects of structure, we used stereoscopic depth borders and disparate planes with no borders, together with three stimulus types that evoked no depth percept: luminance borders, line contours and illusory phase borders. Responses to these stimuli in the KO region were compared with the responses in retinotopically defined areas that have been variously associated with disparity processing in neurophysiological and fMRI studies. The strongest responses in the KO region were to stimuli evoking perceived depth structure from either disparity or motion cues, but it showed negligible responses either to luminance-based contour stimuli or to edgeless disparity stimuli. We conclude that the region designated as KO is best regarded as a primary center for the generic representation of depth structure rather than any kind of contour specificity.

Introduction

The medial surface of occipital cortex is now well-established as being devoted to the primary visual projection areas V1–3 (Schneider et al., 1993, Engel et al., 1994, Sereno et al., 1995, DeYoe et al., 1996, Tootell et al., 1996, Engel et al., 1997, Hadjikhani et al., 1998, Smith et al., 1998). Consequently, efforts are switching to the analysis of lateral occipital cortex, which is much less strongly retinotopic. Functional MRI studies have identified a cortical area between retinotopic area V3A and motion area V5 in human cortex as particularly responsive to motion-defined borders, designated as the “kinetic occipital” region, KO (Van Oostende et al., 1997, Dupont et al., 1997, Grossman et al., 2000, Kononen et al., 2003). The typical location of this area relative to other activation sites on the lateral occipital cortex is shown in Fig. 1 (see Materials and methods).

Zeki et al. (2003) have questioned the designation of this region as particularly responsive to kinetic borders, finding responses in the same cortical region to static forms presented via color grating borders described as equiluminant with no kinetic component. Indeed, Van Oostende et al. (1997) also reported significant responses in their KO region to stimuli with only luminance borders. Moreover, the chromatic segmentation stimuli used by Zeki et al. (2003) is a type often classed as containing subjective contours. Since the KO region lies within the lateral occipital area shown by Mendola et al. (1999) to respond well to subjective contours of the conventional kind (Kanizsa, 1978), one hypothesis is that the KO region is specialized for the processing of subjective contours in general rather than solely those that are defined kinetically.

A second property in common between the kinetic stimuli and the figure-ground stimuli of Zeki et al. (2003) is that they may both elicit depth segregation. The depth aspect of the stimuli is unremarked by all authors, but it is a strong perceptual component of their visual processing. If the depth structure of the stimuli is the key feature for the activation of the KO region, it raises the prediction that the KO region should be strongly responsive to depth structure generated by binocular disparity cues, in the absence of motion, luminance or subjective contours. Note that this hypothesis focuses on the activity underlying the perceptual experience of depth structure rather than the activation of disparity-specific neurons per se. These two types of neural activity (for disparity and for depth structure) may well be separate aspects of the full circuit for depth processing (Tyler, 1983, Tyler, 1991, Tyler and Kontsevich, 1995).

At first sight, the depth structure hypothesis for activation of the KO region seems incompatible with the consensus result from previous neuroimaging studies in human, that V3A is the region of strongest response for stereoscopic stimuli (Ptito et al., 1993, Gulyas and Roland, 1994, Mendola et al., 1999, Kwee et al., 1999, Backus et al., 2001, Merboldt et al., 2002, Negawa et al., 2002, Gillaie-Dotan et al., 2002, Fortin et al., 2002). However, these studies need to be considered with care because in many of them V3A was defined purely by gyral landmarks that could have included more anterior regions, while those that use retinotopic criteria for V3A ignore activation in neighboring regions such as that corresponding to area KO.

Studies focusing on stereoscopic depth structure, such as Gulyas and Roland (1994), Mendola et al. (1999) and Tsao et al. (2003), report activation in lateral occipital regions that overlap with the typical location of area KO, although no specific identification of the KO region by means of kinetic borders was made. (These studies used random-dot stereograms containing no monocular cues to the stereoscopic shapes, so the stereoscopic structure was purely cyclopean and invisible monocularly.) Furthermore, studies of illusory contour stimuli of the figure-ground type (Hirsch et al., 1995, Mendola et al., 1999, Larsson et al., 1999, Skiera et al., 2000, Andrews et al., 2002), which typically evoke a strong depth percept, show strong activation in lateral occipital areas overlapping with the region defined as KO. In summary, then, studies with stimuli containing depth structure defined by binocular disparity or by other cues typically show pronounced activation of the lateral occipital region corresponding to that identified as KO. The depth structure in these static stimuli was not defined by moving border shear, implying that activation of the KO region is not restricted to motion-defined stimuli.

In a striking comparison, Tsao et al. (2003) found that responses for a cyclopean random disparity checkerboard (a “relative disparity” stimulus whose depth structure was monocularly invisible) were much greater than for the same stimulus with monocular contours occluding the edge structure (compare their Figs. 4 and 9C, right). The implication is that the border segmentation implicit in the stereoscopic checkerboard stimulus is a much stronger component for the lateral occipital activation than are the local disparity changes per se, supporting the suggestion of Zeki et al. (2003) that the key feature for the KO region may be the generic border structure of the disparity contours, although neither study provides a definition for the KO region in terms of a kinetic contour localizer.

Classification of responses in the KO region requires clear definition of nearby retinotopic areas. In specifying the retinotopic landmarks in the region of V3A, for example, there has been a substantial level of disagreement among the various groups. All agree that this retinotopic region has a 180° representation of the contralateral field. However, retinotopic stimuli of rotating wedges reveal strong retinotopic activation in the regions lateral to this dorsal foveal response, implying that there is a second retinotopic region that shares the same foveal confluence, termed V3B (Smith et al., 1998, Press et al., 2001). On the other hand, both Smith et al. (1998) and Zeki et al. (2003) identified V3B as being the same area as KO, on grounds of the similarity of its Talairach localization and responsiveness (without employing retinotopic criteria, however). The Harvard group (Hadjikhani et al., 1998, Malach et al., 1995, Sereno et al., 1995, Tootell et al., 1995, Tootell et al., 1996, Tootell et al., 1997, Tootell et al., 1998a, Tootell et al., 1998b, Tsao et al., 2003) has not recognized a separate V3B area but designates all the cortex lateral to area V3A as being incorporated into the “V4d topolog”, which is defined topologically rather than functionally as the region of cortex connecting the boundaries of V3A, V7 and V5 (hMT+). Thus, their V4d topolog would incorporate both V3B and the KO region, regardless of whether they are separate or coextensive areas.

For the present study, we follow Press et al. (2001) in designating area V3B on the basis of its full retinotopic response characteristics and to define the KO region as lying between retinotopic V3B and the motion area V5 (hMT+) and responding to motion-defined structure in contrast to uniform motion (kinetic contours). It will be seen that, in some hemispheres, this specification defines a KO region adjacent to retinotopic V3B, whereas, in others, it is distinctly separated from V3B. Tootell et al. (1998a) further defined a retinotopic area V7 lying adjacent and dorsal to V3A, including at least a dorsal quadrant, which Press et al. expanded to include a full hemifield.

Having identified this cluster of dorsal retinotopic regions V3A, V3B, V5 and V7, the objective of the study is to evaluate the relative responsiveness of the KO region to a variety of motion, depth and contour stimuli. This goal requires us to distinguish among three hypotheses of the principal function of the KO region, in comparison with its neighboring retinotopic and motion-sensitive regions. These hypotheses are:

  • 1.

    The original concept of Van Oostende et al. (1997) that KO is specialized for motion-defined contours.

  • 2.

    The Zeki et al. (2003) hypothesis that KO is specialized for contours in general.

  • 3.

    The new hypothesis that KO is specialized for encoding depth structure, whether derived from motion cues, figure-ground segregation or binocular disparity.

Section snippets

Stimuli

To determine the response of the KO region to more general aspects of structure, we used a variety of stimuli corresponding with the different components of the kinetic border stimuli in order to test which of its perceptual properties were responsible for the activation of the KO region (Fig. 1). These stimuli were:

  • A.

    a standard kinetic contour localizer consisting of motion-defined contours (Van Oostende et al., 1997), which evoked a strong depth percept of a set of bars standing out in front of

Results

Examples of the definitions of the retinotopic areas and functional areas KO and V5 (hMT+) are shown for three of the seven observers in Fig. 3 at a coherence level of 0.3 (see Materials and Methods). The two left columns depict flattened occipital maps centered near the occipital pole for the left and right hemispheres, oriented as if viewed from the rear of the brain, together with the activation pattern of the rotating wedge stimulus that defines the projection of the retinal meridians. The

Discussion

In the retinotopic hierarchy, the first area to show a consistent response to the disparity structure stimuli was V7 (Table 3). (The patchy activation in areas V3A/B shown in the examples of Fig. 5 did not reach statistical significance in the full analysis but was supported by the individual analysis of Fig. 4.) However, Table 3 indicates that V7 did not show a significantly stronger response to kinetic contours than to any other stimuli, with or without contours. Thus, for the present

Conclusion

The area in lateral occipital cortex that is maximally responsive to kinetic contours also shows strong response to stimuli containing stereoscopic contour structure in the absence of differential motion cues or monocular cues to the structure, but no significant response to unstructured disparity or luminance-based contour stimuli. We therefore conclude that the primary stimulus property activating this areas is the depth structure of the stimuli as opposed to their motion or luminance

Acknowledgments

Supported by NIH/NEI grant EY 7890. Thanks to Anthony M. Norcia for comments on a prior draft of the manuscript.

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