Elsevier

NeuroImage

Volume 46, Issue 4, 15 July 2009, Pages 1114-1126
NeuroImage

Parietal regions processing visual 3D shape extracted from disparity

https://doi.org/10.1016/j.neuroimage.2009.03.023Get rights and content

Abstract

Three-dimensional (3D) shape is important for the visual control of grasping and manipulation. We used fMRI to study the processing of 3D shape extracted from disparity in human parietal cortex. Subjects stereoscopically viewed random-line stimuli portraying a 3D structure, a 2D structure in multiple depth planes or a 2D structure in the fixation plane. Subtracting the second from the first condition yields depth-structure sensitive regions and subtracting the third from the second position-in-depth sensitive regions. Two anterior intraparietal sulcus (IPS) regions, the dorsal IPS medial (DIPSM) and the dorsal IPS anterior (DIPSA) regions, were sensitive to depth structure and not to position in depth, while a posterior IPS region, the ventral IPS (VIPS) region, had a mixed sensitivity. All three IPS regions were also sensitive to 2D shape, indicating that they carry full 3D shape information. Finally DIPSM, but not DIPSA was sensitive to a saccade-related task. These results underscore the importance of anterior IPS regions in the processing of 3D shape, in agreement with their proximity to grasping-related regions. Moreover, comparison with the results of Durand, J.B., Nelissen, K., Joly, O., Wardak, C., Todd, J.T., Norman, J.F., Janssen, P., Vanduffel, W., Orban, G.A., 2007. Anterior Regions of Monkey Parietal Cortex Process Visual 3D Shape. Neuron 55, 493–505 obtained in the monkey indicates that DIPSA and DIPSM may represent human homologues for the posterior part of AIP and the adjoining part of LIP respectively.

Introduction

The human parietal cortex is thought to extract three-dimensional (3D) shape representations that can support the ability to manipulate objects both physically (Binkofski et al., 1998, Culham et al., 2003) and mentally (Gauthier et al., 2002). 3D shape can be recovered from binocular disparity, which is allegedly the strongest depth cue, yet little is known about the implication of the human parietal cortex in this process. So far, only a couple of studies (Chandrasekaran et al., 2007, Georgieva et al., 2009) have been devoted to the processing of 3D shape from disparity in the human brain. This stands in sharp contrast to the many studies of simple depth from disparity processing which has received much more attention (Backus et al., 2001, Neri et al., 2004, Preston et al., 2008, Tsao et al., 2003, Tyler et al., 2006). Using textured surfaces curved in depth and an interaction design, Georgieva et al. (2009) found several intraparietal sulcus (IPS) regions to be involved in the extraction of depth structure from stereo: the dorsal IPS anterior (DIPSA), the dorsal IPS medial (DIPSM), the parieto-occipital IPS (POIPS) and ventral IPS (VIPS) regions. Interestingly, these regions had been previously shown to be involved in the extraction of 3D shape from motion (Murray et al., 2003, Orban et al., 1999, Vanduffel et al., 2002) and also from texture (Georgieva et al., 2008, Shikata et al., 2003, Shikata et al., 2008).

The objective of the present study was to further characterize the role of human parietal cortex in the extraction of 3D shape from disparity. To do that, we used connected random lines as stimuli for the fMRI experiment instead of textured surfaces. Indeed, computational studies (Li and Zucker, 2006a, Li and Zucker, 2006b) have shown that the processing of both kinds of stereoscopic stimuli requires different operations, and may thus involve different cortical areas. Some support for this view was provided by a recent imaging study in the monkey (Durand et al., 2007). These authors observed that the anterior part of monkey IPS, including posterior AIP and anterior LIP, was involved in processing depth structure from disparity for both textured surfaces and random lines. On the other hand, posterior IPS, corresponding to CIP (Taira et al., 2000, Tsutsui et al., 2002) or pIPS (Denys et al., 2004) or LOP (Lewis and Van Essen, 2000b), was involved chiefly in the extraction of 3D shape from disparity in random lines. Further differences in the activation pattern elicited by the two stimulus sets were observed in ventral premotor cortex and in anterior STS, both of which were activated by 3D shape from disparity in textured surfaces but not in random lines (Durand et al., 2006, Joly et al., 2007). Hence we followed the strategy of Georgieva et al. (2009) and used exactly the same random-line stimuli as those used by Durand et al. (2007) in the monkey. This allows us to make two predictions with respect to processing of 3D shape from disparity in human parietal cortex. First, we expect an activation corresponding to anterior IPS in the monkey. Given the earlier hypothesis of Orban et al. (2006) that human regions DIPSM and DIPSA correspond to anterior LIP and posterior AIP in the monkey respectively, we expect an involvement of DIPSM and DIPSA in 3D shape from disparity in random lines, as Georgieva et al. (2009) observed for textured surfaces. Second, in posterior IPS, we expect an additional region to be involved. The homology of monkey CIP/pIPS/LOP is less clear (Shikata et al., 2003, Shikata et al., 2008, Tsao et al., 2003), but one indication from the monkey study (Durand et al., 2007) is that such posterior IPS region should exhibit a mixed sensitivity, being involved in the processing of 3D shape as well as of simple depth from disparity.

There is growing evidence from monkey studies that the two components of the anterior IPS region involved in 2D and 3D shape processing, anterior LIP and posterior AIP, have different single cell properties (Janssen et al., 2008, Lehky and Sereno, 2007, Murata et al., 2000, Sereno and Maunsell, 1998, Srivastava et al., 2006, Srivastava et al., 2007). This is not surprising, as LIP and AIP are supposedly involved in the control of different effectors: the control of the hand in grasping and manipulation for AIP and the control of the eye and attention for LIP (Andersen et al., 1990, Gnadt and Andersen, 1988, Gottlieb et al., 1998, Murata et al., 2000, Sakata et al., 1995, Snyder et al., 1997, Taira et al., 1990). It is therefore important to distinguish between these two regions and one obvious difference is the activation by saccades, which has been used as an indicator of LIP/AIP boundary (Borra et al., 2008, Luppino et al., 1999). Indeed, imaging studies in monkeys (Baker et al., 2006, Koyama et al., 2004) have shown that LIP is activated by saccades, and Durand et al. (2007) showed that the anterior limit of the saccade activation in IPS corresponds closely to the boundary between LIP and AIP. Therefore the present study used exactly the same saccade task as the Durand et al. study and made the additional prediction, derived from the Orban et al. (2006) hypothesis, that in humans DIPSM, but not DIPSA should be activated in the saccade task.

Thus, in the present experiments we scanned a large group of human subjects with established stereo vision and submitted them to three experiments that were the exact replications of those performed by Durand et al. (2007) in the monkey. First we scanned subjects as they tracked the orientation of a small bar in the fixation plane while we presented the random-line stimuli portraying either a 3D structure, a 2D structure in different depth planes or a 2D structure in the fixation plane. The fixation task ensures that the eyes remain converged on the fixation plane, while we investigated the processing of depth structure from disparity. In a second experiment we tested the subjects with the intact and scrambled images of objects (Denys et al., 2004, Kourtzi and Kanwisher, 2000) to assess sensitivity to 2D shape. In this experiment, subjects fixated a small target while the stimuli were presented, as did the monkeys in the Durand et al. (2007) study. However, an earlier study performed in both species with the same stimuli has shown that introducing a task similar to that used in the first experiment yielded equivalent results (Denys et al., 2004). Regions activated in common in these two experiments are sensitive to both 2D shape and depth structure and can therefore be considered to be involved in the processing of the full 3D shape of objects. Finally, in a third experiment subjects performed the saccade task of Durand et al. (2007).

While the main objectives of the present study were related to the 3D shape processing in human parietal cortex, they also provide additional information about possible homologies between human and monkey parietal cortex. This topic has received considerable interest recently (Binkofski et al., 1998, Bremmer et al., 2001, Culham and Valyear, 2006, Grefkes and Fink, 2005, Grefkes et al., 2002, Hagler et al., 2007, Koyama et al., 2004, Orban et al., 2006, Sereno et al., 2001, Simon et al., 2002, Tsao et al., 2003). Unlike previous studies however, this is the first time that multiple functional tests are compared using parallel imaging of both species. Earlier parallel imaging studies (Denys et al., 2004, Koyama et al., 2004, Sawamura et al., 2005, Tsao et al., 2003, Vanduffel et al., 2002) concentrated on a single functional property: 3D shape from motion, position in depth, saccades, 2D shape processing or adaptation.

Section snippets

Subjects

Twenty-seven right-handed subjects (including fourteen females, mean age 22 years, range 19–31 years) with normal or corrected-to-normal vision and no history of neurological or psychiatric disease participated in at least one of the three experiments of the present study (see Experimental designs). We ensured that all the subjects involved in the first experiment perceived stereoscopic depth with the stereo stimuli used in this experiment (on this basis, we excluded two subjects who reported

Sensitivity to depth structure extracted from disparity (first experiment)

In the first experiment, we identified, amongst the cortical regions sensitive to binocular disparity (‘3D structure and 3D position’ > twice ‘Zero disparity’), those sensitive to shape-related information or depth structure (‘3D structure’ > ‘3D position’) and those sensitive to position in depth (‘3D position’ > ‘Zero disparity’). Fig. 3 shows the performances in the acuity task for the 20 subjects during scanning. Percentage of correct detections averaged 83.8% across the subjects and ranged from

Discussion

Our results show that, as predicted, human parietal cortex includes two regions involved in the processing of 3D shape from disparity. The anterior region is sensitive to depth structure but not to position in depth. It includes two sites DIPSM and DIPSA that differ in their sensitivity to saccades. The second posterior region has a mixed sensitivity and corresponds to VIPS.

Acknowledgments

The authors are indebted to W. Depuydt, P. DePaep, S Verstraeten and P. Kayenbergh for help with the experiments and to S. Raiguel, and W. Vanduffel for comments on earlier versions of the manuscript. The work was supported by grants FWO G151.04, GOA 2005/18, EF/05/014, EU-project Neurobotics and Fyssen Fundation (J.-B.D).

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    Present address: Centre de Recherche Cerveau et Cognition, UMR 5549, CNRS-UPS, Toulouse, France.

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