Two Retinotopic Visual Areas in Human Lateral Occipital Cortex
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13128 • The Journal of Neuroscience, December 20, 2006 • 26(51):13128–13142 Behavioral/Systems/Cognitive Two Retinotopic Visual Areas in Human Lateral Occipital Cortex Jonas Larsson and David J. Heeger Department of Psychology and Center for Neural Science, New York University, New York, New York 10003 We describe two visual field maps, lateral occipital areas 1 (LO1) and 2 (LO2), in the human lateral occipital cortex between the dorsal part of visual area V3 and visual area V5/MTϩ. Each map contained a topographic representation of the contralateral visual hemifield. The eccentricity representations were shared with V1/V2/V3. The polar angle representation in LO1 extended from the lower vertical merid- ian (at the boundary with dorsal V3) through the horizontal to the upper vertical meridian (at the boundary with LO2). The polar angle representationinLO2wasthemirror-reversalofthatinLO1.LO1andLO2overlappedwiththeposteriorpartoftheobject-selectivelateral occipital complex and the kinetic occipital region (KO). The retinotopy and functional properties of LO1 and LO2 suggest that they correspond to two new human visual areas, which lack exact homologues in macaque visual cortex. The topography, stimulus selectivity, and anatomical location of LO1 and LO2 indicate that they integrate shape information from multiple visual submodalities in retinotopic coordinates. Key words: fMRI; homology; human; lateral occipital; retinotopy; V4; visual cortex Introduction and KO are large and functionally heterogeneous cortical regions The primate visual cortex can be subdivided into a number of that are believed to include multiple subregions (Grill-Spector et distinct areas on the basis of retinotopy, functional properties, al., 1999; Hasson et al., 2003; Zeki et al., 2003; Sawamura et al., anatomical connections, and microstructure (Gattass et al., 2005; Tyler et al., 2005a). In the macaque there are at least two 2005). Many of these areas have been described only in nonhu- distinct visual areas between dorsal V3 and MT: dorsal V4 (V4d) man primates (particularly the macaque), but a growing number (Zeki, 1971, 1977; Gattass et al., 1988; Brewer et al., 2002; Fize et have also been identified in humans (Zeki et al., 1991; Watson et al., 2003) and an area that has been called either V4t (Desimone al., 1993; Engel et al., 1994; Sereno et al., 1995; Tootell et al., 1995, and Ungerleider, 1986) or MTc (Tootell and Taylor, 1995). 1997, 1998; DeYoe et al., 1996; Press et al., 2001; Huk et al., 2002; We used functional magnetic resonance imaging (fMRI) to Brewer et al., 2005). Several homologous visual areas can be iden- study the retinotopic organization of human lateral occipital cor- tified in both species, including V1, V2, V3, V3A, and V5/MTϩ. tex. Our data suggest that there are two adjacent retinotopic maps Beyond V3, however, the homology between human and monkey of the contralateral hemifield in the region between dorsal V3 ϩ areas is less certain (Tootell et al., 1997; Smith et al., 1998; Press et (V3d) and V5/MT . In contrast with previous reports, we found al., 2001; Tootell and Hadjikhani, 2001; Brewer et al., 2005; that these maps contained orderly representations of both visual Schluppeck et al., 2005; Silver et al., 2005). field eccentricity and visual polar angle. Unlike macaque V4d and The retinotopic organization in the human lateral occipital V4t, which represent only the lower quadrant, our results indi- cortex between dorsal V3 and V5/MTϩ remains incompletely cated that the two human maps in this region each contained a characterized. A few studies have reported that this region of full hemifield representation, implying that they are not directly cortex exhibits an eccentricity bias, but lacks a clear map of polar homologous to the macaque areas. We propose that these maps angle (Levy et al., 2001; Tootell and Hadjikhani, 2001; Tyler et al., are two new human visual areas, which we have labeled LO1 and 2005b). Functional studies have shown that this region is part of LO2 (for lateral occipital areas 1 and 2). The functional properties the object-selective lateral occipital complex (LOC) (Malach et of LO1 and LO2 suggest they play different but complementary al., 1995; Grill-Spector et al., 1998a; Levy et al., 2001; Hasson et roles in shape recognition. Some of these results have been pub- al., 2003; Kourtzi et al., 2003) and the kinetic occipital region lished previously in preliminary form (Larsson et al., 2006). (KO) (Dupont et al., 1997; Van Oostende et al., 1997). Both LOC Materials and Methods Subjects and scanning sessions Received April 18, 2006; revised Oct. 3, 2006; accepted Oct. 4, 2006. Fifteen experienced subjects participated in this study with written con- This work was supported by National Eye Institute Grants R01-EY11794 (D.J.H.) and R01-EY16165 (Michael sent. Procedures complied with safety guidelines for MRI research and Landy) and a grant from the Seaver Foundation. We thank Alyssa Brewer, Michael Landy, Tony Movshon, Andy Smith, Brian Wandell, and members of the Heeger laboratory for discussion and comments. were approved by the human subjects Institutional Review Board at New CorrespondenceshouldbeaddressedtoJonasLarsson,DepartmentofPsychologyandCenterforNeuralScience, York University. Each subject participated in at least two scanning ses- New York University, New York, NY 10003. E-mail: [email protected]. sions: one to obtain a high-resolution anatomical volume, and another to DOI:10.1523/JNEUROSCI.1657-06.2006 measure the retinotopic maps in visual cortex (see below). Nine subjects Copyright © 2006 Society for Neuroscience 0270-6474/06/2613128-15$15.00/0 participated in an additional session to localize V5/MTϩ and, in seven of Larsson and Heeger • Retinotopy of Human Lateral Occipital Cortex J. Neurosci., December 20, 2006 • 26(51):13128–13142 • 13129 these subjects, we also localized LOC and KO in the same session. Three topic mapping experiments, response phase corresponded to visual field subjects participated in a previous study that measured orientation- location. For the localizer experiments, response phase reflected the selective adaptation in the visual cortex (Larsson et al., 2006). stimulus condition that evoked the larger response (e.g., objects vs scrambled objects). Cortical surface extraction and analysis Inner (gray/white) and outer (pial) cortical surfaces were extracted from Retinotopic mapping high-resolution T1-weighted MR images [magnetization-prepared Retinotopic visual areas were identified by measuring the BOLD fMRI rapid-acquisition gradient echo (MPRAGE); voxel size 1 ϫ 1 ϫ 1 mm] of response in the visual cortex of human observers viewing high-contrast each subject using the public domain software SurfRelax (Larsson, 2001) checkerboard stimuli that gradually traversed the visual field (Engel et al., (www.cma.mgh.harvard.edu/iatr). Surface patches covering the occipital 1994). The polar angle components of the retinotopic maps were mea- cortex (roughly defined as the cortex within 10 cm surface distance from sured using stimuli restricted to a wedge that rotated (clockwise or the occipital pole) of each hemisphere were cut from the inner cortical counter-clockwise) slowly around the fixation point. The radial compo- surface and flattened for visualization of functional data. Calculations of nents were measured using stimuli restricted to a ring that gradually surface area and distance were done on the triangulated mesh represen- expanded from or contracted toward the fixation point. These stimuli tation of the original, folded surface. Mesh distances (number of edges) evoked traveling waves of activity simultaneously in multiple retinotopi- were measured along the folded white matter surface using a flood-fill cally organized visual cortical areas. The temporal phases of the fMRI algorithm. The distances calculated by this procedure are equivalent to responses in each voxel indicated the corresponding visual field location. shortest path distances between pairs of vertices obtained by Dijkstra’s The resulting retinotopic maps were visualized on flattened surface rep- algorithm (Dijkstra, 1959). Mesh distances were converted to millime- resentations of each subject’s occipital cortex. ters by scaling with the average edge length, divided by a heuristic cor- Visual stimuli were presented at 800 ϫ 600-pixel resolution with a rection factor of 1.2. This factor compensated for the overestimation of refresh rate of 60 Hz on an electromagnetically shielded analog NEC2110 distances that result from approximating a smooth surface by a discrete liquid crystal display (LCD). The display was located behind the scanner triangulated mesh. The correction factor was obtained by repeatedly bore at a viewing distance of 150 cm, yielding a viewing angle of ϳ16 ϫ measuring the mesh distance between random pairs of vertices on syn- 12°. (For the one subject scanned with a GE scanner, viewing distance was thetic triangulated parabolic surface patches and dividing this distance by 320 cm, yielding a smaller viewing angle.) Stimuli consisted of a black and the true distance (calculated analytically as the length of the line integral white high-contrast radial checkerboard pattern presented within a between the two vertex coordinates). The correction factor was essen- slowly rotating (clockwise or counter-clockwise, in stepwise increments tially constant for parabolic surfaces with a radius of curvature 8 mm or of 15 angular degrees per TR) wedge aperture or a slowly expanding or larger (similar